Phylogeny and Subfamilial Classification of the Grasses (Poaceae)

Author(s): Grass Phylogeny Working Group, Nigel P. Barker, Lynn G. Clark, Jerrold I.
Davis, Melvin R. Duvall, Gerald F. Guala, Catherine Hsiao, Elizabeth A. Kellogg, H. Peter
Linder, Roberta J. Mason-Gamer, Sarah Y. Mathews, Mark P. Simmons, Robert J.
Soreng and Russell E. Spangler
Source: Annals of the Missouri Botanical Garden , Summer, 2001, Vol. 88, No. 3
(Summer, 2001), pp. 373-457
Published by: Missouri Botanical Garden Press

Stable URL: https://www.jstor.org/stable/3298585

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 Volume 88 Annals
Number 3 of the
2001 Missouri
Botanical
Garden

PHYLOGENY AND Grass Phylogeny Working Group2,3

SUBFAMILIAL
CLASSIFICATION OF THE
GRASSES (POACEAE)'

ABSTRACT

A large collaborative effort has yiel(led a comprehensive study of the phylogeny and a new suhfanilial classification
of the grass family (Poaceae/Graminieae). The stu(ly was (con(luc(ted on an integratedl andl representative set of 62 grasses
(0.6% of the species and ca. 8% of the genera) plus four outgroup taxa using six molecular sequence (lata sets ({ndhFl,
rbcL, rpoC2, phyB, ITS2, and (;BSSI or waxy), chloroplast restriction site (lata, and( morphological idata. A parsimony
analysis using 2143 informative characters (the comblined analysis) resulted in a single most parsimonious tree of 8752
steps with an RI of 0.556 and bootstrap support of > 90% for more than half of the internal no(les. Significant
relationships that appear consistently in all analyses of all (lata sets and are strongly supported by the combined
analysis include the following: Joinvilleaceae are sister to a monophyletic Poaceae; the earliest (liverging lineages of
the Poaceae are Anomochlooideae, Pharoideae, and Puelioideae, respectively; and( all remaining grasses form a clade.
Multiple monophyletic clades were recovere(, including Bambusoideae s. str., Ehrhartoideae, Pooideae s.l., Aristidoi-
deae, l)anthonioideae, Chloridoideae s. str., Chloridoideae s.l., Panicoideae, Parianeae, Olyreae s. str., Oryzeae, Stipeae,
Meliceae, Lygeum + Nardus, and Molinia + Phragmites. 'The PACCAI) Clade is monophyletic, containing Aristidoi-
deae, Danthonioideae, Arundinoideae s. str., Chloridoideae s.l., Centothecoideae, Panicoideae, Eriachne, Micraira, and
Gynerium. Based on the phylogeny, a classification of 11 previously published subfamilies (Anomochlooideae, Pharo-
ideae, Puelioideae, Bambusoideae, Ehrhartoideae, Pooideae, Aristidoideae, Arundinoideae, Chloridoideae, Centothe-
coideae, and Panicoideae) and 1 new subfamily (Danthonioideae) is proposed. Several changes in the circumscription
of traditionally recognized subfamilies are included. Previous phylogenetic work and classifications are reviewed in
relation to this classification and circumscription, and major characteristics of each subfamily are discussed and de-
scribed. The matrix, trees, and updated data matrix are available at (http://www.virtualherbarium.org/grass/gpwg/
default.htm).
Key words: cereals, classification, DNA sequence data, evolution, grass, phylogeny, Poaceae.

I Work presented here was supported in part by NSF grants DEB-9806584 and DEB-9806877 to LGC, DEB-9727000
to JID, DEB-9419748 and DEB-9815392 to EAK, and BIR-9508467 to SYM. Miwa Kojima prepared the line illustra-
tions of leaf anatomy and spikelets. We thank T. Cope, J. Everett, S. W. L. Jacobs, S. Phillips, S. A. Renvoize, and P.
F. Stevens for helpful comments on the manuscript.
2 This paper is to be cited as authored by the Grass Phylogeny Working Group, or GPWG. The group includes the
following members, listed here in alphabetical order; there is no senior author. Nigel P. Barker, Department of Botany,
Rhodes University, P.O. Box 94, Grahamstown, 6140, South Africa; Lynn G. Clark, Department of Botany, Iowa State
University, Ames, Iowa 50011-1020, U.S.A.; Jerrold I. Davis, L. H. Bailey Hortorium, Cornell University, 462 Mann
Library, Ithaca, New York 14853, U.S.A.; Melvin R. Duvall, Department of Biological Sciences, Northern Illinois
University, DeKalb, Illinois 60115-2861, U.S.A.; Gerald F. Guala, Fairchild Tropical Garden, 11935 Old Cutler Road,
Miami, Florida 33156, U.S.A.; Catherine Hsiao, 6005 Crossmont Court, San Jose, California 95120, U.S.A.; Elizabeth
A. Kellogg, Department of Biology, University of Missouri-St. Louis, 8001 Natural Bridge Road, St. Louis, Missouri
63121, U.S.A.; H. Peter Linder, Institut fur Systematische Botanik, Zollikerstrasse 107, CH-8008, Zurich, Switzerland;

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374 Annals of the
Missouri Botanical Garden

The economic and ecological significance ofand theare somewhat more distantly related to Flagel-
grasses (Poaceae) has led to widespread interest lariaceae
in (Dahlgren et al., 1985; Campbell & Kel-
their evolution and classification. The cereals, logg,
sug- 1987; Linder, 1987; Doyle et al., 1992; Kel-
arcane, bamboos, and forage and weedy grasseslogg are & Linder, 1995; Briggs et al., 2000); this group
of pre-eminent importance in human economy. forms the graminoid clade, a subset of the order
Grasses, which occur in virtually every terrestrial
Poales (APG, 1998). A sister-group relationship be-
habitat, cover as much as one-fifth of the Earth's
tween Poaceae and Joinvilleaceae consistently has
land surface (Shantz, 1954). Long recognized been as a supported (Campbell & Kellogg, 1987; Doyle
"natural" group, the grass family includes approx-
et al., 1992; Clark et al., 1995; Soreng & Davis,
imately 10,000 species in over 700 genera (Dahl- 1998), although rbcL sequence data suggest that
gren et al., 1985; Tzvelev, 1989; Watson & Dall- Joinvilleaceae + Ecdeiocoleaceae is the sister
witz, 1992; Renvoize & Clayton, 1992). Efforts to to Poaceae (Briggs et al., 2000).
clade
produce a comprehensive, formal taxonomic struc- The grass family was recognized as distinctive
ture of the family began over 200 years ago, while
and coherent long before the term monophyly was
serious study of grass evolution began late inever the applied. The fruit (caryopsis) is unique to the
19th century. family, with the outer integument developmentally
The Grass Phylogeny Working Group (GPWG) fused to the inner wall of the ovary. The embryo is
was established in 1996 to (1) combine a series of lateral and, unlike most monocot embryos, is highly
existing data sets to produce a comprehensive phy- differentiated, with clear shoot and root meristems,
logeny for the grass family; (2) focus taxon sampling leaves and vascular system. The pollen, as is typ-
in the development of existing and future data sets; ical for the whole order Poales, has only one ap-
and (3) reevaluate the subfamilial classification of erture, but in grasses the pollen wall lacks scrobi-
the grass family based on the results of the phylo-
culi. In all but the earliest-diverging lineage, the
genetic analyses. We combined and performed cla-
grass spikelet consists of a set of distichous bracts,
distic analyses on eight data sets (one structural,
the basal two empty (glumes) with a series of one
four plastome, and three nuclear) from 62 grasses
to many bracts (lemmas) above, each lemma sub-
and 4 outgroup taxa. The phylogenetic results and
tending a contracted floral axis on which is borne
a revised subfamilial classification of the grass fam-
a presumed prophyll (palea), two or three reduced
ily are presented in this paper.
perianth parts (lodicules), the androecium, and the
REVIEW OF GItASS PHYLOGENY AND gynoecium (see discussion under Spikelet).
CLASSIFICATI)N Although subdivision of the grasses into groups
we today call tribes began in the 18th century (see
Historically, the Poaceae were thought to be re- reviews in Calder6n & Soderstrom, 1980; Gould &
lated to Cyperaceae (Engler, 1892; Cronquist,
Shaw, 1983; Pohl, 1987), works by Brown (1810,
1981) based on floral reduction and chemical char-
1814) represent the earliest attempt to define
acters, but evidence accumulated during the past
groups of tribes, or what we now call subfamilies.
15 years unequivocally shows that the similarities
Brown (1814) divided the grasses into the tribe
are convergent. Phylogenetic studies based on mor-
Paniceae (roughly equivalent to the modern Pani-
phological and molecular characters show that the
coideae) and the tribe Poaceae (roughly equivalent
grasses are most closely related to Joinvilleaceae,
to the Festucoideae of Hitchcock & Chase, 1950)
Restionaceae, Anarthriaceae, and Ecdeiocoleaceae,
based on spikelet compression, articulation, and
floret number. Brown is credited with describing
grass spikelets in detail and recognizing them as
Roberta J. Mason-Gamer, Department of Biological Sci-
branched
ences, University of Idaho, Moscow, Idaho 83844, U.S.A.;
structures, as well as noting the tendency
for the panicoids to grow in warm climates and the
Sarah Y. Mathews, Division of Biological Sciences, Uni-
pooids in cooler climates (Gould & Shaw, 1983;
versity of Missouri-Columbia, 226 Tucker Hall, Columbia,
Missouri 56211, U.S.A.; Mark P. Simmons, The Ohio State
Pohl, 1987). Brown's division of the family into two
University Herbarium, Ohio State University, 1315 Kin-
near Road, Columbus, Ohio 43212, U.S.A.; Robert J. major
So- groups was formalized by Bentham (1878),
reng, Department of Botany, Natural History Museum, was retained by Bentham and Hooker (1883) and
Smithsonian Institution, Washington, D.C. 20560-0166,Hackel (1887), and persisted well into the 20th
U.S.A.; Russell E. Spangler, Department of Ecology, Evo-
century (e.g., Hitchcock, 1935; Hitchcock &
lution, and Behavior, University of Minnesota, 1987 Upper
Buford Circle, St. Paul, Minnesota 55108, U.S.A.
Chase, 1950).
3Author for correspondence: Elizabeth A. Kellogg, Several classifications for the grasses based on
[email protected]. spikelet and inflorescence morphology were pro-

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Volume 88, Number 3 Grass Phylogeny Working Group 375
2001 Phylogeny and Classification of Poaceae

posed in the 19th century (see reviews in Calder6n

of Diarrhena, Nardus, and Lygeum, the remaining
& Soderstrom, 1980; Gould & Shaw, 1983; Camp- seven clusters corresponded to the subfamilies Fes-
bell, 1985; Pohl, 1987), with usually nine or ten tucoideae, Oryzoideae, Arundinoideae, Centothe-
tribes recognized. Some tribes, for example Pani- coideae, Panicoideae, Eragrostoideae, and Bam-
ceae, Andropogoneae, and Bambuseae, contain busoideae. Watson et al. (1985) used the DELTA
largely the same genera now as nearly 200 years system to conduct comprehensive phenetic analy-
ago. Others, such as the various "pooid" tribes, in-
ses of the family, and their character list continues
cluded disparate elements and are now seen as ar- to be developed. Watson and Dallwitz (1992) ini-
tificial. tially recognized five subfamilies and subsequently
Whether explicit or not, a different perspective updated their classification to include seven (Wat-
on the evolution of grasses and relationships withinson & Dallwitz, 1999; http://biodiversity.uno.edu/
the family began to emerge by the end of the 19th delta/grass/www/class.htm); these are Stipoideae,
century. Workers such as Celakovsky (1889), Goe- Pooideae, Bambusoideae, Centothecoideae, Arun-
bel (1895), and Schuster (1910) carefully analyzed dinoideae, Chloridoideae, and Panicoideae. Sub-
spikelet structure and proposed that Streptochaeta, sequent phenetic analyses of immunological data
or something very much like it, was representative (Esen & Hilu, 1989) and plastid DNA reassociation
of the most primitive grasses. With the development (Hilu & Johnson, 1991) were limited in sampling
of leaf anatomical (Duval-Jouve, 1875; Prat, 1932), but in each case produced four major groups.
embryological (van Tieghem, 1897), and cytological Only within the past 15 years have cladistic
(Avdulov, 1931) data, a profound reassessment methods
of been applied to questions of grass phylog-
evolutionary relationships among grasses began. eny and evolution. The first attempt to produce an
Additional data on embryo anatomy (Reeder, 1957, explicit hypothesis of relationships was the mor-
1961, 1962), starch grains (Tateoka, 1962), lodi- phological phylogeny of Kellogg and Campbell
cules (Jirisek & Jozifova, 1968; Guedes & Dupuy, (1987), who analyzed 33 characters scored for vir-
1976), and leaf anatomy (Brown, 1958; Metcalfe, tually all grass genera. The pooids (including Sti-
1960) accumulated and were also incorporated into peae), Panicoideae, Chloridoideae, and Bambuso-
evolutionary and classification schemes. Several ideae were consistently monophyletic in their
classification systems were published in the 20th analyses, but Arundinoideae were polyphyletic, and
century (e.g., Roshevits, 1937, 1946; Tateoka, the pooid clade formed the basal lineage in the
1957; Prat, 1960; Stebbins & Crampton, 1961; family. Bambusoideae s.l. (including herbaceous
Jacques-Felix, 1962; Caro, 1982; Clayton & Ren-tribes such as Anomochloeae, Phareae, Strepto-
voize, 1986; Tzvelev, 1989; Renvoize & Clayton, chaeteae, and Streptogyneae) were interpreted as
1992; Watson & Dallwitz, 1992); major ones thatmonophyletic based on the presence of arm and
are global in scope are compared in Table 1. The fusoid cells; several tribes often included in the
number of subfamilies recognized ranged from 2tra(litional Bambusoideae were placed in other
(Tzvelev, 1989) to 13 (Caro, 1982). All but the Wat-clades (e.g., Brachyelytreae, Diarrheneae, and
son and Dallwitz (1992) classification, which is Phaenospermatidae in the pooid clade).
avowedly phenetic, were based on presumed evo- Hamby and Zimmer (1988) and Doebley et al.
lutionary relationships. The major change was the (1990) published the first molecular phylogenies for
subdivision of the old Festucoideae (or Pooideae) the family, based respectively on ribosomal RNA
into several subfamilies; Panicoideae were retained and plastid gene rbcL (ribulose 1,5-bisphosphate
almost without modification. Other differences carboxylase/oxygenase, large subunit) sequence
among the major classification systems primarily data. Relatively few taxa were sampled in both
relate to the treatment of Arundinoideae and Bam- studies, but both supported the core Pooideae as
busoideae. Clayton and Renvoize (1986) in partic- well as the group that came to be known as the
ular published a number of diagrams depicting re- PACC clade (Davis & Soreng, 1993), containing
lationships based on their synthesis of knowledge subfamilies Panicoideae, Arundinoideae, Centothe-
at that time. These diagrams have served as a start-coideae, and Chloridoideae.
ing point for much subsequent work. The first extensive application of molecular data
Phenetic analyses of the grass family generallyto grass phylogeny was undertaken by Davis and
found groups consistent with the five or six subfam-Soreng (1993), using plastid DNA restriction site
ilies commonly recognized by the mid 1980s. Hilu variation for 31 taxa representing the six subfami-
and Wright (1982), in a cluster analysis of morpho- lies of Clayton and Renvoize (1986). This study
logical and anatomical data, found eight majormarked the beginning of wider sampling in the tra-
groups with strong support. Except for the cluster ditional Bambusoideae (= Bambusoideae s.l.), long

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 Table 1. Comparison of the major 20th century classification systems of the Poaceae.

Roshevits (1946) Tateoka (1957) Prat (1960) Caro (1982) Wa

Clavton & Renvoize Tzvelev (1989
(1986)

Bambusoideae Pharoideae Bambusoideae Bambusoideae Bambusoideae Bambusoideae Ba

Bambuseae Bambuseae Bambuseae s.l. Bambuseae Bambuseae Bambuseae Ba

Arundinarieae
Shibataeeae
77

77
Dendrocalameae
Melocanneae
Oxytenanthereae
Oryzoideae Olyroideae O

Olyreae Olyreae Olyreae Olyreae Olyreae Olyreae Oly

Parianeae Parianeae Pariana ? Parianeae Parianeae
? 9
In Olyreae In Olyreae Buergersiochloeae

Anomochlooideae

Anomochloeae Anomochloeae Incertae Sedis Anomochloeae Anomochloeae Anomochloeae Anom

Streptochaetoideae
Streptochaeteae Streptochaeteae Streptochaeta Streptochaeteae Streptochaeteae
Streptochaeteae St

Phareae In Olyreae
9 Phareae Leptaspideae Ph

In Bambuseae 9 In Bambuseae In Bambuseae Atractocarpeae Pu

In Bambuseae 9 In Bambuseae In Bambuseae In Bambuseae Gu

Pooideae

See Arundoideae Incertae Sedis 9

Streptogyneae Streptogyneae St
Oryzoideae Pooideae

Oryzeae Oryzeae Oryzeae Oryzeae Oryzeae Oryzeae Or

? 9 Diarrheneae Diarrheneae Dia
See Arundoideae 9
Brachyelytreae Brachyelytreae Br

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 Table 1. Continued.

Phenospermeae See Arundoideae Phaenospermatae Phaenospermatae Ph

9
Phyllorachieae Phyllorachideae Phyllorachideae Ph
Ehrhartoideae

In Oryzeae See Arundoideae Incertae Sedis Ehrharteae Ehrharteae Ehrharteae Eh

Centhostecoideae Centothecoideae

Centotheceae See Arundoideae Incertae Sedis Centhosteceae Centotheceae Centosteceae Ce

Micraireae

Pooideae Festucoideae Festucoideae Pooideae Po

Hordeae Triticeae Hordeae Triticeae Triticeae Tri

Brachypodieae Brachypodieae Br
Bromeae Bromeae Bromeae Br
Festuceae Festuceae Festuceae Poeae Poeae Po
Aveneae Agrosteae Aveneae Aveneae Av
Agrostideae Agrostideae
Phalarideae Phalarideae In Phleeae
In Poeae Ampelodesmeae In
Phleeae Ses
Meliceae See Arundoideae In Festuceae Meliceae Meliceae Me
Brylkinieae Brylkinieae
Monermeae Monermeae Hainardieae 9
In
Stipeae See Arundoideae Stipeae Stipeae Stipeae Se
Nardeae See Arundoideae Incertae Sedis Nardeae Nardeae Se
Lygeae See Arundoideae Incertae Sedis Lygeae Lygeeae Se

Beckmannia

Arundoideae Phragmitiformes Phragmnitoideae Arundinoideae Ar

Stipeae Sti
Ste
Nardeae Na
Lygeae Ly

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 Table 1. Continued.

Arundineae Arundineae Arundineae Arundineae Arundineae Ar

In Aveneae Danthonieae Danthonieae Da
,, ,,

Sp
Cy
Er
Micrairoideae

See Pharoideae Incertae Sedis Micraireae Micraireae Micraireae Mi

Aristidoideae

Aristideae Aristideae Aristideae Aristideae Aristideae A

See Panicoideae Thysanolaeneae Incertae Sedis Thvsanolaeneae Thysanolaeneae In
Unioleae
Coleantheae
Brachyelytreae
Meliceae
Glycerieae
Centotheceae
Streptogyneae
Ehrharteae
Phaenospermeae
Garnotieae
Arundinelleae Arundinelleae

Panicoideae Eragrostoideae Chloridoideae Eragrostoideae Chloridoideae Ch

Thysanolaeneae
In Eragrostideae In Cynodonteae Tr
Pappophoreae Pappophoreae Pappophoreae Pappophoreae Pap
Orcuttieae Or
Chlorideae Chlorideae Chlorideae Cynodonteae Cynodonteae Ch
??

Zoysieae Lappagineae Zoysieae

Spartineae
Eragrosteae In Chlorideae Eragrosteae Eragrostideae

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 Table 1. Continued.

Sporoboleae In Chlorideae Sporoboleae

Leptureae
various isolated
genera

Panicoideae Panicoideae Panicoideae Panicoideae Pa

Steyermarkochloeae See
Steyermarkochloea
9 9
In Eragrosteae Eriachneae In Arundineae See
? 9
Hubbardieae 9
In
In Festuceae Isachneae Isachneae Isachneae Isachneae Isa
Paniceae Paniceae Paniceae Paniceae Paniceae Pa
Boivinelleae Bovinelleae Boivinelleae
,, ,,

Melinideae Melinideae Melinideae

,,

In Paniceae 9 ,?

Anthephoreae
In Paniceae Lecomtelleae 9

9
In Zoysieae
,,

Trachyeae
9 ,,

In Zoysieae Ne
In Melinidae 9
Arthropogoneae In
Arundinelleae See Arundoideae See Phragmitiformes Arundinelleae Arundinelleae Ar
Andropogoneae Andropogoneae Andropogoneae Andropogoneae Andropogoneae An
Maydeae Maydeae
I,,

Maydeae
,,

Ma
various isolated
genera including
Phaenosperma

Incertae Sedis

Anomochloa
Centotheca
Ehrharta
Lygeum, Nardus

Micraira

Streptogyna

Thysanolaena and
other genera

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380 Annals of the
Missouri Botanical Garden

as the
presumed to include the most ancestral elements of monophyly of the core Bambusoideae, in ad-
dition to supporting the PACC and pooid clades.
the grass family. Davis and Soreng's (1993) results
supported an expanded pooid clade, the PACC The topology recovered by Liang and Hilu (1996)
(now PACCAD) clade, and suggested that thefrom tra- analysis of matK (maturase K) sequence data
ditional Bambusoideae were not monophyletic. was similar to the rbcL topologies, with the PACC
Nadot et al. (1994) analyzed sequences of andthe pooid clades sister to each other, and Oryza
sister to that clade and a woody bamboo sister to
plastid gene rps4 (ribosomal plastid small subunit,
protein 4) for 26 genera of grasses. Their sampling
the whole family. By this time, reassessment of sub-
was heavily weighted toward the pooid grasses,familial
but classification was necessary; Clark and
they did include three genera of woody bamboosJudziewicz (1996) resurrected Anomochlooideae
and Zizania and Oryza of the ehrhartoids (ory-and Pharoideae to accommodate the basal lineages
zoids). They recovered both a monophyletic of the family, which could not be retained in a
pooid
clade (including Stipa) and the PACC clade.monophyletic
The Bambusoideae.
bambusoid/oryzoid taxa were paraphyletic and Soreng and Davis (1998) combined a structural
formed a polychotomy with the PACC clade. dataCum-set (including morphological, anatomical,
mings et al. (1994), using sequence data from chromosomal,
the and biochemical characters as well
plastid rpoC2 (RNA polymerase II, [" subunit) as structural features of the chloroplast genome)
gene, sampled only 13 genera, but did derive and aan expanded chloroplast restriction site data
monophyletic PACC clade and a monophyletic set to analyze phylogenetic relationships within the
pooid clade. The rbcL sequence analysis of Barker
grass family. They confirmed the basal positions of
et al. (1995) focused on the subfamily Arundino-
Anomochlooideae and Pharoideae, monophyly of an
expanded Pooideae, monophyly of Panicoideae,
ideae. Both the PACC and pooid clades were shown
Centothecoideae, and Chloridoideae, and polyphyly
to be monophyletic, although the traditional Arun-
of the traditional
dinoideae appeared as polyphyletic. Bambuso- Arundinoideae. The core Bam-
ideae, represente(d by a woody bamboo (Bambusa) busoideae, supported as monophyletic in other
and Ehrhartoideae (Zizania and Oryza), wereanalyses
par- along with the ehrhartoid grasses, ap-
aphyletic to the rest of the family. peared as a set of clades paraphyletic to the [Bra-
Clark et al. (1995) were the first to includechyleytrum
a + (Pooideae + PACC)] clade. Soreng
broad sample of bambusoid and ehrhartoid and Davis (1998) also identified structural syna-
taxa.
Using ndhF (NADH dehydrogenase, subunit pomorphies
F) se- for major clades, including, for exam-
quence data, they confirmed the polyphyly of ple,
theloss of the epiblast and gain of an elongated
traditional Bambusoideae and demonstrated that mesocotyl internode in the PACC clade.
Anomochloa and Streptochaeta, two broad-leaved Barker et al. (1999) used sequences of the grass-
Neotropical forest genera, formed the earliestspecific
di- insert in the chloroplast gene rpoC2 (here-
after referred to only as rpoC2) to study relation-
verging branch of the family, with Pharus, another
broad-leaved tropical forest genus, constitutingships
the among a broad sample of "arundinoid" taxa.
next most basal branch. Their results also con- They were the first to include molecular data on
firmed strong support for monophyly of the such PACCtraditionally arundinoid genera as Centropo-
dia, Merxmuellera, Notochloe, Tribolium, Mona-
clade, an expanded pooid clade (including Stipeae,
Phaenospermatideae, Brachyelytreae, and Diarrhe-chather, Pentaschistis, Prionanthium, Cortaderia,
and Spartochloa. Because Arundinoideae were
neae), a derived, monophyletic core bambusoid
clade (Olyreae + Bambuseae), and the polyphyly
known to be polyphyletic, previous classifications
of the traditional Arundinoideae. They also recov-
were not helpful in placing these genera. rpoC2 se-
ered a weakly supported clade including thequences
core of Anomochloa and Streptochaeta could not
bambusoids, ehrhartoids, and pooids, which be they
aligned with those of other grasses, so their basal
named the BOP clade (here updated to the position
BEP could not be tested. Relationships among
the Bambusoideae, Pooideae s.l., and the PACC
Clade based on nomenclatural priority of Ehrhar-
toideae over Oryzoideae). They concluded that
clade varied depending on the analytical method
and inclusion of phylogenetically informative in-
many features previously used to define the tradi-
tional Bambusoideae, including the presence of
sertion/deletion characters. Consistent with previ-
arm and fusoid cells and pseudopetiolateous leaf
studies, they identified Panicoideae and Chlor-
blades among others, were probable synapomor-idoideae as monophyletic. They showed clearly that
phies for the family. a large clade corresponding to Danthonioideae is
The rbcL study of Duvall and Morton (1996)monophyletic
con- and that this corresponds at least in
firmed the basal placement of Anomochloa, aspart
well
to the clade with haustorial synergids identi-

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Volume 88, Number 3 Grass Phylogeny Working Group 381
2001 Phylogeny and Classification of Poaceae

fled by Verboom et al. (1994). They also showedsistent with certain broad phylogenetic groups (Kel-
that the genus Merxmuellera is polyphyletic, with logg, 1998). Unique combinations of linkage groups
are synapomorphic for subfamilies Pooideae (Moore
one species, M. rangei, most closely related to Cen-
tropodia and the chloridoids. et al., 1995; Gale & Devos, 1998), Panicoideae
Hilu et al. (1999) sequenced the chloroplast (Moore et al., 1995; Gale & Devos, 1998; Wilson
gene matK for 62 species of Poaceae and produced et al., 1999), and Ehrhartoideae (Kennard et al.,
1999). In addition, unique linkages support mono-
a tree that was quite similar to those found in pre-
vious studies. Streptochaeta and Anomochloa werephyly of Triticeae (Devos et al., 1993) and Andro-
the earliest diverging lineages, although paraphy-pogoneae (Wilson et al., 1999).
letic instead of monophyletic. The matK data sup- Phylogenetic analyses of individual molecular
ported a PACC clade and a clade including Pooi- data sets within the last decade have converged on
deae and Bambusoideae. Oryzoideae ( a set of well-supported relationships within Po-
Ehrhartoideae) was sister to the PACC clade, ratheraceae. Changes in the circumscriptions of subfam-
than the pooid/bambusoid clade, but this was ilies,
notand in the number of subfamilies recognized,
strongly supported. clearly are necessary. The GPWG analyses pre-
Zhang (2000) used the intron in the chloroplast sented here provide robust support for the major
gene rpll6 (ribosomal protein 16) to construct cladesa within the grass family, and provide the ba-
phylogeny of the grasses and confirmed (again) sis the
for the first family-wide subfamilial classifica-
early divergence of Anomochloa and Streptochaeta, tion based on an explicit phylogenetic hypothesis.
although his data did not support the monophyly of
the pair. The next branch was Pharus. The MATERIALS
rpll6 ANI) METHODS

data supported a PACC clade and a BEP Clade;

O()RGANIZATION OF THlE CPWC
Puelia olyriformis was sister to the BEP Clade, with
modest bootstrap support. The Grass Phylogeny Working Group was formed
Analyses of nuclear sequence data have provid-
explicitly to combine available (lata on the phylog-
ed results complementary to those obtained foreny
mo-of the grass family an(l to use these (lata to
lecular plastid data sets. Mathews and Sharrock
)rop)ose a new classification. Most contributors had
(1996) and Mathews et al. (2000) sequenced already
loci published papers on grass phylogeny an(d
in the phytochrome gene famlily antl resolved were
a to- invite(l to contri)ute their (lata, both pul)-
lished and unpublished. Each contributor retaine(l
pology similar to that (lerived from IIndtlh sequence
data, although the phytochrome data provided control
sig- over his or her data an(l was free to publish
nificantly stronger support for the B3EP Cladeatthan
any time, but the group agreed that the entire
data set woul(l be published as a single paper. Most
did the ndhF data. Additionally, the basal positions
of Anomochloa, Pharus, and Puelia (as notedofinthe collaboration has been conducted via e-mail,
an(d the entire group has never met in a single
Zhang, 1996) were confirmed. Hsiao et al. (1999)
inferred phylogenetic relationships within theThis may serve as a model for future collab-
place.
grasses based on sequences of the internal tran-
orations in plant systematics.
scribed spacer (ITS) region of nuclear ribosomal A list of taxa was drawn up in 1995 by LGC,
DNA. As in the other studies, Streptochaeta and
JID, and EAK to improve parallel sampling for all
Pharus were resolved as the basal lineages,data andsets (Table 2; Appendix I). This list was cho-
monophyly of the PACC clade and monophyly ofinclude as many of the major lineages in the
sen to
the Pooideae were strongly supported. Unlikefamily
pre- as possible, based on our knowledge from
vious studies, however, some of Hsiao et al.'s previous
(1999) studies. Although sampling of taxa is still
not perfectly parallel, many sequences were gen-
analyses found that the traditional Arundinoideae
were monophyletic. erated for this particular set of taxa. DNA was ex-
Combined analysis of sequence data fromchanged two as necessary among members of the group.
chloroplast genes (ndhF, rbcL) and one nuclear The list was expanded slightly based on results ac-
quired
gene (phytochrome B) provided strong support for during the study.
the placement of Puelia + Guaduella as the next All sequences available at the end of 1997 were
assembled by EAK into a single large data set in
most basal lineage of the family after Anomoch-
looideae and Pharoideae (Clark et al., 2000). NEXUS
These format. The data set was then distributed
results necessitated the description of a newvia e-mail to all participants, who had the oppor-
sub-
family, the Puelioideae. tunity to comment on it. A "final" version of the
Mapping studies of the nuclear genome are datain
set was then distributed. Based on the results
their infancy, but genome rearrangements are ofcon-
the first round of analyses (GPWG, 2000), the

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382 Annals of the
Missouri Botanical Garden

Table 2. Summary of genes and taxa included in the combined analysis. Taxa are listed approximately in the
in which they appear in Figure 1. cp rs = chloroplast restriction sites; GBS = GBSSI; struc. = structural da
composite taxon, represented by sequences from several genera; # = composite taxon, represented by sequence
different species within the same genus (as in Appendix I). For details of species, authorities, origina1 publicat
and GenBank accession numbers, see Appendix I. Merxmuellera m. = Merxmuellera macowanii, Merxmueller
Merxmuellera rangei.

Genus cp rs ndhF phyB rbcL rpoC GBS ITS struc.

Flagellaria x x x x x

Elegia# x x x

Baloskion x x x x

Joinvillea# x x x x x x x

Anomochloa x x x x x x

Streptochaeta# x x x x x

Pharus# x x x x x x

Guaduella x x x

Puelia x x x x

Eremitis x x x x x

Pariana x x x x

Lithachne# x x x x x x

Olyra# x x x x x

Buergersiochloa x x x

Pseudosasa* x x x x x x

Chusquea# x x x x x x x

Streptogynca x x x

Ehrharta# x x x x x x

Oryza x x x x x x x x

Leersia# x x x x x

Phaenosperma x x

Brachyelytrum x x x x

Lygeum x x x x x x x

Nardus x x x x x x

Anisopogon x x x x x x

Ampelodesmos x x x x

Stipa# x x x x x x

Nassella# x x x x X

Piptatherum# x x X X

Brachypodium# x x x x X
Melica# x x x X X X

Glyceria# x x x X X X
Diarrhena# x x x X X
Avena* x x x x x X X
Bromus# x x x x x X X
Triticum* x x x x X X X
Aristida# x x x x x X X

Stipagrostis x x x X X

Amphipogon# x x x x X X
Arundo x x x x X X
Molinia* x x x x x X X

Phragmites x x x x x X X
Merxmuellera m. x x x X X X
Karroochloa x x x X X X
Danthonia# x x x x x X X
Austrodanthonia x x x X X X
Merxmuellera r. x x x X X X

Centropodia x x x X X X

Eragrostis# x x x x x X X
Uniola x x x

Zoysia# x x x

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Volume 88, Number 3 Grass Phylogeny Working Group 383
2001 Phylogeny and Classification of Poaceae

Table 2. Continued.

Genus cp rs ndhF phyB rbcL rpoC GBS ITS struc.

Distichlis X X X

Pappophorum* X X X X
Spartina# X X X X X
Sporobolus# X X X X X
Eriachne# X X X
Micraira# X X X X

Thysanolaena X X X X X X
Gynerium X X X X X
Chasmanthium# X X X X X X X
Zeugites X X
Danthoniopsis# X X X X
Panicum# X X X X X X
Pennisetum# X X X X X X X X
Miscanthus* X X X X X X X X
Zea X X X X X X X

taxon groups. This choice

list was was based on previousex work
danthonioid taxa
(summarized in Kellogg & Linder, 1995) indicating
by JID. Althoug
that these represent the closest relatives of the
were invited
grasses. The results of Briggs et to u
al. (2000) suggest
ment onthat thethe final
Ecdeiocoleaceae should be included in
text, this was
outgroup comparisons not
for the grasses in the future.
text of Within
this paper
the grass family, 62 exemplar species were
JID, andchosen toEAK, wit
represent the commonly recognized sub-
the group. The
families Anomochlooideae, Arundinoideae, Bam- G
maintained by
busoideae, Centothecoideae, GF
Chloridoideae, Ehr-
hartoideae (=Oryzoideae), Panicoideae, Pha-
TAXA
roideae, and Pooideae, as well as species from sev-
eralgen-
The taxa used in this analysis include four genera whose placement was uncertain (Am-
phipogon,
era representing the families Flagellariaceae, Res- Anisopogon, Brachyelytrum, Buerger-
tionaceae (two genera), and Joinvilleaceaesiochloa,
as out-Danthonia, Danthoniopsis, Eriachne,

Table 3. Tree statistics for subsets of the (lata matrix. The percent missing data is the number of cells that are
missing for the particular block when included in the total data matrix, and thus is equivalent to the number of missing
taxa times the total number of informative characters plus missing data within sequences for scored taxa. Chloroplast
r.s. = Chloroplast restriction sites.

Total # # Inf. % Missing

Data set # Taxa characters characters data Length CI RI # Trees

Morphological 66 53 50 16.0 227 0.300 0.690 38,000+

Chloroplast r.s. 45 364 293 42.2 939 0.312 0.569 7
ndhF 65 2210 680 4.7 2894 0.379 0.582 16
phytochrome B 40 1182 417 45.5 1997 0.369 0.522 1
rbcL 37 1344 213 44.8 651 0.448 0.660 1

rpoC2 34 777 150 49.9 374 0.503 0.648 33

GBSSI 19 773 213 71.2 720 0.479 0.504 1
ITS 47 322 127 28.8 745 0.349 0.541 24

cp sequence data 66 4331 1043 25.2 3952 0.399 0.597 8

All cp data 66 4695 1336 26.5 4903 0.381 0.589 3
Nuclear 57 2277 757 51.9 3513 0.382 0.512 8
All molecular 66 6972 2093 33.6 8488 0.378 0.554 6
Combined data 66 7025 2143 33.2 8752 0.375 0.557 1

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 384 Annals of the
Missouri Botanical Garden

Table 4. List of structural characters and states. The first number in parentheses indicates the number of the sa
character in Soreng and Davis (1998), and the second number indicates the number of the same character in Kello
and Campbell (1987); a "-" indicates that the character was not used in one or both of those analyses.

Culm
1 (1;-). Perennating woody culms: 0 = absent; 1 = present.
2 (2;-). Culm internodes: 0 = solid; 1 = hollow.
Leaf
3 (3;-). Leaf sheath margins: 0 = free; 1 = fused for at least 1/4 of length.
4 (4;-). Adaxial ligule type: 0 = membrane (with or without fringe of hairs); 1 = fringe of hairs only.
5 (5;-). Abaxial (contra-) ligule: 0 = absent; 1 = present.
6 (-;-). Leaf blade: 0 = absent; 1 = present.
7 (6;-). Pseudopetiole: 0 = absent; 1 = present.
Spikelet
8 (-;-). Floret with a structure identifiable as a palea, this recognized as present when a flower arises on a contracted
axis above an enshrouding prophyll (or something like it), in the axil of a lemma: 0 = absent; 1 = present.
9 (-;-). Spikelet pairs: 0 = absent; 1 = present.
10 (7;-). Pedicel of spikelet: 0 = absent; 1 = present.
11 (8; 3, 4). Proximal female-sterile florets in female-fertile spikelets: 0 = absent; 1 = present.
12 (9; 6). Number of female-fertile florets per female-fertile spikelet: 0 = two or more; 1 = one.
13 (10;-). Awn or mucro on fertile or sterile lemma: 0 = absent; 1 = present.
14 (-;-). Number of awns: 1 1 awn; 2 = 13-23 awns (unique to Pappophoruzm); 3 3 awns.
15 (11;-). Awn attachment: 0 = terminal / subterminal; 1 = from a sinus; 2 = dorsal.
16 (12; 1). Disarticulation above glumes: 0 = absent; 1 = present.
17 (13;-). Germination flap in lemma: 0 = absent; 1 = present.
Flower
18 (14;-). Lodicules: 0 = absent; 1 = present.
19 (15; 7). Lodicule number: 2 = two; 3 = three.
20 (16;-). Fusion of anterior pair of lodicules: 0 = free; 1 = fused.
21 (17; 8). Distally membranous portion of lodicule: 0 = absent; 1 = present.
22 (18; 9). Lodicule vascularization: 0 = very faint to absent; 1 = prominent.
23 (19; 1(). Inner whorl, posterior stamen: 0 = absent; 1 = present.
24 (19; 10). Inner whorl, anterior stamen pair: 0 = absent; 1 = present.
25 (19; 10). Outer whorl, anterior stamen: 0 = absent; 1 = present.
26 (19; 10). Outer whorl, posterior stamen pair: 0 = absent; 1 = present.
27 (-;-). Anthers tetrasporangiate, dithecal = 0; anthers bisporangiate, monothecal = 1.
28 (20;-). Styles fused at least at base: 0 = absent; 1 = present.
29 (21;-). Number of stigmas: 1 = one; 2 = two; 3 = three; 4 = four.
30 (22;-). Highest order of stigmatic branching present: 1 = simple (unbranched, or with branches comiposed
elongate papillate receptive cells, or with very short branches composed of a few papillate receptive cells, b
latter case the stigmas linear in outline); 2 = primary (branches well developed, composed of series of d
papillate receptive cells, with secondary branches absent or minimally developed, stigmas lanceolate or [broa
secondary (secondary to tertiary branches well developed, branches composed of series of dispersed papillate r
cells).
31 (23;-). Number of locules and ovules per pistil (all three families have one ovule per locule): 1 = oile; 2 = two;
3 = three.
Embryogeny
32 (-;-). Haustorial synergids: 0 = absent; 1 = present.
Fruit and Embryo
33 (24; 11). Hilum: 0 = long-linear, > 1/3 length of grain; 1 = nonlinear, < 1/3 length of grain, elliptical or broader
to punctiform.
34 (25;-). Embryo position and structure: 0 = embedded, simple; 1 = lateral, grass-type.
35 (26; 15). Embryo epiblast: 0 = absent; 1 = present.
36 (27; 16). Embryo scutellar tail: 0 = absent; 1 = present.
37 (28; 17). Embryo mesocotyl internode: 0 = negligible; 1 = elongate.
38 (29; 18). Embryonic leaf margins: 0 = meeting; 1 = overlapping.
39 (30;-). Endosperm lipid: 0 = absent; 1 = present.
40 (31;-). Endosperm starch grain syndromes: 0 = Triticum-type (simple grains only, dimorphic in size, round or
lenticular, free); 1 = Festuca-type (highly compound grains present, with or without simple grains also present); 2 =
Andropogon-type (simple and compound grains both present, the latter consisting of few granules); 3 = Panicum-type
(simple grains only, uniform in size, small to medium, angular or sometimes smooth walled, densely packed); 4 =
Brachyelytrum-type (simple only, large).
Seedling
41 (32; 20). Lamina of first seedling leaf: 0 = absent; 1 = present.

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Volume 88, Number 3 Grass Phylogeny Working Group 385
2001 Phylogeny and Classification of Poaceae

Table 4. Continued.

Vegetative Anatomy
42 (-;-). Differentiation of leaf epidermal cells into long and short (cork) cells: 0 = absent (i.e., cells ? u
entiated); 1 = present (Campbell & Kellogg, 1987).
43 (34; 21). Multicellular microhairs: 0 = absent; 1 = present.
44 (35; 22). Occurrence in multicellular microhairs of a broad, short terminal cell, often with a longer basal
walls of the terminal and basal cells similar in thickness: 0 = absent; 1 = present.
45 (36; 31). Arm cells: 0 = absent; 1 = present.
46 (37;-). Fusoid cells: 0 = absent; 1 = present.
Chromosomes
47 (-;-). Base chromosome number is same as state number except that 0 = 10; 1 = 11; 2 = 12; 3
5 = 19.
Biochemistry
48 (38; 30). Carbon fixation pathway: 0 = C,; 1 = C4 NADP-ME classical-type; 2 = C4 NADP-ME Arist
C4 NAD-ME; 4 = C4 NADP-ME Arundinelleae-type; 5 = C4 NADP-ME Eriachne-type.
49 (39; 30). Carbon fixation PCK: 0 = absent; 1 = present.
Deletion in Phytochrome B
50 (-;-). 3-bp DNA deletion in phytochrome B: 0 = 3-bp DNA present (i.e., non-deleted state); 1
(i.e., deleted state; the deleted codon is at position 402 in the alignment of Mathews et al., 1995).
Chloroplast Genome Structure
51 (40;-). 6.4 kb inversion in the large single-copy region of the chloroplast genome, relative to the gen
in Nicotiana: 0 = absent; 1 = present.
52 (41;-). trnT inversion in the large single-copy region of the chloroplast genome, relative to the gen
in Nicotiana: 0 = absent; 1 = present.
53 (42;-). 15 bp insertion in ndhF at position 101951 of the chloroplast genome of Oryza sativa: 0
present.

Lygeum, Micralira, Nard(is, Pari(t(a, Phaenosper- here, should break up each conglomerate taxon into
ma, Puelia, Streptogyna, 7Thysanolaelna). real species (i.e., exempflar taxa).
For 31 of the terminal taxa in the matrix, all 'he numb)er of taxa was (dictated by the numb)ers
molecular data were taken from a single species; of available sequences in the largest of the original
for an additional 27, data were from two or more data sets (rdh F andt chloroplast restriction sites).
species of the same genus (noted l)y # in Table 2; Recent work on large phylogenies suggests that
Appendix I). In eight cases, however, data from sev- phylogenetic accuracy is improve(d by a very dense
eral genera were combined to create a "conglom- sample of taxa (e.g., Hillis, 1996, 1998; Graybeal,
erate" taxon (asterisks in Table 2). For example, 1998). Producing a large data set with perfectly
although one listed representative of the Andropo- parallel sampling, however, would have required ei-
goneae is Miscanthus, there is no rbcL sequence ther a centralized effort in a single lab, or a formal,
available for that genus. There is, however, a se-
coordinated, and separately funded effort among
quence for Sorghum. Thus the Sorghum sequence multiple labs, rather than the decentralized ap-
for rbcL was combined with the Miscanthus se-
proach used here.
quences for ndhF, creating a fictive taxon, an ap-
proach used previously by Kellogg and Linder
CHARACTE RS
(1995). This assumes that both genera are part of
a monophyletic higher-level group (in this case,
The data matrix included 7025 characters as-
Andropogoneae, which are certainly monophyletic;
sembled from the following sources:
Spangler et al., 1999). The results of such combi-
1. NADH
nations are potentially misleading, in that they as- dehydrogenase, subunit F (ndhF)-
Clark et al. (1995, 2000); Davis et al. (this
sume certain combinations of characters that may
not ever actually occur in a single plant. We feel Spangler et al. (1999).
paper);
2. Ribulose
that the number of characters involved, however, is 1,5-bisphosphate carboxylase/oxygen-
small, and the addition of phylogenetically infor-ase, large subunit (rbcL)-Barker et al. (1995);
mative characters by including the line of data Barker
out- (1997); Doebley et al. (1990); Duvall and
weighs the risk of misleading results. Any subse- Morton (1996).
3. RNA
quent studies, particularly those for which there arepolymerase II, [3" subunit (rpoC2)-Cum-
more than two representatives of taxa combined mings et al. (1994); Barker et al. (1999).

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386 Annals of the
Missouri Botanical Garden

4. Chloroplast restriction sites-Davis and Soreng

different ways the two programs count res
(1993); Soreng and Davis (1998). of polytomies.
5. Phytochrome B (phyB)-Mathews and Sharrock PAUP* analyses used 10 random additi
(1996); Mathews et al. (2000). quences, MULPARS on, TBR branch swa
and MAXTREES set to automatically incr
6. Internal transcribed spacer of the nuclear ribo-
somal RNA (ITS)-Hsiao et al. (1998, 1999).100. Bootstrap analyses (bts) used the full h
7. Granule bound starch synthase I (GBSSI,option,
or 500 or 1000 replicates. Bremer supp
waxy)-Mason-Gamer et al. (1998). breviated here as brs; Bremer, 1988; Kall
8. Morphology-Soreng and Davis (1998, andal., ad-1992; also called decay index, cf. Dono
ditional members of the GPWG, this paper). al., 1992) was also calculated. For tree len
Information on numbers of characters and taxa to 11 steps longer than the shortest tree (up
for each matrix is in Table 3, and the structuralsteps), all trees were saved and the strict c
character list is in Table 4. The morphological computed. Because of memory limitatio
(structural) matrix is in Appendix II. The first method
four of negative constraints (Baum et a
data sets represent the chloroplast genome, andwas
the used to compute higher Bremer suppor
next three the nuclear genome. Five data sets, The search for optimal trees was found to
inefficient with this method and often led to in
ndhF, rbcL, rpoC2, phyB, and GBSSI, are all protein
coding sequences; introns of GBSSI were notsupport
in- values. To minimize this proble
cluded in the alignments. The full data matrixsearch
in- was done with 10,000 random addi
cluded 66 taxa and 7025 characters, for a total of
quences. Even so, the search frequently fou
463,650 cells. The amount of missing data forshorter
the than the negative constraint tree, in
total data set is 33.2% and varies among genes that
and the previous searches had missed som
Computing Bremer support thus took alm
taxa (Table 3). The full data matrix can be obtained
from LGC, JID, EAK, or HPL, or from the GPWG weeks of computer time on a G3. For the t
sented here, we arbitrarily chose a cut-o
website, or at Tree BASE (http://herbaria.harvard.
edu/treebase/index.html). steps, so brs values above that are simply
Alignments were provided by the contributors as "> 34."

except for the ITS data, for which the alignment To assess robustness of the results to choice of
was constructed by EAK, beginning with an initial
markers, each data set was analyzed by itself. The
alignment in ClustalW (Thompson et al., 1994)morphological
and data set was omitted from one anal-
then continuing by eye. It became apparent ysis,that and the chloroplast data were analyzed sepa-
rately, as were the nuclear data. For analyses of
ITS1 could not be aligned reliably across the fam-
ily, so it was omitted from the data set. Later individual
after data sets, PAUP* was set to perform
extensive data exploration, several regions of heuristic
am- searches using maximum parsimony, gaps
biguous alignment were also omitted from ITS2. were coded as missing data, multistate taxa were
coded as uncertain, and starting trees were ob-
Gaps were treated as missing data. A few indels,
identified as phylogenetically informative in tained
anal- by ten random addition sequences, holding
one tree at each step; branch swapping used tree
yses of individual data sets, were coded as binary
characters and included in the structural data ma-
bisection and regrafting (TBR), steepest descent
trix (Appendix II). was not in effect, and MULPARS was in effect.
Bootstrap analyses of individual data sets were
DATA ANALYSIS done to facilitate comparisons with combined anal-
yses. All bootstraps of individual data sets included
Data were analyzed by parsimony 500 bootstrap replicates;
algorithms, as MAXTREES was set to
500 to minimize
implemented in PAUP*4.0 d64 (Swofford, 1998) times
onfor searches.
a Power Macintosh G3, and Nona (Goloboff, 1993)
Analyses conducted with Nona ver. 1.6 (Golo-
on an Intel-chip-based workstationboff,running Win-
1993) used the default settings amb- (clades
dows NT. Data sets were analyzed individually
resolved only if by they have unambiguous support)
JID, LGC, EAK, and HPL to be sure andthat
poly=e-mail
(polytomies allowed). Tree searches in-
transmittal of such a large file had volved
not introduced
1000 Wagner tree initiations using random
any errors (for which we suggest the taxon
term entry sequences, followed by tree bisection
"network-
induced homoplasy"). Numbers ofreconnection
informative (tbr) swapping with up to 20 most-
characters and tree lengths were the same fortrees
parsimonious the retained in each search (hold/
two programs, although in some cases 20, mult*1000);
the number shortest trees retained from the
of equally parsimonious trees differed because
subsearches were ofthen tbr-swapped to completion,

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Volume 88, Number 3 Grass Phylogeny Working Group 387
2001 Phylogeny and Classification of Poaceae

with up to 10,000 trees held in memory (holO000,different from the model specified for sequence
max*). Structural character autapomorphies of ter-data. Calculation of base frequencies and transi-
minals, and synapomorphies of clades, were deter-tion/transversion ratios would be meaningless. Sev-
mined by optimizing the morphological data oneral neighbor-joining analyses were done with mor-
most-parsimonious trees obtained by the various phological and restriction site data omitted, but this
analyses, using Winclada ver. 0.9.99m6.1 (Nixon,also required omitting several taxa for which dis-
2000). Strict-consensus bootstrap frequencies fortances were then undefined because of missing
just the total evidence analysis (see Soreng & Da-
data. By the time data sets and taxa were omitted,
vis, 1998) were computed with Clados ver. 1.9.95 the results were difficult to compare to those of par-
(Nixon, 1993) running Nona (Goloboff, 1993) as asimony algorithms. Several maximum likelihood
daughter process for the tree searches, using a copyanalyses were also undertaken on sequence data
of the data set from which uninformative characters alone. These did not reach completion even after
had been removed (with the "mop" function of Win- three to five days of analysis time. As with the
clada). One thousand bootstrap replicates were con- neighbor-joining analyses, missing data and differ-
ducted, using the same ambiguity and polytomyent models of evolution for the different genes made
settings as in the basic analyses. Each replicate the results of questionable validity.
consisted of 10 random taxon entry sequences fol-
lowed by tbr swapping with up to 10 trees retainedRESULTS
from each subsearch (ho/10, mult* 10), and with
further tbr swapping then conducted on the result- Consensus trees for analyses of the individual
ing trees from the 10 subsearches, with 101 trees data sets are presented in Appendix III-A to H and
held (ho 101, max*). tree statistics in Tables 3 and 5. Note that the taxa
Uninformative characters were excluded for all included are generally selected from more compre-
hensive analyses that have been published else-
analyses, so all tree statistics reported in this paper
(consistency index [CI] and retention index [RI]) where, as described in Materials and Methods.
Many of the trees differed in topology, but in no
reflect only potentially phylogenetically informative
characters. case was a strongly supported group in one tree
Chloroplast and nuclear trees were compared us-contradicted by a strongly supported group in an-
ing the incongruence length difference test (randomother tree. We interpreted this as lack of significant
conflict. Nonetheless, the ILD test indicated signif-
partition test of Farris et al., 1994), as implemented
in PAUP*. They were also compared using simple icant differences between the nuclear and chloro-

inspection, as recommended by Mason-Gamer and plast data sets, between nuclear protein-coding and
Kellogg (1996). To compare tree topologies, con-chloroplast, between ndhF and phyB, and between
straint trees were constructed as necessary in ndhF and rbcL. These differences persisted in most
MacClade (Maddison & Maddison, 1993); these cases even when taxa with conflicting placements
were then loaded, the constraint enforced, and awere removed. In the only exception to this obser-
heuristic search undertaken using the same param-vation, ndhF and phyB were not significantly dif-
eters as in unconstrained searches. ferent if the PACCAD Clade was reduced to Pani-
The combined data were constrained to fit to- coideae, Chloridoideae, and the clade of Molinia
plus
pologies suggested in previous studies by loading a Phragmites. This provides weak evidence that
constraint tree in PAUP* and then searchingdifferences
for in resolution of the PACCAD Clade
the most parsimonious tree compatible with that(Panicoideae, Arundinoideae s. str., Chloridoideae
s.l., Centothecoideae, Aristidoideae, Danthonioi-
constraint tree. Constrained and unconstrained
trees were compared using the Wilcoxon signed
deae) are partly responsible for the significant dif-
ferences. Differences between ndhF and rbcL, how-
ranks test (WSR) as suggested by Templeton (1983)
and implemented by Mason-Gamer and Kellogg ever, are puzzling because both are part of the same
linkage group. Because of the ambiguity of the re-
(1996). Significance values were determined using
a two-tailed test. sults, we did not attempt to do all possible pairwise
The entire data set could not be analyzed with comparisons of trees. Despite the differences in the
neighbor-joining or maximum likelihood algo- data sets, we chose to combine the data in a single
rithms. The inclusion of morphological and restric- analysis. Different histories for the various genes
tion site data with sequences made it nonsensical remain a formal possibility. However, in other in-
to specify a single model of evolution. While a mod- vestigations we have seen that the ILD test may
el could in principle be hypothesized for morpho- return significant differences if there is extensive
logical or restriction site data, it would have to be missing data (as we have in some data sets here)

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 Table 5. Bootstrap support values for subsets of the total data matrix. Numbers of nodes at particular support values are given as fraction
as decimals. Poly = polyphyletic; para = paraphyletic. Anom. = Anomochlooideae; Phar. = Pharoideae; Puel. = Puelioideae. *Panicoideae
excluded then support values are much higher.

Molec. Chloro-
Total data data plast Nuclear Structural ndhF cprs rbcL rpoC
# Nodes 100 27/64 25/64 22/64 2/55 0 23/63 2/43 8/35 2/32 4
(0.42) (0.39) (0.34) (0.04) (0.36) (0.05) (0.23) (0.06) (0.
# Nodes 90-99 9/64 14/64 14/64 12/55 1/64 11/63 8/43 7/35 6/32 1
(0.14) (0.22) (0.22) (0.22) (0.02) (0.17) (0.19) (0.20) (0.19) (
# Nodes 70-89 11/64 8/64 7/64 5/55 4/64 4/63 9/43 6/35 4/32 1
(0.17) (0.13) (0.11) (0.09) (0.06) (0.06) (0.21) (0.17) (0.12) (
Fraction nodes > 70 0.73 0.73 0.67 0.35 0.08 0.59 0.45 0.60 0.37
Poaceae 100 100 100 97 Para 100 98 99 Not tested 96 Not te
Spikelet Clade 100 99 98 87 Para 94 81 98 Not tested 54 N
Bistigmatic Clade 100 100 100 97 <50 100 <50 Not tested Not te
BEP + PACCAD Clade 100 100 99 81 Poly 100 Not tested Para Not tested 75 N
Bambusoideae 97 98 97 Para Poly 100 Para Para Par
Ehrhartoideae 100 100 100 92 Para 98 72 100 51 99 N
Pooideae 100 100 93 95 Para 88 <50 70 88
BEP 71 90 62 50 Para 53 Para Para 56 89
Aristidoideae 100 100 100 84 84 100 Not tested 98 67 Not tested
Chloridoideae 86 83 86 51 Para <50 98 54 63
Panicoideae* 65 Poly Para 63 Para Poly Para 95 93
Danthonioideae 98 97 98 Poly Para 99 Not tested 83 70 Not te
PACC 100 100 99 77 <50 100 95 73 73 90
Arundinoideae s. str. 77 78 <50 Poly Para <50 Not resolved 23 Poly 52
Centothecoideae Para Poly Para Para Poly Para Not tested 64 Para 98

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Volume 88, Number 3 Grass Phylogeny Working Group 389
2001 Phylogeny and Classification of Poaceae

or if a single terminal taxon differs in its placementported at bts 86 (brs 8). A clade corresponding to
(Z. Magombo, pers. comm.). Because of the lack of Arundinoideae s. str.-Arundo, Amphipogon, Mol-
obvious points of conflict between the data sets, and inia, and Phragmites-receives modest support
because of the clear congruence at the deep nodes from this analysis (bts 77, brs 6), but the sister
with which we are concerned, we interpret the sig- relationship of Molinia and Phragmites is well sup-
nificant ILD tests as misleading. ported (bts 100; brs 16). The other major clade (the
Analyses of the complete data set were faster BEP Clade) is less well supported (bts 71; brs 8)
than analyses of many of the individual data sets, and includes Bambusoideae s. str., Ehrhartoideae
as has been found in studies of other large data (= Oryzoideae), and Pooideae. Bambusoideae are
sets (Soltis et al., 1998). For example, a heuristic monophyletic (bts 97; brs 15), as is the clade in-
search of the complete data set in PAUP* on a cluding the herbaceous bamboos (bts 100; brs 18).
Macintosh G3 with 10 random addition sequences Likewise Ehrhartoideae are monophyletic (bts 100;
took 19.6 seconds. brs 24), as are Oryzeae (bts 100; brs > 34). Pooi-
With all data combined, there were 2143 parsi- deae include Brachyelytrum (bts 100; brs 15), and
mony informative characters, which produced amost
sin- nodes within the pooid clade are strongly sup-
gle tree of 8752 steps, consistency index (CI) of
ported.
0.375, and retention index (RI) of 0.557 (Figs. 1 the strong phylogenetic pattern shown by
Despite
and 2). Bootstrap analyses (1000 replicates) indi-
the combined analysis, placement of some taxa re-
cated that 27 branches were supported in 100% mains
of ambiguous. The major uncertainty remains
the bootstrap replicates, 9 branches in 90-99%,
the monophyly of the BEP Clade. As noted earlier
and 11 branches in 70-89% (Table 5). Put another
(GPWG, 2000), it is almost equally parsimonious
way, of 64 internal nodes, slightly more thantohalf
place Pooideae as sister to the PACCAD Clade,
(36) have bootstrap values over 90% and a clear
and this makes evolution of particular morpholog-
majority (47) have values over 70%. Bootstrapical
val-characters more parsimonious. The Pooideae
plus PACCAD group appears in analyses of rbcL
ues were virtually identical whether done using
strict consensus bootstrap in Nona (Goloboff, (Appendix
1993) III-C), chloroplast restriction sites (Ap-
or the frequency-within-replicates bootstrap in III-A), morphology (Appendix III-H), and
pendix
PAUP*4.0 (Swofford, 1998); for comparison ITS (Appendix III-F), whereas the BEP Cla(le is
with
individual analyses, we report the values fromretrieve(l by analyses of nidhF (Appendix III-B),
PAUP*4.0. rpoC2 (Appendix Ill-I)), and phyB (Appendix III-
The analysis of the combined data confirmsE). GBSSI (Appendix III-G) forms a novel topology,
many
results of previous studies and clarifies somein which
rela- neither the PACCAD nor the BEP Cla(les
tionships that were previously ambiguous. The two
is monophyletic. An analysis combining rbcL, chlo-
species of Restionaceae form a clade. Joinvillea
roplastisrestriction sites, ITS, and morphology re-
sister to a monophyletic Poaceae. The three earliest
trieves, not surprisingly, a clade that links the Pooi-
diverging lineages are the Anomochlooideae,deae with the PACCAD Clade. Bootstrap analysis,
Phar-
however,
oideae, and Puelioideae, in that order, together ac- finds that the Pooideae + PACCAD clade
counting for 30 species of grasses. The vast occurs
major-in only 23% of the replicates, although it
appears in 40% if Streptogyna is considered part
ity of extant grasses fall into two distinct lineages.
One of these is the PACC clade (Davis & Soreng,
of the clade. The BEP Clade was not found in any
1993), here called the PACCAD Clade (Panicoi- of the bootstrap partitions.
deae, Arundinoideae s. str., Chloridoideae s.l., Constraining
Cen- the entire data set to place Pooi-
tothecoideae, Aristidoideae, Danthonioideae) deae sister to the PACCAD Clade resulted in a sin-
to re-
flect the inclusion of two additional subfamilies
gle tree eight steps longer than the most parsimo-
within the clade. Within this clade, Panicoideae s. tree. The net change of eight steps, however,
nious
str. (excluding Danthoniopsis) are monophyleticwas
(btsproduced by changes of one or two steps in
94; brs 10), as are the core Paniceae sampled 107
herecharacters from throughout the data set. A Wil-
(bts 100; brs 25) and Andropogoneae (bts 100;coxon
brs signed rank test (Templeton, 1983; Mason-
Gamer & Kellogg, 1996) resulted in a test statistic
32). Other strongly supported groups in the PAC-
CAD Clade correspond to Aristidoideae (bts of 100;
2654; for n = 107, this corresponds to p < 0.406
brs 25) and Danthonioideae (bts 98; brs 15).(two-tailed
The test). This means that we cannot rule out
traditional Chloridoideae are supported at btsthe99possibility that Pooideae are indeed sister to
the PACCAD Clade. This is true even if the mor-
(brs 16), and the clade including the chloridoids
phological characters are excluded (z = 1.146; P
plus Centropodia glauca and Merxmuellera rangei
(Chloridoideae s.l.) is also reasonably well sup-
< 0.254).

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390 Annals of the
Missouri Botanical Garden

118 Flagellaria
136 115 Elegia
136 I 113113 aloskion
94 Joinvillea
106

134

140

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Volume 88, Number 3 Grass Phylogeny Working Group 391
2001 Phylogeny and Classification of Poaceae

Flagellaria
100 I Elegia
>34 Baloskion
Joinvillea
100 Anomochloade
d00 1 5 StreptochaetaJ Anomochlooideae
100 Pharus -Pharoideae
>34 100 Guaduela Pueliodeae
32 - Puelia Puelioideae
1100 100 -- Eremitis
>34 73 4 Pariana
100 4 Lithachne
97 18 34 1 Olyra Bambusoideae
10 36 1 64 Buergersiochloa
10 0 3 6 1 5 628 I Pseudosasa
17 2 2 Chusquea
14 0 | Streptogyna - Incertae sedis
2 l oO{ Ehrharta 7 Ehrhartoideae
24 >34r Oryza
>34 Leersia
53 Phaenosperma
28 1 Anisopogon
I-00 Ampelodesmos
100 71
0 8 977
29 12 60 3Stipa
Nassella
>34 2 Piptatherum
1 93 Brachypodium
no ^ o~94 i Avena
882 96 9 Bromus Pooideae
7 10 >34 Triticum
88 Diarrhena
88 100 Melica
100 >34 E Glyceria
15 100 Lygeum
>34 Nardus
Brachyelytrumn
100 Arstida Aristidoideae
61 25 Stipagrostis A tidodeae
~8 98Q a IMerxmuellera m.
158
1 100 Karroochloa
5 >001 Dant honioideae
Austrodanthonia
100 41 27 Danthonia
20 79 -- Amphipogon
3 7J 7L' Arundo
76 LQ Ar Molinia Arundinoideae
32 9 16 _ Phragmites
3 2 9 8 Merxmuellera r.
3 11 1 Centropodia
27 86 7 100 - Eragrostis
3 8 4 9 0 Uniola(P ChlorUnold
99 4 Pappophorum Chloridoideae
100 Zoysia
1 85 7 196 Spartina
25 4 7 ' Sporobolus
2 Distichlis
Eriachne - Incertae sedis
65 - Thysanolaena
68 3 L- Zeugites Centothecoideae
8 7 3 Chasmanthiumn_
10 ?8 68 8 Gynerium Incertae sedis
20 868 Danthoniopsis
3 65 100 Panicum Panicoideae
2 194 25 Pennisetum
10 O|--00 Miscanthus
32 -Zea
Micraira - ncertae sedis

Figure 2. Same tree as Figure 1, showing percent of bootstrap replicates

Brackets indicate the revised classification for the Poaceae.

Figure 1. Single most parsimonious tree for the grasses and relatives, based on eight sets of data. Length =
8752 steps, CI = 0.375, RI = 0.557. Numbers above branches are numbers of unambiguous changes. Branches are
drawn proportional to length.

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392 Annals of the
Missouri Botanical Garden

The combined analysis places Streptogynafirmly

as resolved by the combined data set, although
both are clearly members of the PACCAD Clade.
sister to Ehrhartoideae, but this result is not strong-
ly supported (bts 40; brs 2). This partly reflects
This almost certainly reflects missing data. In ad-
missing data, in that only ndhF and phyB dition to morphological data, Eriachne is repre-
sequenc-
es are available for Streptogyna, in addition sented only by rbcL and ITS sequences, and Mi-
to mor-
phological data. ndhF places S. americana craira
sister to by ndhF, rpoC2, and ITS. They are both
Ehrhartoideae, whereas phyB places it as isolated
sister to taxa, and in individual analyses fall at the
the entire BEP Clade, and morphological databasefail of other well-supported clades. The position
to resolve its position. of Micraira as sister to the entire PACCAD Clade
The combined data place the woody bamboos, appears only in the combined analysis, and like-
Pseudosasa and Chusquea, in a clade (bts 68; wise brs the position of Eriachne as sister to the Arun-
2), as would be expected from previous studies dinoideae s. str. + Chloridoideae + Aristidoideae
(Zhang, 2000; Zhang & Clark, 2000). The pair+ap- Danthonioideae clade is both novel and poorly
pears monophyletic in chloroplast restriction supported.
site, Bootstrap analysis of the combined data
morphological, and phyB trees. The two are para- set placed Eriachne and Micraira as sisters in 51%
phyletic, however, in trees using rbcL and ndhF, of the 1000 replicates, a position not supported by
the most parsimonious tree.
although this result is not well supported in these
trees. "Pseudosasa" is a composite taxon, made up Aristidoideae and Danthonioideae are both
clearly monophyletic, and each is strongly sup-
of data from several different genera, and this may
also affect its placement in the combined tree.ported by both bootstrap and decay analyses (bts
Phaenosperma and Anisopogon are clearly mem- 100 and 98; brs 25 and 15, respectively). In the
bers of the expanded pooid clade, where theycombinedare tree they appear as sister taxa. The ar-
istidoid/danthonioid clade is not stronlgly support-
placed by all data sets, either singly or in combi-
nation. Their position within the clade, however, ed, however (bts 61; brs 8), and is reflected only in
remains uncertain. They are sister taxa when theallphyB tree. rbcL places Aristidoideae sister to
data are combined, but this result is not stronglyChloridoideae, whereas ndhF and cllloroplast re-
supported (bts 53; brs 1); together they are sister
striction sites put Aristidoideae sister to the rest of
to the Stipeae, also a poorly supported resultthe (btsPACCAD Clade, and ITS places the subfamily
28; brs 1). In ndhF, chloroplast restriction site,sister
and to Amphipogon + Chloridoideae. rpoC2 in-
phyB trees, Anisopogon is placed on a branch thatdicates that Aristidoideae is derived from within
diverges after the Lygeum + Nardus clade, butArundinoideae.
be- ndhF places Danthonioideae sister
to Panicoideae + Centothecoideae, whereas chlo-
fore the rest of the Pooideae (i.e., Stipeae, Meli-
ceae, Diarrhena, Brachypodium, Aveneae,roplast
and restriction sites do not resolve the position
Poeae). ITS places it sister to Aveneae/Poeae,of and
Danthonia. GBSSI retrieves a novel arrangement
rpoC2 places it sister to Stipa. In no case isinthe which Danthonioideae are polyphyletic, but this
placement strongly supported. The positionresult of is not strongly supported and is likely af-
Phaenosperma is based only on ndhF and morpho- fected by skewed taxon sampling in the GBSSI data
set. rpoC2 suggests that Danthonioideae are sister
logical data, and the latter are largely uninformative
about its position. to Amphipogon.
Meliceae are monophyletic in all gene trees andThe relationships of Zeugites, Thysanolaena,
in the combined tree. Their position, however, Chasmanthium, Danthoniopsis, and (ynerium to
varies among the individual gene trees. The com- each other and to the Panicoideae are not resolved
bined tree provides good evidence that Meliceae by this analysis. The entire group is well supported
diverged after Lygeum + Nardus (bts 82; brsas7), monophyletic (bts 87; brs 8), but other relation-
ships are less clear. Only morphological and ndhF
but evidence is weak that it was the next diverging
branch (bts 29; brs 1). Other possible placementsdata are available for Zeugites, so its placement
include sister to Stipeae (ndhF, phyB), sister maytobe affected by missing data.
Diarrhena + Brachypodium + Aveneae/Poeae (cp The morphological data have little effect on the
analysis. When they are omitted, 6 trees are found
restriction sites), sister to a clade of Brachypodium
+ Brachyelytrum + (Lygeum + Nardus) (ITS),inor two islands (length 8488, CI = 0.378, RI =
paraphyletic at the base of the Pooideae (GBSSI).0.554). The topology of the strict consensus (Ap-
The ambiguity cannot be ascribed to missing data,pendix III-K) is similar to that of the combined tree
although additional sampling among early-diverg- except for the position of Zeugites, which is sister
ing Pooideae might be warranted. to Danthoniopsis, and Gynerium, which is sister to
The positions of Eriachne and Micraira arePanicoideae.
not In the consensus of the six trees, the

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Volume 88, Number 3 Grass Phylogeny Working Group 393
2001 Phylogeny and Classification of Poaceae

relationship of Pseudosasa and Chusquea is unre-

Differences appear only in the placement of the
solved, as is the relationship of Phaenosperma andMeliceae, Eriachne, Micraira, Zeugites, and Dan-
Anisopogon, and the position of Meliceae in thethoniopsis, all poorly supported areas of the trees.
pooid clade. These are areas that were poorly sup-
DISCUSSION
ported even in the combined tree, and thus already
known to be ambiguous. The most notable differ-WELL-SUPPORTED CLADES
ence is the increased support for the BEP Clade,
Some relationships appear consistentl
which is supported at a bootstrap value of 90%.analyses of all data sets and are strongly
The number of nodes with support greater than by the combined analysis. Among these ar
90% (Table 5) is somewhat greater without thelowing (in order from the bottom of the tr
structural data, but the overall consistency index is 1. Joinvilleaceae are sister to Poaceae.
not changed appreciably (Table 3). 2. Poaceae are monophyletic.
The results for the entire data set largely reflect 3. The earliest diverging lineage of Poaceae is
the results for the chloroplast data alone. The chlo-
Anomochlooideae (even if Anomochloa and Strep-
roplast data contribute 1336 potentially phyloge- tochaeta prove to be two separate lineages, they
netically informative characters, or about 62% of would still be the two earliest-diverging lineages in
the total. Analysis of these data alone produces the2 family).
trees (length = 4903, CI = 0.381, RI = 0.589) 4. The next diverging lineage is Pharoideae.
that differ only in the relative positions of Phae- 5. The next diverging lineage is Puelioideae.
nosperma and Anisopogon (Appendix III-I). The 6. All remaining grasses form a clade, which ap-
numbers of strongly supported nodes are about the pears to have diversified well after the origin of the
same as for the entire data set (Table 5), and dif-family.
ferences between the chloroplast tree and the entire 7. Bambusoideae s. str., Ehrhartoideae, Pooi-
data set are all in poorly supported areas of the tree deae s.l., Aristidoideae, Danthonioideae, Arundi-
(see below). noideae s. str., Chloridoideae s. str., Chloridoideae
The chloroplast tree is only slightly affected bys.l., and Panic oideae are all monophyletic.
mixing sequence data with restriction site data. If 8. Bambuseae, Parianeae, (lyreae s. str., Ory-
the restriction site data are exclulded so that the zeae, Stipeae, Meliceae, and LygeiLm + Nardus,
data set consists only of ndh F, rbc I, and rpoC2 and Molinia + Phragmnites are all monophyletic.
data, the tree is virtually identical to the chloroplast9. The PACCAI) Clade- now including Pani-
tree except that Pseiidosasa plus Chusquea, an(l coideae, Arundinoideae s. str., Chloridoideae s.l.,
Phaenosperma plus Anisopogon form monophyletic Centothecoideae, Aristidoideae, Danthonioideae,
pairs rather than being paraphyletic (not shown). Eriachne, Micraira, and Gynerium-is monophylet-
Piptaltherum and Nassella are paraphyletic rather ic.

than sisters, and the Meliceae are sister to the coreAs noted in the introduction, all of these
Pooideae rather than to the Stipeae. tionships have been supported by previous
Analysis of only the three nuclear genes (phyB, and none is unique to the combined analys
GBSSI, and ITS) required elimination of nine taxa
vious studies, however, were limited becau
for which nuclear data were not available. The were based on a single gene, a modest num
analysis thus included 57 taxa and 757 characters
morphological characters, and/or a restrict
and found eight trees (length = 3513, CI = ple 0.382,of taxa. Because of the strong support f
RI = 0.512) on one island (Appendix III-J).relationships
The found in the present study, we
nuclear trees were not as well supported a asrevised
the subfamilial classification (see Tax
chloroplast tree or the tree for the entire data set,
Treatment). The revisions primarily reflect
which presumably reflects extensive missing indata
circumscriptions of the Bambusoideae and
for GBSSI, and a generally smaller number dinoideae
of in- and involve only a small fraction
formative characters. Only two nodes were sup-
species in the family. Over three quarters
species are included in the subfamilies Po
ported in 100% of the 1000 bootstrap replicates,
and 11 had values between 90 and 99%. Chloridoideae, and Panicoideae, the circum
tions of which are changed only slightly by
Analysis of chloroplast data plus the data from
the two protein-coding nuclear genes (that is,visions.
ex-
cluding morphological and ITS data) has little ef-
MOLECULAR CHARACTERS
fect on either topology or support for the tree, per-
haps because omitting morphology and ITS only
Virtually all of the phylogenetic signal in
eliminates 178 characters, or about 8% of the total.
analysis comes from the molecular data (App

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394 Annals of the
Missouri Botanical Garden

III-K), as expected. The combinable component was difficult and confirmed our suspicion that it
consensus (Bremer, 1990) of the molecular may treesnot be useful at this level of divergence. ITS1
(Kellogg, 1998) is remarkably well resolved; andallparts of ITS2 had to be eliminated because of
nodes found in this consensus are stronglydifficultysup- in assessment of sequence similarity. The
ported in the combined analysis presented rpoC2 here. sequences used here code for repeated ami-
When the molecular data are analyzed alone, all motifs inserted into the protein. The inser-
no acid
strongly supported nodes from the combinedtion anal-appears only in the grasses and thus consti-
ysis are recovered, and support for the BEP Clade tutes a synapomorphy for the family (Cummings et
is increased. al., 1994), although we did not code it as such in
Previous theoretical (Graybeal, 1998) and em- this analysis. The repeats are similar but not iden-
pirical (Soltis et al., 1998) studies have indicated
tical to each other in sequence, making alignment
that large numbers of characters may be necessaryproblematical, a point discussed at length by Bark-
er (1995) and Barker et al. (1999). Efforts to im-
to resolve phylogenetic patterns, a conclusion only
partially supported by this study. The molecular prove alignments necessarily reduce apparent ho-
data alone and the entire data matrix included moplasy; this may result in the high CI mentioned
2093 and 2143 phylogenetically informative above. char- Although phylogenetic results from these
acters, respectively (Table 3). These data sets molecules
found are similar to those from the other genes,
the largest percentage of nodes with bootstrap val-
by themselves the two sets of sequences do not per-
ues above 70% (0.73 in both cases) but didmit notconfident assessments of relationships among
subfamilies.
have the highest consistency or retention indices.
The highest CI was produced by the rpoC2 Trees datafrom ndhF and phyB, individlually, are par-
alone (150 informative characters), although this well resolved and well su,pported. Their
ticularly
could be in part an artifact of alignment (see be-
congruence in early-diverging branches contributes
low), and the highest RI by the rbcL data alone (213
to the strength of the overall topology of the com-
informative characters). The fraction of nodes bined
withdata. In particular, phyB provi(les consider-
bootstrap values over 70% was almost as high able for
support for the BEP Clade, a to,,ology that is
only weakly supported by ndhF, an(l not at all by
the phytochrome B data alone (with 417 informative
characters) as for all data combined. We concludeseveral other data sets. The two data sets do appear
to conflict in relationships among members of the
that, while large numbers of informative characters
may provide increased reliability, small numbers PACCAD Clade, and this may be an area for future
are not necessarily misleading or inaccurate sam-
investigations.
ples of the whole. As noted in Methods, sequences for a given ge-
Other studies have shown that the number of nus were in some cases taken from (lifferent, con-
taxa included may affect phylogenetic accuracy generic species. This procedure assumes that the
(e.g., Hillis, 1996, 1998; Graybeal, 1998), although
genus is monophyletic, an assumption that is almost
this is not necessarily the case (Poe & Swofford,
certainly correct in many cases (e.g., Joinvillea,
1999). Certainly future studies should include Streptochaeta),
more and perhaps not as likely in others.
taxa than just the set of exemplars used here. How- For example, the three species of Stipa sampled
ever, the results numbered 1 to 9 above have been here have been placed in the genera Achnatherum,
found in analyses of virtually every individual data Stipa, and Jarava (Barkworth & Fverett, 1987;
set, as well as in the combined tree, and we would Barkworth, 1993; Jacobs & Everett, 1997), which
be surprised if they were overturned by inclusion are distinct and possibly not a monophyletic group
of more taxa. within Stipeae (Jacobs et al., 2000). While this
Most of the molecular data come from chloroplastproblem is not likely to compromise our conclu-
genes, so it is not surprising that the tree from the sions regarding subfamily relationships, it means
chloroplast alone closely matches the tree for the that relationships among species of the Stipeae (or
entire data set. The ndhF data set is missing theother tribes or genera where composite terminal
least data (Table 3) and has the most informativetaxa were used) cannot be addressed by this anal-
characters of the molecular data sets, presumably ysis.
because it is the longest molecule. Our results con-
firm the utility of this molecule for resolving rela- STRUCTURAL CHARACTERS

tionships among grass genera (Clark et al., 1995;

Giussani et al., in press). The structural characters, comprising th
Alignment is a particular problem for the rpoC2phological data set (Table 4), were optimize
and ITS data used here. Alignment of the ITS data phylogeny (Fig. 3). Our results suggest th

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Volume 88, Number 3 Grass Phylogeny Working Group 395
2001 Phylogeny and Classification of Poaceae

3 3147

Flagellaria
3053

31
Joinvillea

2 242938

2 28424345464751 A4 n hAnomochloa
354547
11111141

0-Streptochaeta

2 9 43

1 1

'Puelia
1112

1EP
221

020000

2 122135374050
1o-AooCoPACCAD
0000131

Figure 3 (pp. 395-397). Same tree as Figure 1, with struc

Character number is above the branch, and the state to w
unique occurrences of character states; open circles repre

or not), 11
of the morphological characters may (presence
be useful orfor
ab
delimiting groups within tribes
duced or subfamilies,
flowers), 12 (number but
13 (presence
are too variable to be useful in delimiting or absence subfam- of
of awns), 16hollow
ilies; these include 2 (culms (disarticulation
orabove or below 3 (leaf
not),
sheath margins fused or glumes), 20 (lodicule
free), 10 fusion), 28 (style fusion),
(pedicel present29

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 396 Annals of the
Missouri Botanical Garden

5 1215253045

1 0 1 0 Streptogyna
35

/r111923242846
/>-~Ehrharta
0
17

1 2 1 1 0 0 41 Oryza
OO 23242530
194546 Leersia
pOO- o0003
13 1 1 12232429
1 5 40 Pseudosasa
0113
2 1147

13 - 1 0 Chusquea
I 0 r-Buergersiochloa
\_ 17 gLithachne
13 1 A (-_
0-- "13 Olyra
0 I 2529
1630 Eremitis
01
01Y 2324
01 Pariana

2 4047

0- Brachyelytrum
2 1344

10182943
....- 00 01 / -. Lygeum
j28364347 /OOO-O-( 7123047
0011 13 Nardus
0000 1 1 3
0000 1 I 31647
3 13202130 -Melica
\ 122238 00

o /1 0 1 - Glyceria
13

Diarrhena

L, r~ -Brachypodium
404,7 153940
07 21 Avena
3 35

Bromus

Triticum
0
7 131640

14153638 Phaenosperma

21 0947 1 Anisopogon
2 12

1 3 2 o Ampelodesmos
25

_ Piptathe
1940 Stipa
2 0 -Nassella
Figure 3. Continued.

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Volume 88, Number 3 Grass Phylogeny Working Group 397
2001 Phylogeny and Classification of Poaceae

182547

o0o-- Micraira
1126

xO-- Chasmanthium
2835 1 0
1 5 2845
21 1
712223740 1 Thysanolaena
2 33
11 0 01 Zeugites

1 2 212545
2 122135374050
0000 00-
0000131
,OOO0-- Gynerium
4 133340

{?? Danthoniopsis
2 134047

1121748 9 1747 Miscanthus

1111 1 00 2830
16 Zea

48
28
? 15 ^ Panicum
0
~ Pennisetum
48

[*-Eria rchne
12174748 Aristida
48

4\t~~ 1421 --2 1 Stipagrostis

4 1340 31 Merxmuellera macowanii
1532
47

(2 21 1 4Danthonia 47

111
1\33 0 ~-Karroochloa
1 Austrodanthonia
47

0
33 o olinia
(2V 112845
2 1 1 1 Phragmites
1217222844

/ ~ Amphipogon
1 0
A3 Arundo
33 4348
13-
I 1547 Merxmuellera rangei

1 6 Centropodia
13

35748 14 1- Pappophorum
103

2 0 3 Eragrostis
112835

1344 Uniola
1JJ '110
0 1 4 40
Distichlis
. / 0 0,3,4
13

_ o--Zoysia
1012161849 / 1
2 28

01001 o-Spartina
101647

119 Sporobolus
11 9

Figure 3. Continued.
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398 Annals of the
Missouri Botanical Garden

flower and spikelet affects characters 8, 18, and 19.

(number of stigmas), 30 (highest order of stigmatic
C4 photosynthesis (chars. 48 and 49) is known to
branching), 39 (lipid in the endosperm), 40 (en-
dosperm starch grain syndrome), and 47 (basebe a set of characters that do not co-vary; its origin
chromosome number). is still poorly understood. These characters are dis-
cussed in more detail below.
For other structural characters, our assessment
of character states is inadequate for use in phylo-
genetic analysis. For example, the woodiness of
SPIKELETS AND FLOWERS

bamboo culms (char. 1) is due to numerous, closely

spaced vascular bundles around the periphery of Spikelet. The flowers of most grasses
the culm, each bundle with massive sclerenchyma ranged in bracteate units known as spikel
fiber caps on both sides, combined with heavily usually consist of two bract-like app
(glumes) at the base of a central axis (ra
sclerified ground tissue, but isolated fiber strands
may also occur (Soderstrom, 1981; Liese, 1998). which
It are borne one or more florets, all i
is not clear if the hardness of culms in Arundo,chous pattern. According to Clayton (19
Thysanolaena, and Gynerium and a number of other
the "grass spikelet never ceases to fascinate
"woody" taxa of the PACCAD Clade (Watsonsimplicity
& of its theme is matched by the
Dallwitz, 1992) is derived in the same way; these
of its variations." The apparent simplici
taxa need more careful anatomical study. Similarly,
grass spikelet notwithstanding, its origin
the fringed membranous ligule of some Pooideae mologies, as well as those of the grass flo
(char. 4) may not be the same as the ciliate mem-
been much debated (see reviews in Cliffor
brane found in many members of the PACCAD and Soreng & Davis, 1998).
Clade and requires developmental investigation. The phylogeny highlights the difficulty
cussing the evolution of the grass spike
Spikelet pairing (char. 9) appears in various pani-
coid grasses and also in Pharus, but the pattern of
standard spikelet (or some modification of
development of the pairs in Pharus is unknown. sent in all members of the Pooideae and the PAC-
Membranous lodicules (char. 21) are scored asCAD be- Clade (Figs. 4 and 5). 'The pattern of bracts
and flowers, however, is variable among Pharo-
ing the same wherever they occur, but development
ideae, Puelioideae, Bambusoideae, and Ehrharto-
of these structures has never been compared. Haus-
torial synergids are apparently uniquely derived
ideae (Fig. 4). Pharoideae bear single flowers, each
within the Danthonioideae, but many taxa havewithnot a lemma, a palea, and a pair of glumes, but
no rachilla extension (Fig. 4B; Judziewicz, 1987;
been investigated for this character. Embryo char-
Soderstrom et al., 1987). Puelioideae have multi-
acters (35, 36, 37, 38) are often phylogenetically
informative, but lack of observation of criticalflowered
taxa spikelets, in which each flower has a lem-
makes their use difficult in some cases. Starch
ma and palea, and the whole unit has a pair of
grains (char. 40) are classified according to glumes
their (Fig. 4A). Proximal incomplete florets oc-
apparent structure when viewed with the light cur,
mi-but distal reduction is seen only in Guaduella.
croscope. With much recent work done on theInbio-Bambusoideae, the unisexual, one-flowered
chemistry and molecular genetics of starch granule
spikelets of Olyreae are standard, but the bracteate,
rebranching
formation (e.g., Whistler et al., 1984; Frazier et al., spikelets (pseudospikelets) of many
1997), this character could and should be recir- Bambuseae are difficult to interpret (Fig. 4F; Jud-
cumscribed, although then much scoring willziewicz need et al., 1999). The multiflowered spikelet of
to be redone. Arm cells and fusoid cells (chars. 45
Streptogyna presents no difficulties of interpreta-
and 46) are now seen to be ancestral in the family,
tion, but in the Ehrhartoideae, extra proximal, ster-
ile bracts (usually called sterile lemmas) are com-
yet their development and ultrastructure are poorly
studied, and their physiological function ismon un-(Fig. 4G), and extreme reduction of glumes is
known. Comparisons of chromosome base numbers known (Oryzeae). It is not clear whether the prox-
(char. 47) will almost certainly become moreimal pre- sterile bracts of Ehrhartoideae are truly ho-
cise because of recent studies of nuclear genome mologous to the proximal incomplete florets that oc-
arrangement (e.g., Gale & Devos, 1998). cur in Puelioideae and some bambusoids, or if they
Finally, some of the structural characters areare
phylogenetically (and possibly developmentally
genuine morphological puzzles, ones for which and genetically) distinct. The uncertain position of
strict comparison is difficult. These include theStreptogyna
flo- makes the homology assessment even
ral bracts (glumes, lemmas, paleas, lodicules), more ambiguous.
which occur only in the grasses, and may not even Most characters of the spikelet and the floret
occur in Anomochlooideae. Homology of the grass (chars. 9-12 and 14-17) are treated as inapplicable

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Volume 88, Number 3 Grass Phylogeny Working Group 399
2001 Phylogeny and Classification of Poaceae

1 mm

1 cm

I 1 mm

Figure 4. Spikelets and spikelet equivalents of early-diverging lineages and the BEP clade. -A. Puelia schuman-
niana, Puelioideae (Letouzey 12930, US). -B. Pharus mezii, Pharoideae (Hinton 16059, US; redrawn from Judziewicz,
1987). -C. Streptochaeta spicata, Anomochlooideae (Bailey & Bailey 723, US; redrawn from Judziewicz & Soderstrom,
1989, from originals by A. Tangerini at US). -D. Anomochloa marantoidea, Anomochlooideae (Calderon 2046, US;
redrawn from Judziewicz & Soderstrom, 1989, from originals by A. Tangerini at US). -E. Stipa comata, Pooideae
(Pearson s.n., ISC). -F. Guadua chacoensis, Bambusoideae (Nee 35467, ISC). -G. Ehrharta bulbosa, Ehrhartoideae
(Barker 1119, ISC). -H. Festuca idahoensis, Pooideae (Pohl 15642, ISC).

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400 Annals of the
Missouri Botanical Garden

1mmi

I1

-0? - ,?i E

1 mm

F
G
2mm

1 mm
immi

Figure 5. Spikelets of the PACCAD clade. -A. Arundo donax, Arundinoideae (Bradley & Sears 3558, ISC). -B.
Dichanthelium oligosanthes, Panicoideae (Lelong 2063, ISC). -C. Aristida arizonica, Aristidoideae (Griffiths 7373,
ISC). -D. Tridens flavus, Chloridoideae (Thorne 18302, ISC). -E. Andropogon gerardii, Panicoideae (Clark s.n.,
teaching collection, ISC). -F. Danthonia californica, Danthonioideae (Pohl 9459, ISC). -G. Centotheca lappacea,
Centothecoideae (Liang 66250, ISC). -H. Chloris cucullata, Chloridoideae (Malacara & Gutierrez 33, ISC).

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Volume 88, Number 3 Grass Phylogeny Working Group 401
2001 Phylogeny and Classification of Poaceae

when grass-type spikelets and florets are absent, as the structure still could be derived as a prophyll if
in the non-grass outgroups (see char. 8). Although the axis rotated through 180? (Clifford, 1987). The
pseudospikelets occur in some genera of Bambu- gemmiparous bracts of many Bambuseae are essen-
seae, the two in the present study are regarded as tially glumes with a bud in the axil. If the bud
develops it becomes a second- or higher order
having true spikelets and florets, and thus scorable
for features of these structures. pseudospikelet (Judziewicz et al., 1999). Glumes
Neither Anomochloa nor Streptochaeta (Fig. 4C may be highly reduced or lost, as in Oryzeae. A
and D) has structures clearly homologous withglume-like prophyll at the base of the pseudospike-
glumes, lemmas, or paleas, and thus neither can belet is observed in many Bambuseae (Fig. 4F), al-
described as having grass-type spikelets or florets.though the axis bearing the prophyll is not elon-
We therefore follow Clark and Judziewicz (1996) in gated (McClure, 1966).
using the term "spikelet equivalent" to refer to the
Numbers offlorets. The rachilla may or may not
flowering units of the inflorescences in the Anom-
extend beyond the most distal floret, and reduced
ochlooideae to emphasize this lack of recognizable
or modified florets may be present below or above
homology. Characters of the spikelet and the floret
(or both below and above) the fertile ones. For this
are scored as inapplicable or ambiguous in these
analysis, we have assumed that the grass flower is
two genera except for char. 13 (see Appendix IV). terminal to the axis on which it is borne. In the
The grass spikelet may have originated either be-
Anomochlooideae, there is no identifiable palea
fore or after the divergence of Anomochlooideae. If
and thus the flower appears to be truly terminal to
before, then the spikelet was extensively modified
the main sympodial axes of the inflorescence in An-
in the long history of Anomochlooideae. The origin
omochloa, as discussed in Soreng and Davis (1998);
certainly must have occurred before divergence of
the same is true under Soderstrom's (1981) inter-
Pharoideae. We refer to the clade of all grasses ex-
pretation of the spikelet equivalent of
cept Anomochlooideae as the Spikelet Clade.
Streptochaeta. Within the Spikelet Clade, however,
Bracts outside of the spikelets subtend inflores-
the flowers are borne on lateral branches, as indi-
cence axes and often have a blade. Short to elon-
cated by the presence of a prophyll (i.e., the palea)
gate prophylls are usually present on the branches
in the proximal, a(laxial position on the branch.
subtended by these bracts. Such bracts occur )pri-
This pattern is clear in those taxa with multiflow-
marily in Bambuseae and Andropogoneae, but they
ered spikelets or spikelets with one floret ancd a
are not necessarily homologous between therachilla
two extension. There are a number of taxa with
groups (see Renvoize & Clayton, 1992). Well-de-
a single floret and no rachilla extension, including
veloped sul)tending bracts are usually absent in
the Pharoideae, in which a well-developed palea is
other memlers of the Spikelet Clade, although
found in the floret. It is simple enough to imagine
there may be a ridge or scar which presumably rep-
the reduction of the branch apex to the point where
resents the subtending bract at the base of thenoin-
evidence of a rachilla extension can be ob-
florescence branch.
served, but, as Soreng and Davis (1998) noted, the
Glumes. We have assumed here that glumes are presence of a single-flowered floret (or equivalent)
homologous across the Spikelet Clade. Glumes are appears to be plesiomorphic for the family. This
implies that either the rachilla extension and ad-
typically defined as the two sterile bracts at the
ditional fertile florets evolved subsequently, or that
base of the spikelet, but additional sterile bracts
multiflowered spikelets evolved before the diver-
(usually called sterile lemmas or sterile florets even
gence of the Pharoideae, and reduction to a single
if there is no evidence of any, even vestigial, floral
fertile floret occurred in that lineage (Soreng & Da-
axis) may occur between the glumes and the flower-
bearing lemmas (e.g., Ehrhartoideae, Chusquea,
vis, 1998). Clearly, single-flowered spikelets
evolved a number of times in various lineages in
many Centothecoideae). In general, the first (lower)
the BEP + PACCAD Clade.
glume is abaxial and the second (upper) glume is
adaxial (E. A. Kellogg, pers. obs.; Clifford, 1987),Lemma. Each floral axis is subtended by a lem-
but the first glume may be adaxial in position, ma
as (Fig. 6A and B), a structure that appears to be
in a number of Paniceae (Clifford, 1987). Grassl universally present across the Spikelet Clade. The
(1956) and Stapleton (1997) argued that the firstlemma apparently is formed wholly by the spikelet
glume is actually a prophyll for Andropogoneae and
meristem, and thus is a bract on the rachilla (Clif-
Bambuseae, respectively, and that the prophyll was
ford, 1987). Lemma morphology is extremely vari-
displaced upward to assume the position and func-able, but the number of nerves is consistently odd,
varying from 1 to 15 (Clifford, 1987). Some taxa
tion of a glume. Even if the first glume is abaxial,

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402 Annals of the
Missouri Botanical Garden

]E L
I!

N
e

K:
e 0

st'

i II
i i i:
\\ I | LJ rI
I! C

:
i ; .f v

E
E E
E
E

lo . r

CD 0
ijj

Figure 6. Grass flowers, fruits, and embryos. -A. Floral diagram of a grass with
-B. Floral diagram of a grass with two lodicules and three stamens. -C. Flower o
by D. Friedrick). -D. Lodicules of Pooideae (Poa, redrawn from Jirasek, 1968
(Muhlenbergia, redrawn from Soderstrom, 1967). -F. Lodicules of Panicoideae (Setar
-G. Lodicules of Bambusoideae (Chusquea), showing the anterior pair (lower two
H. Generalized ovule section (Danthonioideae) showing haustorial synergids (stippled
1994). -I. Longitudinal section of a panicoid embryo showing presence of a scu
mesocotyl internode (mi). J. Longitudinal section of a pooid embryo showing prese
section of a panicoid embryo apex showing overlapping embryonic leaf margins. -L
apex showing embryonic leaf margins that meet. M, N. Caryopsis of Eustachys
showing a punctiform hilum (h). -N. Embryo side, showing the large embryo (e). O
busoideae) (redrawn from McClure, 1973). -0. Hilum side, showing a linear hilu
the small embryo (e). c-coleoptile; co-coleorhiza; e-embryo; ep-epiblast; es-
integument; 1-lemma; lo-lodicule; mi-mesocotyl internode; o-outer integme
illa; s-scutellum; st-scutellar tail; t-vascular trace to placenta; w-ovary wall.
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Volume 88, Number 3 Grass Phylogeny Working Group 403
2001 Phylogeny and Classification of Poaceae

cules continue to be controversial. The grass flower

have more than two glumes at the base of the spike-
has been interpreted variously as dichlamydeous
let (see Glumes), but the sterile lemma of the pan-
icoid spikelet does appear to represent an evolu-(with two perianth whorls, the palea representing
tionary reduction from a fertile floret. two fused sepals and the lodicules the petals), mon-
ochlamydeous (with only one perianth whorl, the
Palea. The palea (Fig. 6A and B) is widely in-
lodicules, present, and the palea homologous to a
terpreted as a prophyll (Linder, 1987; Stapleton,
prophyll), achlamydeous (with no perianth, the lod-
1997; Clayton, 1990; Soreng & Davis, 1998; Jud-
icules representing modified bracts or stipules), or
ziewicz et al., 1999), and prophylls do occur in the
pseudanthial (with the flower representing a highly
inflorescences of many Bambuseae and Andropo-
reduced branch system, and the lodicules derived
goneae (Judziewicz et al., 1999; E. A. Kellogg, un-
from leaves or branches) (Clifford, 1987). The mon-
published obs.) relative to subtending bracts in pre-
ochlamydeous interpretation of the grass flower is
cisely the same way a prophyll is related to a
the most widely accepted. Recent molecular genet-
subtending leaf. Although the "palea as prophyll"
ic studies provide support for a petaloid homology
explanation may be more parsimonious, the deri-
of the lodicules (Irish, 1998; Schmidt & Ambrose,
vation of the palea from the fusion of two sepals
1998; Ambrose et al., 2000), thus rejecting the ach-
also has been supported (Schuster, 1910; Stebbins,
lamydeous and pseudanthial hypotheses. Ambrose
1974; Irish, 1998; Schmidt & Ambrose, 1998). Nu-
et al. (2000) also provided genetic evidence that
fiez (1968) and Clifford (1987) have suggested that
the palea and possibly also the lemma have char-
the odd-nerved, often 1-keeled paleas in the Ory-
acteristics in common with an outer perianth whorl,
zeae represent a separate origin of a palea-like
thus suggesting that the dichlamydeous interpreta-
structure, but this interpretation is inconsistent
tion might be revived. Bossinger (1990) and Pozzi
with the phylogeny. There is no reason to suppose
et al. (2000) described mutations in barley in which
paleas have been replaced with something different
the lemma is converted to a leaf. This may suggest
in Oryzeae. Single-flowered spikelets lacking a pa-
that the lemma is more leaf-like than sepal-like.
lea (e.g., Alopecurus) probably represent loss of the
Kellogg (2000a) suggested that these two interpre-
rachilla extension and the palea on the floral axis.
tations are not mutually exclusive, and that the
Vegetative branching in the grasses and other
complex structure of the grass spikelet may reflect
monocots typically involves a leaf with a bud or
simultaneous expression of both leaf and floral de-
branch in its axil, although bud displacement is
velopmental "programs." If the latter interpretation
observed in some palms and grasses (Dahlgren et
is correct, then it may be meaningless to discuss
al., 1985; Serebryakova, 1971; Fisher & Dransfield,
whether the lemma is "really" a leaf or a sepal.
1977). The first appendage of the branching axis is
an adaxial two-keeled bract (= prophyll). This pro- Androecium. All six stamens (arranged in two
phyll encloses the bud, but often persists once the alternating whorls of three stamens each, Fig. 6A;
branch develops. The origin of the vegetative pro- see Clifford, 1987) are plesiomorphically present
phyll is not clear, but whether it is a single struc-
within the study group and at the point of origin of
ture or the result of fusion of two bracts, ultimately
the grass family, but the entire outer whorl is lost
it is foliar in nature (Stebbins, 1974). The relation-
in the Restionaceae. Within the grass family, all six
ship between the subtending leaf and the prophyll
stamens (both whorls) are maintained in the three
is generally constant, and therefore a prophyll earliest-diverging subfamilies (except for the loss of
marks the presence of a lateral branch. If the veg-
the inner anterior pair in Anomochloa, as noted
etative branching pattern is reiterated in the inflo-
above). The outer whorl is maintained throughout
rescence, then the palea ought to be homologous to
most of the grass family, except for the various au-
a prophyll, and prophylls should occur in fully
tapomorphic losses and polymorphisms noted
bracteate inflorescences as the adaxial first ap-
above. Loss of the entire inner whorl (e.g., Fig. 6B)
pendage of branches in the axils of subtending
is interpreted as a synapomorphy of the BEP +
bracts.
PACCAD Clade, but in one subclade within this
Flower. Grass flowers are made up of a gynoe- large group (the bambusoid/ehrhartoid alliance)
cium, androecium, and two or three flap-like struc-there are three or more independent reversions to
tures (lodicules) that force the floret open at ma-presence of this whorl, and possibly a secondary
turity (Fig. 6A-G). The literature on the anatomy loss in Leersia. An alternative interpretation of the
and development of the grass flower should prob- outer stamen whorl, in the context of the present
ably be reinterpreted in the light of the present reconstruction of phylogenetic relationships, and
phylogeny. The origin and homology of the lodi- involving no secondary origins, would have the in-

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404 Annals of the
Missouri Botanical Garden

ner whorl lost independently in Pooideae andare the

additional differences in expression of the en-
PACCAD Clade, as well as in a series of small zymes involved in photosynthesis (Sinha & Kellogg,
lineages within the bambusoid/ehrhartoid alliance.1996). For example, all Chloridoideae except for
Alternatively, if a PACCAD + Pooideae lineage isthe C3 Eragrostis walteri and Merxmuellera rangei
considered, loss of the inner stamen whorl could be form aspartate, use the NAD-malic enzyme, and
interpreted as a synapomorphy of that clade; the have double bundle sheaths, with the inner one of
presence of this whorl in some genera of Ehrhar-thick-walled cells. (Centropodia has not been bio-
toideae and Bambusoideae might then be inter-chemically typed, but is anatomically the same as
preted as retention of a plesiomorphy, while the ab-other NAD-ME taxa.) Stipagrostis, in Aristidoideae,
sence in others would be interpreted as havingis similar to the chloridoids in having two bundle
arisen independently of the loss in the PACCAD +sheaths, the outer of which appears to be carbon-
Pooideae. reducing (Sinha & Kellogg, 1996). Aristida itself
forms malate, using the NADP-malic enzyme; un-
BIOCHEMISTRY like other NADP taxa, it has two bundle sheaths.
The ultrastructure of the outer sheath is similar to
The phylogeny suggests that the C4 photosyn-
that of NADP species, but the inner sheath is more
like anwithin
thetic pathway has evolved multiple times NAD or PCK plant; the extent to which
the PACCAD Clade. In the C4 pathway,these
thesheaths
Calvin-
are developed varies throughout the
Benson cycle, and hence Rubisco, is relegated
genus (Brown,to
1977; Carolin et al., 1973). Eriachne
also
the bundle sheath cells surrounding the uses NADP-ME
veins (Hat- and has a double bundle
sheath,1996).
tersley & Watson, 1992; Sinha & Kellogg, but unlike Aristida the inner sheath ha
Phosphoenolpyruvate carboxylase then catalyzes cells. The C4 Panicoideae also var
thick-walled
biochemically
CO2 reduction in the mesophyll to produce the four- and histologically, although larg
carbon compound oxaloacetate. This compound is
groups are uniform. For example, the entire trib
then reduced to malate or aspartate andAndropogoneae
transported (ca. 100 genera and 1000 species
to the bundle sheath, where the newlyuses
fixedNADP-ME
CO2 is and has a single bundle sheath.
immediately removed and taken up byBoth Rubisco.
the phylogeny and structural/biochemica
This keeps CO2 concentration high at the
dataactive site
indicate that the C4 pathway is not homologou
of Rubisco, preventing competition by O2. Consis-
wherever it occurs. The close relationship of the C
tent with the constant flow of materials between the lineages, however, suggests that there were a set
bundle sheath and mesophyll, C4 species (Fig. 7C) changes at the base of the entire PACCAD Clad
have closer vein spacing than C3 species (Fig. 7B). that made the pathway easier to evolve. If this wer
Other anatomical manifestations of C4 photosynthe- true, then those changes, whatever they wer
sis include enlarged bundle sheath cells (Kranz would be homologous, even though the final man
anatomy), closely packed chlorenchyma cells, and ifestations of the pathway are not.
in some, radiate chlorenchyma (Fig. 7C).
Despite the foregoing generalizations, C4 photo- IMPLICATIONS FOR MORPHOLOGICAL EVOLUTION
synthesis actually represents a suite of characters,
The phylogeny provides a unique and powe
rather than a single genetic and phylogenetic
tool for description of evolutionary pattern (Ke
change. Only down-regulation of Rubisco in the
2000a). Major clades and evolutionary trans
mesophyll, up-regulation of PEP carboxylase, and
are summarized in Figure 8. Additional deta
closer vein spacing are common to all C4 grass lin-
be found at http://www.virtualherbarium.org/g
eages. The four-carbon compound that transports
gpwg/default.htm.
the carbon to the bundle sheath may be malate or
aspartate, the decarboxylating enzyme may be a Sister relationship of Poaceae and Joinvi
malic enzyme using NAD as a co-factor (NAD-ME), aceae. The presence of long and short cells i
or using NADP (NADP-ME). If the former, addi- leaf epidermis (char. 42), with at least some o
tional decarboxylation activity may be provided by short cells containing silica bodies, unambigu
PEP carboxykinase, so PCK activity is dependent supports the sister relationship of Joinville
upon the presence of NAD-ME (Kanai & Edwards, and Poaceae. This arrangement is appare
1999). Some C4 grasses have only one bundle unique among angiosperms (Campbell & Kel
sheath, whereas others have two. In those with two 1987; Kellogg & Linder, 1995). The presenc
bundle sheaths the inner sheath may be made up the 6.4 kb inversion in the chloroplast gen
of thick-walled cells, forming a conventional mes- (char. 51) is also an unambiguous synapomo
tome sheath, or it may be parenchymatous. There supporting this sister relationship, although it

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Volume 88, Number 3 Grass Phylogeny Working Group 405
2001 Phylogeny and Classification of Poaceae

A.k. A

Figure 7. Leaf anatomy. -A. Dinochloa maclelandii (Soderstrom 2607). -B. Poa sp. (Carolina Biological Supply
Co.). -C. Bouteloua sp. (Carolina Biological Supply Co.). ac-arm cell; bc-bulliform cell; ch-chlorenchyma; fc-
fusoid cell; is-intercellular space; ms-mestome sheath; p-phloem; ps-outer parenchyma sheath; rch-radiate
chlorenchyma; sg-sclerenchyma girder; st-stomatal apparatus; x-xylem.

known whether Ecdeiocoleaceae possess this in- gion of the chloroplast genome (char. 52), unam-
version (R. J. Soreng, pers. comm.). biguously support the monophyly of Poaceae. Two
other features unique to and characteristic of Po-
Monophyly of Poaceae. Two characters in this aceae but not included in this analysis are the cary-
analysis, the highly differentiated grass embryo opsis and the presence of intraexinous channels in
(Fig. 61 and J) and its lateral position (char. 34) the pollen wall (Linder & Ferguson, 1985; Camp-
and the trnT inversion in the large single-copy re- bell & Kellogg, 1987; Kellogg & Linder, 1995).

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 Panicoi

Centoth

Aristid

Danthon

Arundin

Chlori

Eriachn

Micrair

Po

Ehr

Str

Bam

Pu

Pharoid

Anomoc

Joinvil

Other P

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Volume 88, Number 3 Grass Phylogeny Working Group 407
2001 Phylogeny and Classification of Poaceae

The caryopsis is a single-seeded, usually dry, in- es except Anomochlooideae) is then likely the re-
dehiscent fruit with the pericarp fused to the seed sult of a cumulative series of changes that occurred
coat in the hilar region and otherwise closely ad- during the early history of the family. Clayton
nate (Sendulsky et al., 1987). The caryopsis devel- (1990), however, pointed out that there are well-
ops from a unilocular ovary containing a single developed bracts in the spikelets of Restionaceae,
ovule (Fig. 6H). Within Poaceae, the basic cary- and what could be interpreted as subtending bracts
opsis has been modified to the fleshy (baccoid) or are present, although not necessarily well devel-
the achene-like (nucoid) caryopses of some woody oped, in Joinvilleaceae (Dahlgren et al., 1985).
bamboos (Sendulsky et al., 1987) or the follicoid or Clayton (1990) also noted that if the palea in grass-
cistoid caryopses of some chloridoids in which the es is interpreted as a prophyll, then there is no
seed is free from the pericarp or separates from ithomolog for it among other Poales; however, pro-
when moistened.
phylls are occasionally found at the base of spike-
The highly differentiated grass embryo and itslets in Restionaceae (H. P. Linder, pers. obs.).
lateral position at the base of the caryopsis (char. The results of this analysis and prior studies
34; Fig. 61 and J) are synapomorphies for the family(Clark et al., 1995; Soreng & Davis, 1998) support
(Campbell & Kellogg, 1987; Kellogg & Linder,the following as plesiomorphic within the grass
1995). In the grasses, the embryo has leaves, vas-family: an herbaceous, perennial, rhizomatous hab-
cular tissue, and clearly localized shoot and rootit; pseudopetiolate and relatively broad leaf blades
meristems before the fruit is dispersed, and thus
bearing multicellular microhairs and anatomically
looks much more like a seedling than the embryos
with commissural veins, fusoid cells (Fig. 7A), and
of non-grass relatives (Fig. 61 and J; Reeder, 1957;
alternating long and short cells on the epidermis
Sendulsky et al., 1987). Constant features of the
with at least some of the short cells including silica
grass embryo are the scutellum, coleoptile, and co-
bodies; leaves with an adaxial ligule and open
leorrhiza. A scutellar cleft (Fig. 6I) may or may not
sheaths; a highly bracteate inflorescence; one-flow-
separate the scutellum from the coleorrhiza, and the
ered spikelets or spikelet equivalents; six stamens
epiblast, an extra flap of tissue opposite the scu-
in two whorls with tetrasporangiate, dithecal an-
tellum, may be present (Fig. 6J) or absent (Fig. 61).
thers; monoporate pollen with intraexinous chan-
Whether or not the embryonic leaf margins meet or
nels in the wall; a uniloculate, uniovulate gynoe-
overlap varies throughout the family (Fig. 6K and
cium with three stigmas and one order of stigmatic
L).
branching; a basic caryopsis with a linear hilum; a
Changes in the inflorescence occurred between
the time that Joinvillea divergetd and the time of highly differentiated, laterally positioned embryo
divergence of Anomochlooideae. Relative to most with a scutellum, coleoptile, coleorhiza, and a neg-
of their poalean sister families (excluding Restion- ligible mesocotyl internode; Festuca-type starch
aceae, Ecdeiocoleaceae, and Centrolepidaceae), the grains in the endosperm; and the C3 photosynthetic
grasses, including Anomochlooideae, have well-de- pathway. The grass spikelet and lodicules may have
veloped bracts (what are normally called subtend- evolved before the divergence of the Anomochlooi-
ing bracts, prophylls, glumes, lemmas, and paleas) deae and the rest of the family, and were lost in the
subtending and enclosing contracted inflorescence Anomochlooideae (cf. Soreng & Davis, 1998), but
branches and flowers (Figs. 4 and 5). This appears these features are not plesiomorphic under the pre-
to be a derived character marking the origin of the sent optimization. Bisexual flowers are probably
family, although this was not used explicitly as a also plesiomorphic, but unisexuality evolved early
character in this analysis. Under this interpretation, and in a number of different lineages within the
the characteristic grass spikelet (found in all grass- family.

Figure 8. Summary phylogeny of the grasses indicating significant morphological, ecological, and molecular (cpDNA
= chloroplast DNA) events in the evolution of the family. Infrequent losses, parallel gains, and reversals are not shown
for these characters. The 12 subfamilies recognized by the GPWG appear in boldface. Poales sensu APG include
Cyperaceae. Marked taxa: (star) At least some included species have unisexual flowers/florets; (?) At least some included
species have a C4 carbon fixation pathway, Kranz anatomy, or both. Dark circles indicate nodes strongly supported by
all data combined (bootstrap > 99; Bremer support > 16). Subfamilies with common names: Aristidoideae (wiregrasses,
etc.), Arundinoideae (reeds, etc.), Bambusoideae (bamboos), Chloridoideae (lovegrasses, tef, etc.), Danthonioideae (oat-
grasses, pampas grass, etc.), Ehrhartoideae (rice, wild-rice, etc.), Panicoideae (maize, panic grasses, millets, sorghum,
sugar cane, etc.), and Pooideae (barley, brome grasses, oats, rye, wheat, etc.).

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408 Annals of the
Missouri Botanical Garden

Anomochlooideae. The basal divergencelet

be-
equivalent of Anomochloa is indeed homologous
tween Anomochlooideae and the rest of the Poaceae to a standard grass lemma, a palea is lacking and
(the Spikelet Clade) is well supported based on mo-
the flower is terminal, whereas in a true grass floret
lecular evidence. Monophyly of Anomochlooideae, the flower is borne on a lateral axis as indicated by
however, is supported morphologically only by the the presence of the palea if it is interpreted as a
unreversed presence of the adaxial ligule asprophyll.
a Some authors interpret the distal three
bracts of the spikelet equivalent of Streptochaeta as
fringe of hairs, a character that appears elsewhere
in the family. The pulvinus at the summit of the lodicules and the next proximal two bracts as a
pseudopetiole is a possible synapomorphy for this bifid palea (e.g., Clayton, 1990), but there is no
clade but requires further study to determine sim-compelling evidence for this. The spikelet equiva-
lent of Streptochaeta might represent a condensed
ilarities with the structure in other grasses. Molec-
ular support for this clade may be due at least branching
in system (Soderstrom, 1981), but it is not
a pseudospikelet as found in the Bambuseae. In
part to long-branch attraction (see Unresolved
questions). any case, lack of a palea in Streptochaeta also im-
Anomochlooideae have been recognized as a plies that the flower is terminal.
separate family (Nakai, 1943), a point of view that
The Spikelet Clade (Pharoideae + [Puelioideae
is completely consistent with the phylogeny. We
have chosen here to retain Anomochlooideae within
+ {BEP + PACCAD]]). This clade, which in-
cludes all of the grasses except for Anomochlooi-
Poaceae because of the strong synapomorphies
deae, is defined by the unambiguous presence of
linking them (notably the caryopsis and the highly
true grass spikelets, florets (char. 8), and lodicules
differentiated embryo, see Fig. 8). Retention of An-
(char. 18). The plesiomorphic condition of the
omochlooideae in Poaceae is also taxonomically
spikelet is clearly the presence of a pedicel (char.
conservative, in line with all previous studies of the
10), two glumes, and a well-developed lemma and
family, and consistent with the efforts of the APG
palea in the floret. The single-flowered spikelet may
to limit monotypic or small families (Chase et al.,
be synapomorphic for the family above the point of
2000a, b).
divergence of Anomochlooideae, with a transfor-
Anomochlooideae are variable with respect to
mation to multiflowered spikelets above Pharoideae
embryonic leaf margins and the epiblast. Embry-
and then numerous reversals, but the first true
onic leaf margins meet and the epiblast is present
spikelets in grasses may have been multiflowered
in Anomochloa, whereas the embryonic leaf mar-
(see discussion under Spikelet). The plesiomorphic
gins overlap and the epiblast is absent in Strepto-
condition for lodicules is clearly three (char. 19),
chaeta (Judziewicz & Soderstrom, 1989). Both gen-
unfused (char. 20), and with a distally membranous
era have an inconspicuous scutellar cleft. The
portion (char. 21). Presence of unisexual flowers
coleoptile is usually represented as a more or less
may be synapomorphic for this clade, with numer-
conical "cap" protecting the embryonic leaves and
ous reversals to bisexual florets, but it may be more
shoot apex, but the coleoptile margins are entirely
likely that unisexuality arose multiple times. A
free and overlapping in Streptochaeta, whereas in
base chromosome number of x = 12 (char. 47) was
Anomochloa the margins at the base of the cole-
established before the divergence of Pharoideae.
optile are fused but free toward the apex, as is also
seen in Pharoideae (Reeder, 1953; Judziewicz & Pharoideae. Monophyly of this clade is strong-
Soderstrom, 1989). ly supported by the presence of resupinate leaf
The inflorescences of both Anomochloa and blades, oblique lateral veins in the leaf blades, and
Streptochaeta are bracteate, but the lack of clear hairs wholly or partially covering the fe-
uncinate
male lemmas (Judziewicz, 1987). The female lem-
homology of these bracts with those of the standard
grass spikelet has been noted. The spikeletmas exhibit a laminar anatomical structure similar
equiv-
alents in both Anomochloa and Streptochaeta to that
areof Anomochlooideae, but the transversely
one-flowered and bisexual. The upper bract elongated
in An- cell layer is subjacent to the adaxial epi-
dermis. In Pharoideae, Anomochlooideae, and
omochloa exhibits a laminar anatomical structure,
some Bambusoideae (Ghopal & Ram, 1985), the
with the transversely elongated cell layer subjacent
coleoptile
to the abaxial epidermis of the bract (Judziewicz & margins are free for at least a portion of
Soderstrom, 1989). This laminar structuretheir is not
length, but the distribution of this feature in
the not
found in bracts of Streptochaeta. (Similar but rest of the BEP + PACCAD Clade is not well
identical laminar anatomy characterizes female
documented. Pharoideae embryos have an epiblast
lemmas in Pharoideae.) As Soreng and and Davis
a small scutellar cleft, and embryonic leaf mar-
(1998) pointed out, if the upper bract of thegins meet (Judziewicz, 1987). The Pharoideae uni-
spike-

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Volume 88, Number 3 Grass Phylogeny Working Group 409
2001 Phylogeny and Classification of Poaceae

formly exhibit one-flowered, unisexual, pairedphological synapomorphies support its monophy

(char. 9) spikelets (Fig. 4B). When present in theloss of the pseudopetiole (char. 7), reduction to t
male spikelets, the three lodicules are small, whichlodicules (char. 19), loss of the inner whorl of s
may be plesiomorphic or may represent a reduc-mens (chars. 23 and 24), and loss of arm and fu
tion. Disarticulation is variable, in that the wholecells (chars. 45 and 46). The pseudopetiole is
inflorescence may disarticulate as in Scrotochloa,gained in Bambusoideae, as well as in a few me
or the whole inflorescence or branches usually dis-bers of the PACCAD Clade. Arm and fusoid cells
articulate in Pharus, or female spikelets disarticu-are also regained in Bambusoideae. The inner
late above the glumes in Leptaspis, and perhaps whorl of stamens is interpreted as having been re-
also in the other genera (Soderstrom et al., 1987). gained three or four times within the bambusoid/
These, along with the uncinate hairs, appear to beehrhartoid clade. Within the BEP + PACCAD
adaptations to epizoochorous dispersal. Multicel-Clade, the lamina on the first seedling leaf is lo
lular microhairs (char. 43) are lost in Pharoideae.only in Bambusoideae and Oryzeae. Unisexual flo
rets have evolved in most lineages of this clade
The Bistigmatic Clade (Puelioideae + [BEP + e.g., Olyreae (Bambusoideae), Zizania (Ehrharto
PACCAD]). This clade is marked by three mor-ideae), Lamarckia (Pooideae), several genera o
phological synapomorphies: transformation from Chloridoideae and Centothecoideae, and very com
three to two stigmas (char. 29), transformation from
monly in Panicoideae. Most lineages include tax
one to two orders of stigmatic branching (char. 30),
with one floret per spikelet and taxa with multipl
and presence of the 15 bp ndhF insertion (char.florets per spikelet. The presence or absence of an
53). Multiple florets per spikelet (char. 12; Fig. 5)
epiblast is variable, as is the presence or absenc
may have arisen within Puelioideae as shown in of the scutellar cleft, although in the PACCAD
Figure 3, or in the common ancestor of the Pue- Clade the scutellar cleft is generally present (Reed
lioideae + (BEP + PACCAD) clade. Regardless of er, 1957).
which scenario is correct, reversals to one floret
The large number of reversals hypothesized in
occurred numerous times in the BEP + PACCAD
this part of the tree raises a number of intriguing
Clade. Disarticulation above the glumes (char. 16)
questions regarding morphological evolution. We do
clearly is established before the divergence of Pue-
not know anything about the development or un-
lioideae.
derlying genetics of the characters, so we are forced
Puelioideae. The forest habitat and broad, into the agnostic assumptions that gains and losses
pseudopetiolate leaf blades of the Anomochlooi-are equally likely, and that pseudopetioles, arm
deae and Pharoideae are retained in this subfamily, fusoid cells, epiblasts, and unisexual flowers
cells,
but no unique morphological synapomorphies are forall developmentally and genetically the same
Puelioideae have been identified. The culms wherever
ap- they occur. The changes that we interpret
as reversals could actually represent retained prim-
parently do not produce aerial branches, nor basal
itive characters if loss of these characters is more
tillering as in Anomochlooideae and Pharoideae.
The presence of proximal female-sterile floretslikely
in than their regain. Equally possible, the
changes interpreted as reversals could represent
the spikelet (char. 11) is an unreversed synapo-
morphy for Puelioideae in this analysis, but is the
also origin of novel characters that look superficially
similar to ancient ones. We have some evidence for
a synapomorphy for Paniceae and autapomorphic
the latter (see below) in that arm cells in the bam-
for multiple other taxa on the tree. In Puelioideae,
busoids are actually morphologically different from
the pattern of sexuality in the spikelets is somewhat
more complex than in many other subfamilies, thosebut in Anomochlooideae and Pharoideae (Zhang
within a spikelet, at least some proximal florets &are
Clark, 2000). Finally, the character optimizations
male. In Guaduella, the 1 to 3 proximal florets reflect
are the hypothesis that the BEP Clade is mono-
male, and additional florets are bisexual with phyletic.
the If, as we outline below, the Pooideae are
distalmost one or few reduced, but in Puelia the actually sister to the PACCAD Clade-a hypothesis
that is neither favored nor excluded by the data-
proximal 3 to 6 florets are male or neuter, with the
then the pattern of morphological evolution is dif-
single apical floret unisexual and female. Multicel-
lular microhairs (char. 43) are lost in Puelia, ferent.
and
a reversion to three stigmas (char. 29) occurs in
some species of Puelia. The BEP Clade (= BOP clade of Clark et al.,
1995). This clade is supported by molecular se-
The BEP + PACCAD Clade. This clade in- quence data, particularly from ndhF, rpoC2, and
cludes the vast majority of grass species. phyB
Six (see Results), but other data sets support a
mor-

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410 Annals of the
Missouri Botanical Garden

Pooideae + PACCAD clade (Soreng & Davis, Pooideae. Monophyly of the pooid clade is
1998). In this analysis, constraining Pooideae + strongly supported by molecular data including
PACCAD as monophyletic was only slightly less cpDNA restriction site data (Soreng et al., 1990;
parsimonious than BEP + PACCAD (see Results). Davis & Soreng, 1993; Nadot et al., 1994; Soreng
In addition, no morphological synapomorphies sup- & Davis, 1998, 2000). Parallel-sided subsidiary
porting the BEP Clade have been identified. Losscells, lack of microhairs, nonvascularized lodicules
of the lemma awn is optimized to this node, but(Fig. 6D), and the presence of an epiblast and lack
awns are regained in many taxa within the BEP of a scutellar cleft in the embryo (Fig. 6J) are char-
Clade. The lack of sequence data for Streptogynaacteristic of a majority of the subfamily but do not
contributes to the uncertainty of its position within constitute unequivocal synapomorphies. In this
the BEP Clade and may also affect assessment ofanalysis, the loss of stylar fusion (char. 28) is an
the monophyly of the clade. Streptogyna appears asunreversed synapomorphy for the Pooideae. Loss of
sister to Ehrhartoideae (Fig. 1), but in other anal- the scutellar tail (char. 36) is widespread in the
yses of these data it appears as sister to the rest ofclade, but polymorphisms prevent its unambiguous
the BEP Clade. optimization. An unreversed transformation to faint
or absent vascularization of the lodicules (char. 22)
Bambusoideae. Monophyly of the true bamboos
occurs within the Pooideae after the divergence of
(i.e., olyroid + woody bamboos) is supported by
Brachyelytrum. A transformation to the embryonic
molecular data in this and other analyses (Clark et
leaf margins meeting (as opposed to overlapping;
al., 1995; Zhang, 1996; Zhang & Clark, 2000).
Fig. 6L) also occurs after the divergence of Bra-
Morphologically, secondary gain of the pseudope-
chyelytrum but is reversed in Phaenosperma (or
tiole (char. 7) and secondary loss of the lamina of
Phaenosperma + Anisopogon). Multicellular micro-
the first seedling leaf (char. 41) are synapomor-
hairs (char. 43) are known only in Lygeum + Nar-
phies. Although only presence or absence of arm
dus; although this character is scored only for the
cells was scored in this analysis, Zhang and Clark
abaxial leaf surface, it appears that Pooideae, at
(2000) found that the presence of strongly asym-
least above this divergence, are the only group of
metrically invaginated arm cells (Fig. 7A) is a po-
grasses to lose completely the ability to make mul-
tential synapomorphy for this clade. Fusoid cells
ticellular microhairs anywhere on the plant (except
are characteristic of the Bambusoideae (Fig. 7A),
possibly the lodicules). Chromosomal evolution in
but it is not known whether their presence repre-
Pooideae is complex (see char. 47), but x = 12 is
sents retention of the plesiomorphic condition or
reversal after loss of fusoid cells at the base of the
apparently plesiomorphic in the BEP Clade, so
numbers such as x = 10 and x = 11 in the earlier-
BEP Clade. Bambuseae are here supported by the
diverging lineages of Pooideae may well be derived
presence of perennating woody culms (char. 1), ab-
from this condition. The presence of x = 12 in
axial ligules (char. 5), and Panicum-type starch
Phaenosperma, Ampelodesmos, and some Stipeae
grains (char. 40). A secondary gain of the inner
may be a retention; x = 7 is clearly a synapomor-
stamen whorl (chars. 23 and 24) occurred at least
phy of the core Pooideae (here represented by Bra-
once but possibly several times. Olyreae have a
chypodium, Avena, Bromus, and Triticum). Two lod-
synapomorphic base chromosome number of x =
icules (char. 19) are found at the base of Pooideae,
11 (char. 47), but the tribe is also characterized by
but a reversal to three occurs in Stipeae (in which
unisexual spikelets.
another transformation, to two, occurs in Nassella);
Ehrhartoideae. This lineage is strongly sup- this is undoubtedly an oversimplification of the pat-
ported by molecular data, and is characterized by
tern in the Stipeae in which lodicule number varies
considerably (Vickery et al., 1986). Loss of the dis-
the presence of one female-fertile floret per spike-
let, often with one or two proximal female-steriletally membranous portion of the lodicule (char. 21)
florets (char. 11). This character is coded as am-is a synapomorphy for Meliceae. The earliest-di-
biguous in Oryza and Leersia, but if the vestigialverging lineages of the pooid clade have one floret
per spikelet (char. 12) (although a rachilla exten-
structures at the base of the spikelets in these gen-
era are interpreted as highly reduced glumes, thension is present in Brachyelytrum), multiple florets
the presence of proximal female-sterile florets is an appear in Meliceae, single florets characterize the
unambiguous synapomorphy. Two lodicules (char.(Phaenosperma + Anisopogon) + Stipeae clade,
19) are found in this clade; in addition, the inner
multiple florets are found at the base of the core
whorl of stamens (chars. 23 and 24) is regained,pooids, and many taxa within the core pooids have
styles are not fused (char. 28), and fusoid cellsone floret per spikelet. Multiple independent ori-
(char. 46) are lost. gins of multiple florets per spikelet can be hypoth-

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Volume 88, Number 3 Grass Phylogeny Working Group 411
2001 Phylogeny and Classification of Poaceae

esized, but subsequent reduction to one floret per lished for the BEP + PACCAD Clade, but no trans-
spikelet has clearly occurred in several groups. Pat- formations to any other number occur in the PAC-
terns of divergence within this clade are complex CAD Clade.
and still are being evaluated, so some inferences The positions of Micraira and Eriachne in the
regarding character evolution are likely to change. phylogeny are not well resolved, presumably due to
a lack of sequence data for both genera (see Results
The PACCAD Clade. Over half the species of and also Unresolved Questions). The two species of
the grass family are included in this clade. Even Eriachne are from quite distinct parts of the genus,
as early as the 1930s (Avdulov, 1931; Prat, 1932, based on the informal classification of Lazarides
1936; Roshevits, 1937), taxa of this clade have (1995). This undoubtedly affects the interpretation
been grouped together. Hilu and Wright (1982) of character state transformations within the entire
were the first to retrieve this clade in a formal anal- clade.
ysis, and subsequently support for the monophyly Early in the evolution of the PACCAD Clade,
of the clade is found in all molecular analyses to some lineages developed the capacity for C4 pho-
date with sufficient sampling (Hilu & Esen, 1988; tosynthesis, apparently as an adaptation to high
Hilu & Johnson, 1991; Davis & Soreng, 1993; Na- light/high temperature conditions and perhaps also
dot et al., 1994; Barker et al., 1995; Clark et al., to falling levels of atmospheric CO2 (Sage & Mon-
1995; Duvall & Morton, 1996; Liang & Hilu, 1996; son, 1999). Most members of the Panicoideae, all
Mathews & Sharrock, 1996; Soreng & Davis, 1998; but two Chloridoideae, the Aristidoideae (except for
Hsiao et al., 1999; Mathews et al., 2000) except for Sartidia), and the Eriachneae are C4. The poor res-
Cummings et al. (1994), in which an oryzoid cladeolution of the phylogeny at the base of the PACCAD
nested within the PACC clade. Davis and Soreng Clade makes it impossible to determine precisely
(1993) named this the PACC clade based on the how many origins of C4 photosynthesis there were,
four subfamilies that were then recognized as com- but certainly there were at least two, and possibly
prising the clade, but we here modify the name to more. The data are also consistent with a polymor-
reflect the recognition of two additional subfamilies, phism at the base of the PACCAD Clade.
the Aristidoideae and the Danthonioideae.
The Panicoideae + Centothecoideae Clade.
The PACCAD Clade is robustly supported based
on molecular data and additionally is supported byThis clade was recovered in virtually all suba
the presence of an elongated mesocotyl internode alyses, and had reasonable support (bts 85, brs
(char. 37) and the loss of the epiblast (char. 35; the combined analysis. The presence of non-li
in
ear hila (char. 33; Fig. 6M) is a potential synap
Fig. 61). The latter character reverses in the clade,
morphy for this clade. Although support for t
so that secondary gain of the epiblast is an apparent
synapomorphy for Centhothecoideae. Two charac- monophyly of Panicoideae (excluding Gyneriu
ters (chars. 21 and 50) are possible synapomor- and Danthoniopsis) was strong (see Results), re
phies for the PACCAD Clade, but because of a lack tionships of the centothecoid taxa, Gynerium, a
Danthoniopsis to the Panicoideae and to each oth
of data or lack of a structure in Micraira, placement
of these transitions is ambiguous. The lack of lod-remain unresolved, but the placement of Gyneri
as sister to traditional Panicoideae is a novel result.
icules in Micraira prevents unambiguous place-
ment of the loss of the distally membranous portionPanicoideae. The presence of proximal female-
of the lodicule (char. 21), and Micraira remains un-
sterile florets (char. 11) and the transformation to
sampled for the presence or absence of the 3 thebp classical NADP-ME C4 subtype (char. 48) are
deletion in phytochrome B (char. 50). Solid culm
unambiguous synapomorphies for Danthoniopsis +
internodes (char. 2) are shown here as synapo- Panicoideae. Some reversions to the C: pathway oc-
morphic, although hollow ones reappear in other cur within the Paniceae among unsampled taxa,
members of the clade. Non-linear hila (char. 33;and at least one secondary transformation to the
Fig. 6M) are widespread in the PACCAD Clade, butNAD-ME C4 subtype occurs in Panicum. This
the point of origin is ambiguous. The Panicum-type
clade is also supported by the presence of one fe-
starch grain syndrome (char. 40) may be a syna-male-fertile floret (char. 12) as a reversal and the
pomorphy for the PACCAD Clade, with a reversal gain of a germination flap (char. 17), but the place-
to the Festuca-type in the clade containing Eri-
ment of this latter transformation is ambiguous. The
achne, Aristidoideae, Danthonioideae, Arundino-loss of disarticulation above the glumes (char. 16)
ideae, and Chloridoideae (the Ligule of Hairs is a synapomorphy for Panicoideae excluding Dan-
Clade, as defined below), but other optimizations
thoniopsis. The presence of paired spikelets (char.
are possible. Two lodicules (char. 19) are estab-
9) is a synapomorphy of Andropogoneae in this

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412 Annals of the
Missouri Botanical Garden

analysis, but paired spikelets do occur withinrelationship

Pan- of these two clades is relatively mod-
iceae (e.g., Brachiaria, Digitaria, Paspalum). est. The gain of the NAD-ME C4 subtype (char. 48)
is a possible synapomorphy for the entire clade,
Centothecoideae. Monophyly of this subfamily
however, and if so it would then revert to C3 in M.
as currently constituted is not strongly supported in
rangei. The gain of chloridoid-type microhairs
this analysis. The secondary gain of an epiblast
(char. 44) is a synapomorphy for the traditional
(char. 35) is a possible synapomorphy (but is un-
Chloridoideae, although the character does occur
known for Thysanolaena), as is fusion of the styles
elsewhere in the PACCAD Clade, and many genera
(char. 28).
of chloridoids also include species with panicoid-
The Ligule of Hairs Clade (Eriachne + [[Aristi- type microhairs (Jacobs, 1987; Van den Borre,
doideae + Danthonioideae] + [Arundinoideae + 1994; Van den Borre & Watson, 1994). The peri-
Chloridoideae}]). The adaxial ligule as a fringe of carp is often free or loose, but this feature is not
hairs (char. 4), awned lemmas (char. 13), and com- uniform and is also found in non-chloridoid grass-
pound starch grains (char. 40) are synapomorphies es.

of this clade, but characters 4 and 13 reverse mul-

tiple times, and character 40 once, within this UNRESOLVED QUESTIONS
clade, as well as elsewhere on the tree (Fig. 3). The
Monophyly of Anomochlooideae. Anomochloa
recovery of this clade is a novel finding, but further
and Streptochaeta are each distinctive genera but
investigation is warranted, given the lack of se-
appear to have little in common. We have not yet
quence data for Eriachne. The transformation to
found a uniquely derived morphological character
embryonic leaf margins meeting (char. 38; Fig. 6L)
that unites them as members of a single clade. Al-
is an unreversed synapomorphy of the four subfam-
ilies above Eriachne. though the analyses presented here indicate that
the two form a monophyletic group, analyses of sin-
The Aristidoideae + Danthonioideae Clade.
gle data sets sometimes show them to be paraphy-
leticsup-
Although each of these subfamilies is well or unresolved (Mathews et al., 2000; Hilu et
al., 1999;isZhang, 2000). Because both genera oc-
ported as monophyletic, their sister relationship
another novel result, and one that is onlycupy
moder-
long branches in gene trees, they may form a
ately supported. Nonetheless, the presence of aonly
clade ba- because of long-branch attraction (Fel-
sic pattern of three awns (char. 14; Fig. 5C and F) 1978). Molecular studies of other species
senstein,
is an unreversed synapomorphy for this of Streptochaeta
clade. Re- would help break up the long
appearance of the distal membranous portionbranch to S. angustifolia and might affect the
of the
lodicules (char. 21) also may be a synapomorphy,
monophyly of the clade. Resolution of Anomochloa
and Streptochaeta as two separate basal lineages
although this reverses within the Danthonioideae.
obviously would affect interpretations of character
Aristidoideae. Gain of a germination flap (char.
evolution within the family.
17) and transformation to a base chromosome num-
ber of x = 11 (char. 47) are unambiguousPosition
syna- of Streptogyna. As noted in Results,
pomorphies for the clade. the position of Streptogyna is ambiguous, appar-
ently caused by lack of data. There are two species
Danthonioideae. The presence of haustorial
in the genus, one in the New World tropics and the
synergids (char. 32) is interpreted as an unreversed
other in Africa. Neither has been collected fre-
synapomorphy, but wider sampling within the clade
is needed.
quently, and we do not know of any plants in cul-
tivation. Morphologically, the genus would fit com-
fortably within the Bambusoideae, but molecular
Arundinoideae. No unambiguous morphologi-
data suggest that it is an early-diverging member
cal support for the monophyly of this subfamily was
found, although a reversal to hollow culms (char. of
2) the BEP Clade or the Ehrhartoideae. The char-
occurs in this clade. acters it shares with Bambusoideae are thus pre-
sumably ancestral, not indicative of relationship.
Chloridoideae. Chloridoideae, including Cen- Accurate placement of Streptogyna is necessary for
tropodia and Merxmuellera rangei, are supported
interpretation of character evolution in the early-
based on molecular data, although no clearcut mor-
diverging members of Bambusoideae, Ehrharto-
phological synapormorphies have been identified.ideae, and Pooideae.
Monophyly of Centropodia + M. rangei is well sup-
ported as is that of the traditional ChloridoideaeEarly-diverging Pooideae. The combined anal-
(i.e., Chloridoideae s. str.), but support for the sister
ysis confirms the position of Brachyelytrum as sister

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Volume 88, Number 3 Grass Phylogeny Working Group 413
2001 Phylogeny and Classification of Poaceae

to the rest of the Pooideae, and Lygeum + Nardus supported as monophyletic by our data. The list of
as the next-diverging lineage; both these results are genera included in and excluded from each sub-
well supported. The next diverging lineages include family, however, is based on a rather limited sample
Phaenosperma, Anisopogon, Stipeae, Ampelodesmos, of species and genera, combined with inferences
Meliceae, and Diarrheneae, but the order of diver- from classical morphological studies. In particular,
gence is not resolved by any data collected to date. the exact circumscriptions of Danthonioideae,
In the case of Phaenosperma, Anisopogon, Diar- Arundinoideae, and Centothecoideae are not pre-
rhena, and Ampelodesmos, the problem may be as- cisely determined by this study. A comprehensive
cribed to insufficient sequence data in this analysis. effort by multiple systematists is needed to improve
For our sample of Stipeae and Meliceae, however, understanding of the many poorly known species
appreciable sequence data are available, yet the and genera.
relative positions of the two lineages remain un-
Centothecoideae. Of the groups recognized here
clear. If the phylogenetic problem is indeed soluble
as subfamilies, Centothecoideae are the only one
with molecular data, the sample of genera and spe-
not strongly supported as monophyletic by the com-
cies in each tribe may have to be increased sub-
bined analysis. We have retained the subfamilial
stantially. A combined analysis of cpDNA restric-
name and expanded the circumscription to include
tion sites and morphology (Soreng & Davis, 2000)
Thysanolaena, formerly a member of the Arundi-
represents the broadest taxon sample for Pooideae noideae. As with the remainder of the PACCAD
among studies to date. The order of divergence of
Clade, a clear picture of the limits of the centothe-
these lineages affects interpretation of the evolution
coid clade depends on much more data, particu-
of such characters as parallel-sided subsidiary
larly on the remaining centothecoid genera, but a
cells, loss of microhairs, and trends in reduction of
study is under way (J. G. Sanchez-Ken, pers.
chromosome number (Kellogg, 1998). The latter
comm.).
may correlate with a marked increase in genome
size (Bennetzen & Kellogg, 1997) and may suggest Circumscription of tribes. This paper does not
possible mechanisms of genome evolution. address tribal circumscription. This will require far
more extensive sampling, particularly in Pooideae,
The PACCAD Clade. Relationships among the Panicoideae, Chloridoideae, and Bambusoideae,
major lineages in the PACCAD Clade are not re- which constitute the four largest subfamilies.
solved by this or any other phylogenetic analysis to Choice of outgroups for such studies is now clear,
date. In the combined analysis, the branches at the however.
base of the clade are short, marked by relatively
few mutations each (11, 41, and 16 steps; Fig. 1). Biogeography. Present-day distributions do not
This suggests that the PACCAD radiation may have indicate much about where the grasses originated.
occurred relatively rapidly. If this is true, then re- Restionaceae are clearly a Gondwanan group, with
lationships may remain difficult to resolve with cer- representatives in Africa and Australia. Joinville-
tainty. The clade also contains a number of taxa of aceae, however, are insular, occurring on Borneo,
New Caledonia, and Pacific Islands. The basal lin-
uncertain placement, many of which have received
little or no attention in phylogenetic studies. The
eages of the grasses are found in the tropical re-
tribe Eriachneae, which includes the Australian gions of South America, Africa, and Asia; the An-
omochlooideae are restricted to South and Central
genera Eriachne and Pheidochloa, is represented
America (Judziewicz & Soderstrom, 1989), the
here only by an rbcL sequence of Eriachne triodioi-
des and an ITS sequence of E. triseta. The genus
Pharoideae are pantropical (Soderstrom et al.,
1987), and the Puelioideae are restricted to tropical
Micraira, the only member of the Australian tribe
Africa (Soderstrom & Ellis, 1987; Clark et al.,
Micraireae, is represented only by an ndhF se-
2000). Due to the absence of an early fossil record,
quence of M. lazaridis and by an ITS sequence of
it is not clear how this distribution was established,
M. subulifolia. Such genera as Cyperochloa, Stey-
whether by long-distance dispersal across the At-
ermarkochloa, and the Crinipes group were not in-
lantic and Indian Oceans, or whether across a con-
cluded in this combined analysis. An rbcL se-
tinuous Gondwanan equatorial forest. Either way,
quence of Cyperochloa places it with the
the continent of origination cannot be determined
centothecoids, whereas a sequence of the crinipoid
with current data.
genus Styppeiochloa places it sister to Arundineae
s. str. (Barker, 1997; Linder et al., 1997). Timing and causes of diversification. The ear-
The subfamilies recognized within the PACCADliest unequivocal grass fossils are pollen grains
Clade are, except for Centothecoideae, strongly from the Paleocene of South America and Africa,

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414 Annals of the
Missouri Botanical Garden

deposited approximately 60 to 55 million years

consistent with available data, that the grasses
(my) ago (Jacobs et al., 1999), although some grains
achieved their Gondwanan distribution by dispersal
(Soreng & Davis, 1998), as has been suggested for
of Monoporites from the upper Maastrichtian (Cre-
taceous) may also represent remains of grasses other taxa with an apparent Gondwanan distribu-
tion (e.g., Adansonia, Baum et al., 1998; Atheros-
(Linder, 1987). The earliest known grass macrofos-
sil appears in an early Eocene formation (ca. 55
permataceae, Renner et al., 2000).
mya) in North America (Crepet & Feldman, 1991). The combination of fossil data and molecular
Based on the fossil record therefore, the family clock is evidence suggests that the major diversifica-
at least 55 my and possibly as much as 70 my tion old. of the grasses occurred between 15 and 25
Establishment of all major lineages had occurred mya, long after the origin of the family at 55 to 70
by the mid-Miocene (Jacobs et al., 1999), which mya.is This is consistent with the observed branch
about the time that grass-dominated ecosystems lengths
ap- on the phylogeny in Figure 1. There may
peared. have been many more representatives of the An-
Attempts to date particular nodes on the clado- omochlooideae, Pharoideae, and Puelioideae (or
gram using molecular clocks are confounded by even additional lineages) that are now extinct, but
non-clocklike behavior of several of the genes grasses are generally rare in the fossil record until
(Gaut et al., 1996, 1997; Mathews et al., 2000; Kel- the Miocene (Jacobs et al., 1999). The simplest ex-
logg & Russo, unpublished obs.). Using sequences planation is that the family diversified long after its
of GBSSI, which has been shown to exhibit clock- origin. The novel characters that arose after the di-
like mutation, Gaut and Doebley (1997) placed the vergence of Joinvillea-the caryopsis, differentiat-
divergence of maize and Pennisetum at 25 mya, ed embryo, reduction in perianth-therefore did
whereas Kellogg and Russo (unpublished) place the not lead immediately or directly to the current dom-
divergence of Danthoniopsis dinteri from the rest of inance of the family. Other characteristics acquired
the panicoids at ca. 16 mya. The two dates conflict later in the evolution of the family may have been
with each other, but do suggest that the PACCAD more important in its diversification and ecological
Clade originated in the early Miocene or late Oli- success. Possibilities include such characters as

gocene. formation of intercalary meristems or the acquisi-

All C4 lineages are included in the PACCAD tion of mechanisms for drought tolerance. We do
Clade, so paleontological evidence for C4 photosyn- not know the phylogenetic distribution of interca-
thesis can establish a minimum age for the common lary meristems, however, and it is possible that in-
ancestor of the clade. The earliest known C4 grass tercalary meristems of the leaves evolved after such
macrofossil is dated at 12.5 mya (Nambudiri et meristems
al., in the stems. This character needs to be
1978), and the earliest isotopic evidence for C4 investigated
is further. Acquisition of drought and
ca. 15 mya (Kingston et al., 1994; Latorre etheat al., tolerance would also be worth investigating,
1997). This suggests that the origin of the PACCAD but would require a precise definition of what is
Clade occurred no later than 15 mya and possibly meant by each term. The cellular components of
as early as 25 mya. such physiological responses are being identified
Both fossil data and molecular clock estimates and could perhaps be studied across a range of
seem at odds with the apparent Gondwanan distri- taxa.

bution of many grass taxa (see for example Simon

& Jacobs, 1990). The Gondwanan distribution of
CONCLUSIONS

such derived groups as the subfamily Danthonioi-

deae might suggest that the PACCAD Clade origi- We present here a resolved and strongly su
nated sometime before the breakup of Gondwana, ported phylogeny of the grass family. It can be u
which would then place the origin of the family to long understand the diversification of morpholog
before the earliest known fossils were deposited. genes, and genomes, to interpret comparative s
This cannot be ruled out, of course, because ities is of cereal crops and forage grasses, and to
an assumption based on negative evidence. If, how- velop hypotheses of adaptation to past and fut
ever, we assume that groups within the PACCAD environments. Some phylogenetic questions rem
Clade originated before the breakup of Gondwana unresolved, and these affect inferences about s
(a process hard to date precisely but perhaps important
100- characters as C4 photosynthesis. No
70 mya), then we would have to assume thattheless,
the this phylogeny is one of the most com
hensive and robust available for any family
family originated more than 200-140 mya, before
plants,
the time of the first appearance of angiosperms in making the grasses an excellent clade
the fossil record. It seems more likely, and more
studies of evolutionary pattern and process.

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Volume 88, Number 3 Grass Phylogeny Working Group 415
2001 Phylogeny and Classification of Poaceae

TAXONOMIC TREATMENT Thysanolaeneae placed in the Centothecoideae and

Gynerium as Incertae Sedis. Centropodia and Merx-
Twelve subfamilies are recognized formally inmuellera rangei are placed in Chloridoideae. Pooi-
this classification system (Table 1). A descriptiondeae have grown by inclusion of Brachyelytreae,
is provided for each subfamily, and where appro- Lygeeae, Nardeae, Phaenospermatideae, Diarrhe-
priate, synonymy is indicated. To permit easy com-neae, Stipeae, and Ampelodesmeae, all formerly
parison with previous work, we have listed for eachclassified within either Bambusoideae or Arundi-
subfamily which of the tribes recognized by Claytonnoideae by some authors; note, however, that Clay-
and Renvoize (1986) are to be included. In someton and Renvoize (1986) placed Lygeeae, Nardeae,
cases (e.g., Pharoideae or Danthonioideae), the newand Stipeae in Pooideae in agreement with the clas-
circumscription of subfamilies makes tribal recog-sification proposed here. A detailed comparison of
nition largely unnecessary. For example, the sub-the GPWG classification with the major grass clas-
family Pharoideae includes three genera in a singlesification systems of the 20th century is presented
tribe; the tribe is effectively redundant and servesin Table 1.
no useful function in the subfamilial classification.
Primary sources for suprageneric names were the
Nonetheless we list the names for comparison. STAR Database (http://matrix.nal.usda.gov:8080/
Our sample of taxa was explicitly designed to star/supragenericname.html), the Catalog of New
explore relationships among major clades that can World Grasses (http://mobot.mobot.org/W3T/
be recognized at the subfamilial level, but it is not
Search/nwgc.html), and Clayton and Renvoize
dense enough to evaluate tribal limits. We have in (1986). Diagnoses of the subfamilies were extracted
many cases combined molecular data from several from various sources including Clayton and Ren-
species to represent a genus (as is also commonly voize (1986) and Watson and Dallwitz (1992).
done for morphological analyses), and in a few cas-
Tribes in Chloridoideae and Panicoideae (except for
es have combined data from several genera that the exclusion of Eriachneae) follow the treatment
represent a putatively monophyletic group. Such
of Clayton and Renvoize (1986); tribes listed for
combinations assume, rather than test, monophyly. the other subfamilies generally are treated accord-
We therefore refrain from formal discussion of tribal
ing to more recent studies and/or consultation with
limits, which cannot be addressed by our (lata; specialists in those groups.
these limits will have to be re-evaluated by future
studies. Three tribes and two genera are placed Poaceae
as (R. Br.) Barnh., Bull. Torrey Bot. Club
Incertae Sedis at the end of the classification, al- 22: 7. 1895. (Nom. alt. Gramineae Juss., Gen.
though the genera may be provisionally placed as P1.: 28. 1789.)
noted below.
A monophyletic family, recognizable by the fol-
This classification reflects our attempt to use the
lowing synapomorphic morphological characters:
phylogeny as the basis for recognizing subfamilies
Inflorescence highly bracteate. Perianth reduced or
while remaining nomenclaturally conservative. Ex-
lacking. Pollen lacking scrobiculi, but with intraex-
cept for Centothecoideae, all subfamilies recog-
inous channels. Seed coat fused to inner ovary wall
nized are well supported as monophyletic in our
at maturity, forming a caryopsis. Embryo highly dif-
analyses. While we could create an unranked clas-
ferentiated with obvious leaves, shoot and root mer-
sification for the grasses using our phylogeny, we
istems, and lateral in position.
feel that the practical interests of the potential us-
ers of this classification currently are best served
I. Anomochlooideae Pilg. ex Potztal, in Willd-
by retaining the Linnaean hierarchy. Nonetheless enowia 1: 772. 1957. TYPE: Anomochloa
we have applied informal names to several of the
Brongn. Figure 4C and D.
well-supported clades (see above).
The most significant changes in our proposedSyn.: Streptochaetoideae (Nakai) Butzin, Neue Unter
Blute Gram.: 148. 1965.
subfamily classification are the breakup of the tra-
ditional Bambusoideae and Arundinoideae and the Plants perennial, rhizomatous, herbaceous, of
expansion of Pooideae. The diversity encompassed shaded tropical forest understories. Culms hollow
by the traditional Bambusoideae (or Bambusoideae or solid. Leaves with phyllotaxis either distichous
s.l.) is now recognized as Anomochlooideae, Phar- or spiral; abaxial ligule absent; adaxial ligule a
oideae, Puelioideae, Bambusoideae s. str., and Ehr-short fringe of cilia or absent, not membranous;
hartoideae. Elements of the traditional Arundino- blades usually relatively broad, venation parallel,
ideae are now recognized as Aristidoideae, with pseudopetioles short to very long, these with
Danthonioideae, and Arundinoideae s. str., with dark, turgid swellings (pulvini) at both ends (An-

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416 Annals of the
Missouri Botanical Garden

omochloa) or only at the summit (Streptochaeta);II. Pharoideae (Stapf) L. G. Clark & Judz., Taxon
sheaths non-auriculate. Inflorescences spicate, with45: 643. 1996. TYPE: Pharus P. Browne. Fig-
complicated branching patterns, bracts outside of ure 4B.

the spikelet equivalents present, large and with a

Syn.: Leptaspidoideae (Tzvelev) C. 0. Morales, Sendtnera
blade or small and bladeless, or absent. Ultimate
5: 244. 1998. Nom. superfl.
structures of the inflorescence (spikelet equiva-
lents) of uncertain homology with typical grass Plants perennial, rhizomatous, monoecious, her-
spikelets but one-flowered and bisexual; bracts baceous, of shaded tropical to warm temperate for-
within the spikelet equivalents with phyllotaxisest understories. Culms hollow or solid. Leaves dis-
dis-
tichous; abaxial ligule absent; adaxial ligule a
tichous or spiral, lacking uncinate macrohairs,
sometimes awned but if so, the awns single; fringed
lodi- membrane; blades resupinate, relatively
cules absent, or, in Anomochloa, their positionbroad,
oc- with pseudopetioles prominent and twisted,
cupied by a ring of short brownish cilia bornewith on lateral nerves diverging obliquely from mid-
a low membranous ring; stamens 4 or 6; ovary nervegla- and running straight to margins; sheaths non-
brous, apical appendage absent, haustorial syner-auriculate. Inflorescences paniculate, the main axis
gids presumed absent, style 1, stigma(s) 1 or and3.branches disarticulating or not, covered with
uncinate macrohairs, bracts outside of the spikelets
Caryopsis with the hilum linear, shallow and incon-
spicuous; endosperm hard, containing compound absent. Spikelets unisexual, one-flowered, mostly in
starch grains; embryo large, epiblast present or male-female
not, pairs on short branchlets, or some fe-
male spikelets solitary. Female spikelets large,
scutellar cleft present but shallow, mesocotyl inter-
short-stalked; glumes 2, shorter than the floret;
node absent, embryonic leaf margins overlapping
or not. Basic chromosome numbers: x = 11 or 18 lemma tubular or inflated, covered wholly or in part
(note: Clark & Judziewicz, 1996, erroneously cited
by uncinate macrohairs, awnless; palea well devel-
these as 12 or 18). oped; lodicules absent; ovary glabrous, apical ap-
pendage absent, haustorial synergids ptresumed ab-
Foliar anatomy. Mesophyll nonradiate, an sent,
ad- style 1, stigmas 3. Caryopsis with the hilum
axial palisade layer absent, with fusoid cells very
linear, extending the full length; end(osperm hard,
large and well developed, arm cells only weaklywithout lipid; embryo small, epiblast present, scu-
developed; Kranz anatomy absent; midrib complex;
tellar cleft present but shallow, mesocotyl internode
adaxial bulliform cells present. absent, embryonic leaf margins overlapping. Male
spikelets small, short- to long-stalked, membra-
Foliar micromorphology. Stomata with low
nous; glumes 2, shorter than the floret; lodicules 3
dome-shaped and triangular subsidiary cells; bi-
or 0, if present then minute, elliptic, glabrous, and
cellular microhairs very large (0.075-0.15 mm), the
nerveless; stamens 6. Basic chromosome number:
pointed apical cell usually one and a half times as
x= 12.
long as the basally constricted basal cell; papillae
absent. Foliar anatomy. Mesophyll nonradiate,
axial palisade layer absent, fusoid cells la
Photosynthetic pathway. Presumed C3. well developed, arm cells weakly to moderat
developed; Kranz anatomy absent; midrib c
INCLUDED TRIBES:
inflated adaxial interstomatal cells presen
form cells poorly developed or absent.
Anomochloeae C. E. Hubb., in Hutchinson, Fam.
Fl. P1. 2: 219. 1934. TYPE: Anomochloa Foliar micromorphology. Stomata with pa
Brong. sided to dome-shaped subsidiary cells; bic
Streptochaeteae C. E. Hubb., in Hutchinson, Fam. microhairs and papillae absent.
Fl. PI. 2: 205. 1934. TYPE: Streptochaeta
Schrad. ex Nees.
Photosynthetic pathway. Presumed C3.

INCLUDED TRIBE (NOW IDENTICAL TO SUBFA

Notes. There is no unique morphological syn-
apomorphy for this subfamily, but both tribesAND
lack THUS REDUNDANT):
lodicules and they apparently also lack grass-type
Phareae Stapf, in Thiselton-Dyer, Fl. Cap.
spikelets. As noted above (Unresolved Questions),1898. TYPE: Pharus P. Browne.
this lineage may not be monophyletic, in which
Notes. In his original description of the tribe,
case two subfamilies would need to be recognized.
The subfamily includes 4 species. Stapf specifically included Olyra (based on its uni-

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Volume 88, Number 3 Grass Phylogeny Working Group 417
2001 Phylogeny and Classification of Poaceae

sexual spikelets), but did not explicitly list Pharus axial palisade layer absent, fusoid cells well de-
or Leptaspis, although his choice of the name Phar- veloped, arm cells only weakly developed; Kranz
eae implicitly recognized the membership of Pha- anatomy absent; midrib complex or less commonly
rus in the tribe and automatically placed Pharus as simple; adaxial bulliform cells present.
its type, according to Article 10.6 of the Code
Foliar micromorphology. Stomata with dome-
(Greuter et al., 2000). As long as Olyra was re-
shaped to triangular subsidiary cells; microhairs
tained in the same tribe as Pharus, Phareae was a
absent (Puelia) or multicellular, uniseriate micro-
superfluous name for the Olyreae. When Pharus
hairs present (Guaduella); papillae present or more
and Leptaspis are segregated into their own tribe,
commonly absent.
and Olyra is excluded, then Phareae becomes the
valid, correct name for the tribe. Clark and Jud- Photosynthetic pathway. Presumed C3.
ziewicz (1996) based the name of the subfamily on
INCLUDED TRIBES:
this tribal name. Tzvelev (1989) argued that the
name Phareae was illegitimate because the type of Guaduelleae Soderstr. & R. P. Ellis, in Sod
the previously described tribe Olyreae was includ- et al. (editors), Grass Syst. Evol.: 238
ed in it, and provided the name Leptaspideae for TYPE: Guaduella Franch.
this tribe. Morales (1998) agreed with Tzvelev and Puelieae Soderstr. & R. P. Ellis, in Soderstrom et
rejected the name Pharoideae for this subfamily, al. (editors), Grass Syst. Evol.: 238. 1987.
according to Article 52.1 of the Code (Greuter et TYPE: Puelia Franch.
al., 2000), replacing it with Leptaspidoideae. Under
Article 52.3, however, "A name that was nomen- Notes. This subfamily, which comprises ap-
claturally superfluous when published is not ille- proximately 14 species, is poorly known, and mor-
gitimate ... if it is based on the stem of a legitimate phological, anatomical, cytological, and ecological
studies are needed.
generic name." We therefore accept the name Phar-
oideae for this subfamily, as Pharus is a legitimate
IV. Bambusoideae Luerss., Grundz. Bot., ed. 5:
generic name. The subfamily includes 12 species.
451. 1893. TYPE: Bambusa Schreb. Figures
4F, 6C, G, O, P, 7A.
III. Puelioideae L. G. Clark, M. Kobay., S. Ma-
thews, Spangler & E. A. Kellogg, Syst. Bot. 25: Syn.: ()lyroideae Pilger, Nat. Pfl.-Fam. ed. 2, 14(1: 168.
1956.
181-187. 2000. TYPE: Puelia Franch. Figure
4A. Parianoideae (Nakai) Butzin, Neue Unters. lIiite
(ram.: 148. 1965.

Plants perennial, rhizomatous, herbaceous, of

shaded rainforest understories. Culms hollow.
Plants perennial (rarely annual), rhizomatous
herbaceous or woody, of temperate and tropical for
Leaves distichous; abaxial ligule absent (Guaduel-
ests, tropical high montane grasslands, riverbank
la) or present (Puelia); adaxial ligule a fringed
and sometimes savannas. Culms hollow or solid.
membrane; blades relatively broad, pseudopetiola-
Leaves distichous; abaxial ligule absent (Olyreae)
te, venation parallel; sheaths non-auriculate. Inflo-
or present (Bambuseae); adaxial ligule membranous
rescences racemose or paniculate, bracts outside of
or chartaceous, fringed or unfringed; blades usually
the spikelets sometimes present. Spikelets with two
relatively broad, pseudopetiolate, venation parallel;
glumes and several florets, the 1 to 3 proximal flo-
sheaths often auriculate. Inflorescences spicate, ra-
rets male, the next several florets female-fertile,
cemose or paniculate, completing development of
with distal incomplete florets (Guaduella), or the
all spikelets in one period of growth and subtending
proximal 3 to 6 florets male or neuter with the sin-
bracts and prophylls usually absent, or pseudo-
gle distal floret female (Puelia), disarticulating
spikelets with basal bud-bearing bracts producing
above the glumes and between the florets (Guad-
two or more orders of spikelets with different phas-
uella) or not (Puelia); lemmas lacking uncinate ma-
es of maturity and subtending bracts and prophylls
crohairs, awnless; palea well developed, sometimes
usually present. Spikelets (or spikelets proper of
tubular; lodicules 3, membranous, ciliate; stamens
the pseudospikelets) bisexual (Bambuseae) or uni-
6; ovary glabrous or hairy, an apical appendage
sexual (Olyreae), consisting of 0, 1, 2 or several
present or not, haustorial synergids presumed ab-
glumes, 1 to many florets; lemma lacking uncinate
sent, styles 2 or 3, the bases close, stigmas 2 or 3.
macrohairs, if awned, the awns single; palea well
Caryopsis with a long-linear hilum; embryo small.
Basic chromosome number: x = 12.
developed; lodicules usually 3 (rarely 0 to 6 or
many), membranous, vascularized, often ciliate;
stamens usually 2, 3, or 6 (10 to 40 in Pariana, 6
Foliar anatomy. Mesophyll nonradiate, an ad-

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418 Annals of the
Missouri Botanical Garden

to 120 in Ochlandra); ovary glabrous or hairy, ittate (Phyllorachideae), somewhat broad to usually
sometimes with an apical appendage, haustorial narrow, sometimes pseudopetiolate, venation par-
synergids absent, styles 2 or 3, sometimes veryallel; sheaths sometimes bearing auricles. Inflores-
short but close, stigmas 2 or 3. Caryopsis withcences
hi- paniculate or racemose, bracts outside of
lum linear (or rarely punctate), extending its the
full spikelets rarely present (Humbertochloa).
Spikelets bisexual or unisexual, with glumes 2 (ab-
length (or rarely less than full length); endosperm
hard, without lipid, containing compound starchsent in some Oryzeae), sterile florets 0 to 2, and
female-fertile floret 1, disarticulating above the
grains; embryo small, epiblast present, scutellar
glumes or infrequently primary branches disartic-
cleft present, mesocotyl internode absent, embry-
onic leaf margins overlapping. Basic chromosomeulating as units; lemma lacking uncinate macro-
numbers: x = 7, 9, 10, 11, and 12. hairs, if awned, the awn single; palea well devel-
oped; lodicules 2, membranous or rarely fleshy,
Foliar anatomy. Mesophyll nonradiate, an ad-
heavily vascularized; stamens usually 3 or 6 (some-
axial palisade layer absent, fusoid cells large and
times 1, 2, or 4); ovary glabrous, apical appendage
well developed, arm cells usually well developed
absent, haustorial synergids absent, styles 2, free,
and strongly invaginated; Kranz anatomy absent;
fused basally or for their full length (Zizaniopsis),
midrib complex or simple; adaxial bulliform cells
close, stigmas 2. Caryopsis with the hilum long-
present.
linear; endosperm hard, without lipid, containing
Foliar micromorphology. Stomata with dome- compound starch grains (rarely simple); embryo
shaped, triangular, or parallel-sided subsidiary small, epiblast usually present (absent in Ehrhar-
cells; bicellular microhairs present, panicoid-type; ta), scutellar cleft usually present (absent in Leersia
papillae common and abundant. and Potamophila), mesocotyl internode absent (pre-
sent but short in Microlaena), embryonic leaf usu-
Photosynthetic pathway. C3.
ally with overlapping margins (meeting in Pota-
INCIUDED TRI:LS:
mophila). Basic chromosome numbers: x = 12 (10
in Microlaena; 15 in Zizania).
Bambuseae Dumort., Anal. Fam. Pi.: 63. 1829.
TYPE: Bamuttsa Schreb. Foliar anatomy. Mesophyll nonradiate, an ad-
axial palisade layer usually absent, fusoid cells ab-
Olyreae Kunth ex Spenn., Fl. Friburg. 1: 172.
sent or sometimes present (Zizania and Zizaniop-
1825. TYPE: Olyra L. (Including Buerger-
sis), arm cells absent or present; Kranz anatomy
siochloeae Blake, Blumea, Suppl. 3: 62. 1946;
absent; midrib simple or complex; adaxial bulliform
Parianeae C. E. Hubbard, in Hutch., Fam. Fl.
cells present.
P1. 2: 219. 1934.)
Foliar micromorphology. Stomata with dome-
Notes. The current circumscription of this sub-
shaped or triangular subsidiary cells; bicellular mi-
family is much narrower than the traditional view.
crohairs present, panicoid-type; papillae often pre-
In their recent analysis, Zhang and Clark (2000)
sent in Oryzeae, otherwise absent.
recovered two robustly supported clades, the oly-
roid bamboos and the woody bamboos, which theyPhotosynthetic pathway. C3.
recognized as tribes Olyreae and Bambuseae, re-
INCLUDED TRIBES:
spectively. Following Zhang and Clark (2000),
Buergersiochloeae and Parianeae are included in
Ehrharteae Nevski, Trudy Bot. Inst. Akad.
Olyreae. This subfamily includes approximately SSSR 4: 227. 1937. TYPE: Ehrharta Thunb.
1200 species. Oryzeae Dumort., Observ. Gramin. Belg.: 83. 1824.
TYPE: Oryza L.
V. Ehrhartoideae Link, Hort. Berol. 1: 233.
Phyllorachideae C. E. Hubb., in Hook. Ic. P1. 34:
1827. TYPE: Ehrharta Thunb. Figure 4G. t. 3386, p. 5. 1939. TYPE: Phyllorachis Tri-
men.
Syn.: Oryzoideae Kunth ex Beilschm., Flora 16(2): 52,
109. 1833.
Notes. Although we did not sample Phy
Plants annual or perennial (rhizomatous or sto- we place it here based on morpholo
ideae,
loniferous), herbaceous to suffrutescent, of forests,
ilarity. Nonetheless, any future studies of
should
open hillsides, or aquatic habitats. Culms hollow or include this tribe to test its relat
solid. Leaves distichous; abaxial ligule absent; ad-
Ehrharteae and Oryzeae. Under the presen
axial ligule a fringed or unfringed membrane, scription,
or a this subfamily includes appr
120
fringe of hairs; blades rarely basally cordate or sag-species.

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Volume 88, Number 3 Grass Phylogeny Working Group 419
2001 Phylogeny and Classification of Poaceae

VI. Pooideae Benth., Fl. Hongk. 407. 1861. or circular and less than 1/3 the length of the fruit;
TYPE: Poa L. Figures 4E, H, 6D, J, L, 7B. endosperm hard or sometimes soft or liquid (some
Poeae), with or without lipids (some Poeae), con-
Syn.: Avenoideae Link, Hort. Berol. 1: 108. 1827.
Festucoideae Link, Hort. Berol. 1: 137. 1827.
taining compound starch grains, or simple starch
Glycerioideae Link, Hort. Berol. 1: 160. 1827. grains (Brachyelytreae, Bromeae, Triticeae, some
Echinarioideae Link, Hort. Berol. 1: 197. 1827. Stipeae); embryo small, epiblast present (rarely ab-
Cynosuroideae Link, Hort. Berol. 1: 198. 1827. sent), scutellar cleft absent (rarely present, but not
Anthoxanthoideae Link, Hort. Berol. 1: 232, 271. 1827.
deeply incised), mesocotyl internode absent (rarely
Agrostidoideae Kunth ex Beilschm., Flora (Beib.) 16(2):
52, 104. 1833. short, Brachyelytrum), embryonic leaf margins
Stipoideae Burmeist., Handb. Naturgesch. 199. 1837. meeting (infrequently margins overlapping). Basic
Hordeoideae Burmeist., Handb. Naturgesch. 202. 1837. chromosome numbers: x = 7 (Bromeae, Triticeae,
Phalaroideae Burmeist., Handb. Naturgesch. 208. Poeae generally, few Brachypodieae), 2, 4, 5, 6, 8,
1837.
Secaloideae Rouy, Fl. France 14: 2, 298. 1913.
9, 10, 11, 12, 13 represented in a few Poeae and
the other tribes, generally medium or large.
Plants annual or perennial (rhizomatous, stolon-
iferous, or neither), herbaceous, of cool temperateFoliar anatomy. Mesophyll nonradiate, an ad-
and boreal regions, extending across the tropics axial
in palisade layer absent, fusoid cells absent, arm
the high mountains. Culms hollow (rarely solid). cells absent; Kranz anatomy absent; midrib simple;
Leaves distichous; abaxial ligule absent; adaxialadaxial bulliform cells present.
ligule scarious or membranous, the margin not or
Foliar micromorphology. Stomata with parallel-
infrequently short ciliate fringed (rarely long cili-
sided subsidiary cells; bicellular microhairs absent
ate, Anisopogon); blades somewhat broad to usually
(rarely present, Lygeum, where chloridoid, Nardus,
narrow, rarely pseudopetiolate (Phaenosperma), ve-
where panicoid), unicellular microhairs absent
nation parallel; sheaths sometimes auriculate. In-
(rarely present, few Stipeae); papillae usually ab-
florescences spicate, racemose, or paniculate,
sent, when present rarely more than one per long
bracts outside of the spikelets absent or rarely pre-
cell.
sent (e.g., Sesleria, Echinaria, Ammochloa). Spike-
lets bisexual, infrequently unisexual or mixed, usu-Photosynthetic pathway. C3.
ally with two glumes (rarely without glumes,
Lygeum, or the first absent, Hainardia, Lolium, INCI,LUDI)E! TRIEKS:

Nardus, except on terminal spikelets), 1 to many

female-fertile florets with apical or infrequentlyAmpelodesmeae (Conert) Tutin, Bot. J. Linn. Soc
basal reductions, compressed laterally, infrequently 76: 369. 1978. TYPE: Ampelodesmos Link.
not or dorsally compressed, disarticulating above Brachyelytreae Ohwi, Bot. Mag. Tokyo 55: 361
the glumes (infrequently below the glumes, some 1941. TYPE: Brachyelytrum P. Beauv.
Brachypodieae (Hack.) Hayek, Oesterr. Bot. Z
Poeae, or at the nodes of the inflorescence, various
genera); lemma lacking uncinate macrohairs, if 74(10): 253. 1925. TYPE: Brachypodium P.
awned, the awn single; palea usually present and Beauv.
well developed, but variable and sometimes very Bromeae Dumort., Observ. Gramin. Belg.: 83.
reduced or absent; lodicules 2 (rarely 3, Anisopo- 1824. TYPE: Bromus L.
gon, Ampelodesmeae, many Stipeae and few Poeae; Brylkinieae Tateoka, Canad. J. Bot. 38: 962. 1960.
fused, Meliceae; rarely absent, Lygeum, Nardus, TYPE: Brylkinia F. Schmidt.
and few Poeae), usually lanceolate, broadly mem- Diarrheneae (Ohwi) C. S. Campb., J. Arnold Arbor.
branous apically (fleshy, truncate, Meliceae), often 66: 188. 1985. TYPE: Diarrhena P. Beauv.
lobed (Triticeae, Poeae), obscurely few-nerved, Lygeeae
or J. Presl, Wsobecny Rostl. 2: 1708, 1753.
infrequently + distinctly few-nerved, not or con- 1846. TYPE: Lygeum Loefl. ex L.
spicuously ciliate on the margins; stamens usuallyMeliceae Link ex Endl., Fl. Poson.: 116. 1830. [as
3 (infrequently 1 or 2); ovary glabrous or pubes- "Melicaceae"] TYPE: Melica L.
cent, rarely with an apical appendage (Bromus, Nardeae W. D. J. Koch, Syn. Fl. Germ. Helv.: 830.
Diarrhena) or rostellum (e.g., Brachyelytrum, Ros- 1837. TYPE: Nardus L.
Phaenospermatideae Renvoize & Clayton, Kew
traria), haustorial synergids absent, styles usually
2, close, stigmas 2 (rarely 1, Lygeum, Nardus, and Bull. 40: 478. 1985. TYPE: Phaenosperma
a few others, or 3, scattered genera). Caryopsis with Munro ex Benth.
the hilum linear and up to as long as the fruit, Poeae
or R. Br., Voy. Terra Austral. 2: 582. 1814.
subbasal and punctiform, linear, ellipsoidal, ovate, TYPE: Poa L. (Including Aveneae Dumort.,

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420 Annals of the
Missouri Botanical Garden

fusoid cells absent, arm cells absent; Kranz anat-

Observ. Gramin. Belg.: 82. 1824; Agrostideae
Dumort., Observ. Gramin. Belg.: 83. 1824.)
omy absent (Sartidia) or present (Stipagrostis, Ar-
Stipeae Dumort., Observ. Gramin. Belg.: 83.istida),
1824 when present with one (Stipagrostis) or two
[as "Stipaceae"]. TYPE: Stipa L. (Aristida) parenchyma sheaths, although both not
Triticeae Dumort., Observ. Gramin. Belg.: 82, 84, well developed throughout the genus; mid-
equally
91. 1824. TYPE: Triticum L. rib simple; adaxial bulliform cells present.

Notes. Relationships among some of the major Foliar micromorphology. Stomata dome-shaped
lineages of the core Pooideae clade remainorunre- triangular; bicellular microhairs present, pani-
solved, and conflicts between molecular data coid-type;
and papillae absent.
morphologically based tribal classifications exist
Photosynthetic pathway. C3 (Sartidia); C4 (Ar-
(e.g., Poeae vs. Aveneae; see Soreng & Davis,
istida, NADP-ME; Stipagrostis, not biochemically
2000). This is one of several reasons that we do not
typed, but anatomically NAD-ME; Hattersley &
offer a formal classification of tribes at this point.
Watson, 1992).
Relationships among the earlier diverging lineages
of the whole pooid clade are only weakly supported,
INCLUDED TRIBE (NOW IDENTICAL TO THE
and also require further investigation. The tribal
SUBFAMILY AND THUS REDUNDANT):
classification presented here is almost certain to
change as additional data accumulate, and thusAristideae C. E. Hubbard, in Bor, Grasses Burma,
should be taken only as an indication of the taxa Ceylon, India & Pakistan: 685. 1960. TYPE:
included within the subfamily. The subfamily in- Aristida L.

cludes approximately 3300 species.

Notes. The presence of a basal column of the
awn is a potential morphological synapomorphy for
VII. Aristidoideae Caro, Dominguezia 4: 16. this clade. Sartidia diverges from Stipagrostis and
1982. TYPE: Aristida L. Figure 5C. Aristida in other respects, and should be sampled
Plants annual or perennial, caespitose, herba-in future analyses. The subfamily includes approx-
ceous, xerophytic or less commonly mesophytic, ofimately 350 species.
temperate, subtropical and tropical zones, often in
open habitats. Culms solid or hollow. Leaves dis-VIII. Arundinoideae Burmeist., Handb. Natur-
tichous; abaxial ligule absent or present as a line gesch.: 204. 1837. TYPE: Arundo L. Figure
5A.
of hairs; adaxial ligule a fringed membrane or a
fringe of hairs; blades relatively narrow, without Syn.: Phragmitoideae Parodi ex Caro, Dominguezia 4: 13.
pseudopetioles, venation parallel; sheaths non-au- 1982.
riculate. Inflorescences paniculate, bracts outside
Plants perennial (rarely annual), rhizomatous,
of the spikelets absent. Spikelets with bisexual flo-
stoloniferous, or caespitose, herbaceous to some-
rets, glumes 2, female-fertile floret 1, and no rach-
what woody, of temperate and tropical areas, me-
illa extension, cylindrical or laterally compressed,
sophytic or xerophytic, the reeds found in marshy
disarticulating above the glumes; lemma with three
habitats. Culms hollow or less commonly solid.
awns, the awns separate from each other, or fused
Leaves distichous; abaxial ligule absent or rarely
below into a twisted column; palea short, less than
present as a line of hairs (Hakonechloa); adaxial
half the lemma length; lodicules present or rarely
ligule a fringed or unfringed membrane or a fringe
absent, when present 2, free, membranous, gla-
of hairs; blades relatively broad to narrow, without
brous, heavily vascularized; stamens 1 to 3; ovary
pseudopetioles, venation parallel; sheaths usually
glabrous, apical appendage absent, haustorial syn-
non-auriculate. Inflorescences usually paniculate,
ergids absent, styles 2, free, close, stigmas 2. Cary-
rarely spicate or racemose, bracts outside of the
opsis with the hilum short or long-linear; endo-
spikelets absent. Spikelets with bisexual florets,
sperm hard, without lipid, containing compound
glumes 2, a sterile lemma sometimes present, fe-
starch grains; embryo small (Sartidia) or large (Ar-
male-fertile florets 1 to several, apical reduction
istida, Stipagrostis), epiblast absent, scutellar cleft
usually present, usually laterally compressed, dis-
present or absent (Sartidia), mesocotyl internode
articulating above the glumes; lemma lacking un-
elongated, embryonic leaf margins meeting. Basic
chromosome numbers: x = 11, 12. cinate macrohairs, if awned, awn usually single,
sometimes awns three, but then lacking a basal col-
Foliar anatomy. Mesophyll radiate or nonra-umn; palea usually well developed; lodicules 2,
diate (Sartidia), an adaxial palisade layer absent,
free (rarely joined at the base), fleshy, glabrous or

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Volume 88, Number 3 Grass Phylogeny Working Group 421
2001 Phylogeny and Classification of Poaceae

infrequently ciliate, not or scarcely vascularized to monophyletic arundinoid clade, although Linder et
heavily vascularized; stamens (1 to)3; ovary gla- al. (1997) linked Arundo, Phragmites, and Molinia
brous, apical appendage absent, haustorial syner- by the presence of hollow culm internodes, a punc-
gids absent, styles 2, usually free, close, stigmas 2. tiform hilum, and convex adaxial rib sides in the
Caryopsis with the hilum short or long-linear (Mol- leaf blade. This subfamily clearly requires further
inia); endosperm hard, without lipid, containing study. The subfamily includes 33 to 38 species,
compound starch grains; embryo large or small counting the crinipoids.
(Amphipogon), epiblast absent, scutellar cleft pre-
sent, mesocotyl internode elongated, embryonic leaf IX. Danthonioideae Barker & H. P. Linder, sub-
margins meeting or overlapping (Hakonechloa). Ba- fam. nov. TYPE: Danthonia DC. Fl. Franc. 3:
sic chromosome numbers: x = 6, 9, 12. 32. 1805. Figure 5F.

Foliar anatomy. Mesophyll nonradiate or rarely Haec subfamilia ab aliis subfamiliis Poacearum syner-
radiate (Arundo, Amphipogon), without an adaxial gidis haustorialibus, ligula ciliata, embryone mesocotyle-
palisade layer, without fusoid cells, arm cells ab- done praedito, spicula pluriflora vel si uni- vel biflora
nunc rhachilla in extensionem desinente, stylorum basi-
sent or present (Phragmites); Kranz anatomy ab- bus plerumque distantibus atque anatomia "Kranz" et mi-
sent; midrib simple; adaxial bulliform cells present. cropilis chloridoideis carentibus bene distincta.
Distinct from the other subfamilies of the grasses by the
Foliar micromorphology. Stomata with low haustorial synergids, and by the conjunction of a ciliate
dome-shaped or triangular subsidiary cells; bicel- ligule, the presence of an embryo mesocotyl, a several-
lular microhairs present or less commonly absent, flowered spikelet, which, if 1- or 2-flowered, has a rachilla
extension, usually distinctly separated style bases, the ab-
when present of panicoid-type except in Amphipo-
sence of Kranz anatomy, and the absence of chloridoid
gon, which has unique microhair morphology; pa- microhairs.
pillae absent except in Amphipogon.
Plants perennial (caespitose, rhizomatous or sto-
Photosynthetic pathway. C,. loniferous) or less commonly annual, herbaceous or
rarely suffrutescent, of mesic to xeric open habitats
INCLUDEI) TRIBE (NOW II)FNTICA, T() SU3BFAMIL,Y in grasslands, heathlands, and open woodlands.
AND THUS REDUNI)ANT): Culms solid or very rarely hollow. Leaves disti-
chous; abaxial ligule usually absent (sometimes
Arundineae Dumort., Obs. Gram. Belg.: 82. 1824.
TYPE: Arundo L. present in Cortaderia, Karroochloa, and Pentas-
chistis); adaxial ligule a fringe of hairs or a fringed
Notes. The traditional Arundinoideae were well membrane; blades relatively narrow, without a
known as a dustbin group (e.g., Clayton & Renvo- pseudopetiole, venation parallel; sheaths not auric-
ize, 1986; Kellogg & Campbell, 1987). A number ulate except in Pentameris thuarii. Inflorescences
of studies indicated that this subfamily as tradi-
paniculate or less commonly racemose or spicate,
bracts outside of the spikelets absent (but the sub-
tionally circumscribed was polyphyletic (e.g., Bark-
er et al., 1995; Clark et al., 1995), although some
tending leaf + spatheate and disarticulating with
support for a monophyletic Arundinoideae (includ-the inflorescence in Tribolium pusillum). Spikelets
ing Arundinoideae s. str., Danthonioideae, Aristi-
bisexual (but sometimes without bisexual florets in
doideae, Micraira, and Eriachne) was found by Cortaderia) or unisexual (Cortaderia, Lamprothyr-
Hsiao et al. (1999). The results of the combined sus), glumes 2 and usually equal, female-fertile flo-
rets 1 to 6(to 20), with apical reduction and a rach-
analysis presented here suggest that a monophyletic
core arundinoid group does exist, even though illain- extension usually present, laterally compressed,
disarticulating above the glumes and between the
dividual data sets do not strongly support the group.
The exact generic membership of the subfamilyflorets,
re- less commonly below the glumes; lemma
mains to be determined; however, we include lackingthe uncinate macrohairs, awn single and from
following genera: Amphipogon, Arundo, Dregeo- a sinus; palea well developed, sometimes relatively
chloa, Hakonechloa, Molinia (and Moliniopsisshort; if lodicules 2, free (rarely joined), fleshy or
recognized), and Phragmites. We provisionally rarely with an apical membranous flap, glabrous or
place the crinipoid group (Crinipes, Dichaetaria,ciliate, often with microhairs, sometimes heavily
Elytrophorus, Leptagrostis, Nematopoa, Piptophyl-vascularized; stamens 3; ovary glabrous or rarely
lum, Styppeiochloa, and Zenkeria) here as well, with apical hairs (Pentameris), apical appendage
based on molecular evidence from Linder et al. absent, haustorial synergids present, only weakly
(1997) and Barker (1997). No morphological syn- developed in a few taxa, styles 2, the bases usually
apomorphies have been identified to support the separated, stigmas 2. Caryopsis with the hi-
widely

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422 Annals of the
Missouri Botanical Garden

lum short or long-linear; endosperm hard, contain-

perate woodlands and tropical forests. Culms solid
ing compound starch grains (simple in Prionan-
or hollow. Leaves distichous; abaxial ligule absent
thium); embryo large or small, epiblast absent,
or present as a line of hairs (Calderonella, Thysan-
olaena); adaxial ligule membranous or ciliate, or
scutellar cleft present, mesocotyl internode elon-
membranous with ciliate margins; blades relatively
gated, embryonic leaf margins meeting (overlapping
broad to narrow, often pseudopetiolate, venation
in Danthonia decumbens). Basic chromosome num-
bers: x = 6, 7, 9. parallel; sheaths sometimes auriculate. Inflores-
cences racemose or paniculate, bracts outside of
Foliar anatomy. Mesophyll nonradiate, an ad-
the spikelets absent. Spikelets bisexual or unisex-
axial palisade layer absent, fusoid cells absent, arm
ual, (1 to)2- to many-flowered with reduction either
cells absent; Kranz anatomy absent; midrib simple,
above or below the fertile florets, often compressed
usually with one bundle, an arc of bundles in Cor-
laterally; lemma lacking uncinate macrohairs, if
taderia; adaxial bulliform cells present or absent.
awned, the awn single; palea usually well devel-
Foliar micromorphology. Stomata with dome- oped, sometimes relatively short; lodicules 2 or ab-
shaped or parallel-sided subsidiary cells (rarelysent, + cuneate, many-nerved or less commonly not
high dome-shaped or slightly triangular); bicellular
or scarcely vascularized; stamens (1 to)2 or 3; ovary
microhairs present, panicoid-type, sometimesglabrous,
ab- apical appendage absent, haustorial syn-
ergids
sent; papillae usually absent but often present in presumed absent, styles 2, free or fused,
Chionochloa and Merxmuellera. close, stigmas 2. Caryopsis with the hilum basal,
punctiform; endosperm hard, without lipid, contain-
Photosynthetic pathway. C3.
ing simple or compound starch grains; embryo
small or large, the epiblast present, scutellar cleft
INCLUDED TRIBE (NOW IDENTICAL TO SUBFAMILY
present, mesocotyl internode present, embryonic
AND THUS REDUNDANT):
leaf margins overlapping. Basic chromosome num-
ber: x = 12 (x = 11 or 12? in Thysanolaena).
Danthonieae Zotov, New Zealand J. Bot. 1 (1): 86.
1963. (Including Cortaderieae Zotov, New Zea-
Foliar anatomy. Mesophyll nonradiate, often
land J. Bot. 1 (1): 83. 1963.) TYPE: Danthonia
DC. with an adaxial palisade layer, fusoid-like cells fre-
quently present as extensions of the outer paren-
Notes. The presence of haustorial synergids inchyma bundle sheath, arm cells absent; Kranz anat-
the ovule and distant styles support the monophyly omy absent; midrib simple; adaxial bulliform cells
of this clade (Verboom et al., 1994). Bilobed pro- large.
phylls also may be a synapomorphy, but this feature
has not been investigated sufficiently in the rest of Foliar micromorphology. Stomata with dome-
the family. The results of this study indicate robustshaped and/or triangular subsidiary cells; bicellular
molecular support for the monophyly of this clade microhairs present, panicoid-type; papillae absent.
(excluding Centropodia and Merxmuellera rangei), Photosynthetic pathway. C3.
but its placement within the larger PACCAD Clade
is equivocal. Pending further studies of the diver- INCLUDED TRIBES:
sity of the danthonioid grasses, we recognize only
one tribe, which includes the following genera (sen- Centotheceae Ridl., Mat. Fl. Malay Pen. 3:
su Barker et al., 2000): Austrodanthonia, Chaeto- 1907. TYPE: Centotheca P. Beauv.

bromus, Chionochloa, Cortaderia, Danthonia, Joy-Thysanolaeneae C. E. Hubb., in Hutch., Fam. Fl.

cea, Karroochloa, Lamprothyrsus, Merxmuellera P1. 2: 222. 1934. TYPE: Thysanolaena Nees.
(minus M. rangei), Notochloe, Notodanthonia, Pen-
Notes. Support for the monophyly of this sub-
tameris, Pentaschistis, Plinthanthesis, Prionan-
family as recognized here is moderate, and no mor-
thium, Pseudopentameris, Rytidosperma, Schismus,
phological synapomorphies have been identified.
and Tribolium. The subfamily includes approxi-
The sister relationship between the centothecoid
mately 250 species.
and panicoid clades, however, is relatively robust.
The positions of Gynerium and Danthoniopsis are
X. Centothecoideae Soderstr. [as "Centostecoi-
unstable. A majority of the Centotheceae are char-
deae"], Taxon 30: 615. 1981. TYPE: Cento-
acterized by unusual leaf anatomy, including the
theca Desv. Figure 5G.
presence of palisade mesophyll and laterally ex-
Plants annual or perennial (rhizomatous or sto-tended bundle sheath cells. Additional study of this
loniferous), herbaceous or reedlike, of warm tem-clade is under way (J. G. Sanchez-Ken, pers.

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Volume 88, Number 3 Grass Phylogeny Working Group 423
2001 Phylogeny and Classification of Poaceae

comm.). The subfamily includes approximately 45 lar or dome-shaped subsidiary cells; bicellular mi-
species. crohairs present, panicoid-type, rarely absent; pa-
pillae absent or present (mostly in the
XI. Panicoideae Link, Hort. Berol. 1: 202. 1827. Andropogoneae).
TYPE: Panicum L. Figures 5B, E, 6F, I, K. Photosynthetic pathway. C3, C4 (PCK, NAD-ME
Syn.: Andropogonoideae Burmeist., Handb. Naturgesch.:
201. 1837. and NADP-ME), and some C3/C4 intermediates.
Rottboellioideae Burmeist., Handb. Naturgesch.: 202.
1837. INCLUDED TRIBES:

Saccharoideae (Rchb.) Horan., Char. Ess. Fam.: 34.

1847. Andropogoneae Dumort. [as "Andropogineae"
serv. Gramin. Belg.: 84. 1824. TYPE: An
Plants annual or perennial (rhizomatous, stolon- pogon L.
iferous, caespitose or decumbent), primarily her- Arundinelleae Stapf, Fl. Cap. 7: 314. 1898.
baceous, of the tropics and subtropics, but also di- Arundinella Raddi.
verse in the temperate zone. Culms solid or less
Hubbardieae C. E. Hubb., in Bor, Grasses India
commonly hollow. Leaves distichous; abaxial ligule Burma Ceylon Pakistan: 685. 1960. TYPE:
usually absent, occasionally present as a line of Hubbardia Bor.
hairs; adaxial ligule a fringed or unfringed mem-
Isachneae Benth., J. Linn. Soc. Bot. 19: 30. 1881.
brane, or a fringe of hairs, or sometimes absent; TYPE: Isachne R. Br.
blades relatively broad to narrow, sometimes pseu- Paniceae R. Br., Voy. Terra Austr. 2: 582. 1814.
dopetiolate, venation parallel; sheaths usually non- TYPE: Panicum L.
auriculate. Inflorescences panicles, racemes, or Steyermarkochloeae Davidse & R. P. Ellis, Ann.
spikes, or complex combinations of these, bracts Missouri Bot. Gard. 71: 994. 1984. TYPE:
outside of the spikelets present (Andropogoneae) or Steyermarkochloa Davidse & R. P. Ellis.
absent (Paniceae). Spikelets bisexual or unisexual
Notes. While support for the panicoid/centothe
(if the latter plants dioecious or monoecious), fre-
coid clade is high, relationships within the clad
quently paired in combinations with long and short
remain unclear. No robust phylogeny for the Pani
pedicels, usually with glumes 2, sterile lemma 1,
coideae is yet available, although work is in pro
and female-fertile floret 1, dorsally compressed or
gress (Giussani et al., in press; Duvall et al., in
less commonly not compressed or laterally com-
press). Preliminary results indicate that the Pan
pressed, disarticulating below the glumes (above
ceae as currently circumscribed may not be mono
the glumes in Arundinelleae) or the inflorescence
phyletic, and that the large genus Panicum is poly
axes breaking apart; lemma lacking uncinate ma-
phyletic (Zuloaga et al., 2000; G6mez-Martinez &
crohairs, if awned, the awn single; palea well de-
Culham, 2000). Andropogoneae + Arundinella ap
veloped (Paniceae) or reduced to absent (Andro-
pear to be monophyletic (Spangler et al., 1999
pogoneae); lodicules 2 or sometimes absent,
other genera of the Arundinelleae are likely to be
cuneate, free, fleshy, usually glabrous; stamens 3;
distributed among the Andropogoneae, Paniceae
ovary usually glabrous, apical appendage absent,
and perhaps even the Centothecoideae (Kellogg
haustorial synergids absent, styles 2, free or fused,
2000b). This subfamily includes approximately
close, stigmas 2 (rarely 1 or 3). Caryopsis with the
3270 species.
hilum usually short; endosperm hard, without lipid,
containing simple or less commonly compound
XII. Chloridoideae Kunth ex Beilschm., Flora
starch grains; embryo usually large, epiblast absent
16(2): 52, 105. 1833. TYPE: Chloris Sw. Fig-
or rarely present, scutellar cleft present, mesocotyl
ures 5D, H, 6E, M, N, 7C.
internode elongated, embryonic leaf margins over-Syn.: Pappophoroideae Burmeist., Handb. Naturgesch.
lapping or rarely meeting. Basic chromosome num- 205. 1837.
bers: x = 5, (7), 9, 10, (12), (14). Eragrostoideae Pilger, Nat. Pfl.-Fam. ed. 2, 14d: 167.
1956.

Foliar anatomy. Mesophyll radiate or nonra-

Plants annual or perennial (rhizomatous, stolon-
diate, an adaxial palisade layer absent, fusoid cells
absent except in Homolepis and Streptostachys, arm
iferous, caespitose or decumbent), herbaceous
(rarely woody), of dry climates, especially in the
cells usually absent; Kranz anatomy present or ab-
tropics and subtropics, also found in the temperate
sent; midrib simple or rarely complex; adaxial bul-
zone. Culms solid or hollow. Leaves distichous; ab-
liform cells present.
axial ligule usually absent, rarely present as a line
Foliar micromorphology. Stomata with triangu-of hairs; adaxial ligule a fringed or less commonly

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424 Annals of the
Missouri Botanical Garden

unfringed membrane; blades relatively narrow, INCERTAE SEDIS:

without pseudopetioles, venation parallel; sheaths

Centropodia Reichenb., Merxmuellera rangei
usually non-auriculate. Inflorescences paniculate,
Conert
paniculate with spicate branches, racemose, or spi-
cate, bracts outside of the spikelets absent. Spike-
Notes. Reduction in the number of veins in the
lets bisexual or sometimes unisexual (if so the lemma is a general trend within the subfamily but
plants dioecious or monoecious), with glumes is 2,
clearly not a synapomorphy. Except for the C3
rarely a sterile lemma, and female-fertile florets 1
Eragrostis walteri and Merxmuellera rangei, the
to many, apical reduction usually present, usually
Chloridoideae are uniformly C4 with both the NAD-
laterally compressed, sometimes dorsally com- ME and PCK subtypes. The current tribal classifi-
cation for this subfamily conflicts with molecular
pressed, usually disarticulating above the glumes
data and is likely to be modified (Hilu et al., 1999).
(below in a few Eragrostis species); lemma lacking
uncinate macrohairs, if awned, the awns single This
or subfamily includes approximately 1400 spe-
if multiple, lacking a basal column; palea wellcies.
de-
veloped; lodicules 2 or absent, fleshy, glabrous; sta-
mens 1 to 3; ovary glabrous, apical appendageXIII.
ab- Incertae Sedis
Eriachneae (Ohwi) Eck-Borsb., Blumea 26: 1
sent, haustorial synergids absent, styles 2, free,
close, stigmas 2. Caryopsis with the pericarp often1980.
Micraireae Pilger, Nat. Pfl.-Fam. Ed. 2, 14d: 167.
free or loose; hilum short; endosperm hard, without
lipid, containing simple or compound starch grains;1956.
embryo large or rarely small, epiblast presentStreptogyneae
or C. Calder6n & Soderstr., Smithsoni-
rarely absent, scutellar cleft present, mesocotyl in-an Contr. Bot. 44: 18. 1980.
Cyperochloa Lazarides & L. Watson, Brunonia 9:
ternode elongated, embryonic leaf margins meeting
216. 1987.
or rarely overlapping. Basic chromosome numbers:
x =(7), (8), 9, 10. Gynerium Willd. ex P. Beauv., Ess. Agrostogr. 138,
153, t. 24. 1812.
Foliar anatomy. Mesophyll usually radiate,
Notes. These five taxa are left Incertae Sedis
without an adaxial palisade layer, fusoid cells ab-
because the data presented here do not firmly sup-
sent, arm cells absent; Kranz anatomy present;
port their inclusion in any of the 12 subfamilies.
midrib simple; adaxial bulliform cells present.
This approach has also been taken by the APG
(1998) for taxa of uncertain placement. Some pos-
Foliar micromorphology. Stomata with dome-
sible placements of the five taxa above will require
shaped or triangular subsidiary cells; bicellular mi-
publication of new names, and we feel strongly that
crohairs present, usually chloridoid-type; papillae
nomenclatural changes should not be made until
absent or present.
appreciable data support the conclusion. That said,
recent unpublished data (J. G. Sanchez-Ken, pers.
Photosynthetic pathway. C3 (Eragrostis walteri,
comm.) suggest that Gynerium can be placed as its
Merxmuellera rangei), otherwise C4 (PCK, NAD-
own tribe in Panicoideae, and the tribal name may
ME, but reported as NADP-ME in Pappophorum,
be available by the time this paper is published
by Hattersley & Watson, 1992; the latter may be
(Sanchez-Ken & Clark, 2001). It is likely that Cy-
an error).
perochloa will be placed in Centothecoideae, but
this is based on its morphological similarities to
INCLUDED TRIBES:
Spartochloa and not on any data on Cyperochloa
itself. Streptogyneae will probably fall within Ehr-
Cynodonteae Dumort., Observ. Gramin. Belg.:but
hartoideae, 83.limitations of our data and lack of
1824. TYPE: Cynodon Rich. support in our trees make us cautious about placing
Eragrostideae Stapf, Fl. Cap. 7: 316.it 1898. TYPE:
there unequivocally; there may be an argument
Eragrostis Wolf. for recognition of the tribe as its own subfamily.
Leptureae Dumort., Observ. Gramin. TheBelg.: 83.
name Micrairoideae has been published (Pil-
1824. TYPE: Lepturus R. Br. ger, 1956). Our data are too limited and the place-
Orcuttieae Reeder, Madrofio 18: 20. ment
1965. ofTYPE:
the group too uncertain to add it as a thir-
Orcuttia Vasey. teenth subfamily, although flora writers may choose
Pappophoreae Kunth, Rev. Gramin.to1:do82.
so. Our data on Eriachne are weak, and show
1829.
TYPE: Pappophorum Schreb. only that the genus does not fall within the Pani-

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Volume 88, Number 3 Grass Phylogeny Working Group 425
2001 Phylogeny and Classification of Poaceae

coideae, where it has been placed traditionally. Its a one-way ticket to genomic obesity? P1. Cell 9: 1509-
1514.
placement near the base of the PACCAD Clade is
Bentham, G. 1878. Flora Australiensis 7: 449-670.
based on a single-stranded rbcL sequence from one & J. D. Hooker. 1883. Gramineae. Pp. 1074-
species, and an ITS sequence from a second. The 1215 in Genera Plantarum, vol. 3, pt. 2. L. Reeve, Lon-
two species represent two sections of the genus, one don.
Borre, A. Van den. 1994. Taxonomy of the Chloridoideae
of which has actually been recognized as its own
(Poaceae), with Special Reference to the Genus Era-
genus. We therefore feel that Incertae Sedis best
grostis. Unpublished Ph.D. Dissertation, Australian Na-
reflects what we know of the position of the tribe-tional University, Canberra.
its position is uncertain. & L. Watson. 1994. The infrageneric classification
of Eragrostis (Poaceae). Taxon 43: 383-422.
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Volume 88, Number 3 Grass Phylogeny Working Group 431
2001 Phylogeny and Classification of Poaceae

Appendix I. Taxa included. For each data set, species name, voucher, and reference are listed, as well as GenBank
accession numbers for gene sequences. EAK = Elizabeth Kellogg; HPL = Peter Linder; JID = Jerrold Davis; LGC =
Lynn Clark; NPB = Nigel Barker; PMP = Paul Peterson; RJS = Robert Soreng; SJ = Surrey Jacobs; WZ = Weiping
Zhang; XL = Ximena Londono; BBG = Berlin Botanic Garden; BHC = L. H. Bailey Hortorium Conservatory; FTG
= Fairchild Tropical Garden; NTBG = National Tropical Botanical Garden (Hawaii); PI = USDA Plant Introduction
Station (Pullman, Washington) as source of seed.

Genus Species Voucher Reference GenBank #

ndhF

Flagellaria indica L. LGC & WZ 1305 (ISC) Clark et al. (1995) U22007

Elegia stipularis Mast. Eldenas 2 (BOL) This paper AF251443

Baloskion tetraphyllum (Labill.) B. Kew-6565-1977 (BH) This paper AF251444

G. Briggs & L. A. S.
Johnson
Joinvillea ascendens Gaudich. ex NTBG-800379 (living) Clark et al. (1995) U21973

Brongn. & Gris.

Anomochloa marantoidea Brongn. LGC 1299 (ISC) Clark et al. (1995) U21991

Streptochaeta angustifolia Soderstr. LGC 1304 (ISC) Clark et al. (1995) U21982
Pharus latifolius L. LGC 1302 (ISC) Clark et al. (1995) U21992
Guaduella marantifolia Franch. Kobayashi et al. 1539 Clark et al. (2000) AF164777

(ISC)
Puelia ciliata Franch. Kobayashi et al. 1541 Clark et al. (2000) AF164779

(ISC)
Eremitis sp. nov. LGC & WZ 1343 (ISC) Zhang & Clark (2000) AF182353
Pariana radicifora Sagot ex DollLGC & WZ 1344 (ISC) Zhang & Clark (2000) AF182354
Lithachne hurmilis Soderstr. LGC 1298 (ISC) Clark et al. (1995) U21977

Olyra latifolia L,. XL & LGC 911 (1SC) Clark et al. 1995 U21971

Buergersiochloa bambusoides Pilg. Iransfield 1382 (K) Zhang & Clark (2000) A F182341
Arundinaria gigantea (Walter) Muhl. WZ 8400703 (ISC) Clark et al. (1995) U21846
Chusqlue latifolia 1. (;. Clark LGC & XL 4/7 (ISC) Clark et al. (1995) U21989

Streptogyna americana C. fE. Hubb). lohl & Davidse 12310 Clark el al. (1995) U21965

(ISC)
Ehrharta calycina Sin. NPB s.n. (BOL) Clark et al. (1995) U21995
Oryza sativa L. Sugiura (1989) Clark et al. (1995) X159()1

Leersia virginica Willd. LGC 1316 (ISC) Clark et al. (1995) U21974
Phaenosperma globosum Munro ex LGC 1292 (ISC) Clark et al. (1995) U22005
Benth.

Brachyelytrum erectum (Schreb.) P. LGC 1330 (ISC) Clark et al. (1995) U22004
Beauv.
Lygeum spartum L. RJS 3698 (BH) This paper AF251445
Nardus stricta L. BBG: Royl & Schiers This paper AF251446

s.n. 1988 (B)

Anisopogon avenaceus R. Br. HPL 5590 (BOL) This paper AF251447

Ampelodesmos mauritanica (Poir.) T. BBG: Royl & Schiers This paper AF251448
Durand & Schinz s.n. 1988 (B)
Stipa barbata Desf. PI-229468 (BH) This paper AF251449

Nassella viridula (Trin.) Barkworth PI-387938 (BH) This paper AF251450

LGC ex
Oryzopsis (=Piptath- racemosa (Sm.) Ricker & WZ 1288 (ISC) Clark et al. (1995) U21924

erum) Hitchc.
Brachypodium distachyon (L.)
PI-422452 (BH)P. Beauv.
This paper AF251451
Melica altisssima L. PI-325418 (BH) This paper AF251452

Glyceria striata (Lam.) Hitchc. JID & RJS s.n. (BH) This paper AF251453
Diarrhena obovata (Gleason) Bran- LGC & WZ 1216 (ISC) Clark et al. (1995) U21998

denburg
Avena sativa L. material from R. Wise Clark et al. (1995) U22000

(ISU)
Bromus inermis Leyss. PI-314071 (BH) This paper AF251454

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432 Annals of the
Missouri Botanical Garden

Appendix I. Continued.

Genus Species Voucher Reference GenBank #

Hordeum vulgare L. material from R. Wise Clark et al. (1995) U22003

(ISU)
Aristida purpurea Nutt. var. longi- Gabel 2700 (ISC) Clark et al. (1995) U21966

seta (Steud.) Vasey ex

Rothr.

Stipagrostis zeyheri (Nees) DeWinter NPB 1133 (BOL) This paper AF251455

Amphipogon strictus R. Br. HPL 5634 (BOL) This paper AF251456

Arundo donax L. LGC s.n. (ISC) Clark et al. (1995) U21997
Molinia caerulea (L.) Moench LGC 1165 (ISC) Clark et al. (1995) U21994

Phragmites australis (Cav.) Trin. ex LGC 1294 (ISC) Clark et al. (1995) U21996
Steud.
Merxmuellera macowanii (Stapf) ConertNPB 1008 (BOL) This paper AF251457
Karroochloa purpurea (L.f.) Conert & HPL 5360 (BOL) This paper AF251458

Tuirpe
Danthonia californica Bolander PI-232247 (BH) This paper AF251459

Austrodanthonia laevis (Vickery) HPL

H. 5633
P. (BOL) This paper AF251460
Linder

Merxmuellera rangei (Pilg.) Conert NPB 960 (GRA) This paper AF251461

Centropodia glauca (Nees) Copt NPB 967 (BOL) This paper AF251462

Eragrostis curvula (Schrad.) Nees LGC 1303 (ISC) Clark et al. (1995) U21988
Uniola paniculata L. JID s.n. (BH) This paper AF251463

Zoysia matrella (L.) Merr. LGC 1174 (ISC) Clark et al. (1995) U21975

Distichlis spicata (L.) E. Green Allred s.n. (BH) This paper AF251464

subsp. stricta (Torr.) R.

F. Thorne

Pappophorum bicolor E. Fourn. Pohl 12464 (ISC) This paper AF352581

Spartina pectinata Link LaDuke s.n. (BH) This paper AF251465

Sporobolus indicus (L.) R. Br. LGC 1293 (ISC) Clark et al. (1995) U21983

Micraira lazaridis L. G. Clark, LGC 1157 (ISC) Clark et al. (1995) U21972
Wendel & Craven

Thysanolaena maxima (Roxb.) Kuntze FTG (living) Clark et al. (1995) U21984

Gynerium sagittatum (Aubl.) P. LGC & P Asimbaya This paper AF251466

Beauv. 1472 (ISC)
Chasmanthium laxum (L.) H. O. Yates D. Lewis s.n. (ISC) Clark et al. (1995) U27296
Zeugites pittieri Hack. LGC 1171 (ISC) Clark et al. (1995) U21987

Danthoniopsis petiolata (J. B. Phipps) LGC 1173 (ISC) Clark et al. (1995) U22008

Clayton
Panicum virgatum L. LGC 1164 (ISC) Clark et al. (1995) U21986

Pennisetum alopecuroides (L.) Spreng. RJS s.n. (BH) This paper AF251467
Miscanthus japonicus Andersson Arnold Arboretum 301 Spangler et al. (1999) AF117417

80c (living)
Zea mays L. cv. 'B73' Material from M. Lee Clark et al. (1995) U21985

(ISU)
rbcL

Flagellaria indica Chase 206 (NCU) Chase et al. (1993) L12678

Elegia Duvall
capensis (Burm. f.) Schel- Chase 209 & Morton
(NCU) (1996) L12675
pe
Baloskion tetraphyllum No voucher Katiyama & Ogihara D38296

(1996)
Joinvillea plicata (Hook. f.) Newell Thren 84 (NO) Duvall & Morton (1996) L01471
& B. C. Stone
Anomochloa marantoidea LGC 1299 (ISC) Duvall & Morton (1996) AF021875
Guaduella marantifolia Kobayashi et al. 1539 Clark et al. (2000) AF164778
(ISC)

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Volume 88, Number 3 Grass Phylogeny Working Group 433
2001 Phylogeny and Classification of Poaceae

Appendix I. Continued.

Genus Species Voucher Reference GenBank #

Puelia ciliata Kobayashi et al. 1541 Clark et al. (2000) AF164780

(ISC)
Lithachne humilis LGC s.n. (ISC) Duvall & Morton (1996) U13231
Bambusa multiplex (Lour.) Sanders 62-616 (UCR) Duvall & Morton (1996) M91626
Raeusch. ex Schult. &
Schult. f.
Chusquea circinata Soderstr. & C. Quail Botanic Garden Duvall & Morton (1996) U13227
Calderon (living)
Oryza sativa No voucher Nishizawa & Hirai D00207

(1987)
Leersia oryzoides (L.) Sw. LGC s.n. (ISC) Duvall & Morton (1996) U13228
Stipa dregeana Steud. var. dre- McDowell s.n. (BOL) Barker et al. (1995)
geana
Avena sativa No voucher Duvall et al. (1993) L15300
Bromus inermis Leyss. No voucher Seberg & Linde-Laursen Z49836

(1996)
Hordeum vulgare No voucher Zurawski et al. (1984) X00630
Aristida congesta Roem. & NPB 1130 (BOL) Barker et al. (1995) U31359
Schult.

Stipagrostis zeyheri NPB 1133 (BOL) Barker et al. (1995) U31378

Amphipogon strictus HPL 5634 (BOL) Barker (1997) U88403

Arundo donax NPB 1131 (BOL) Barker et al. (1995) U31360

Moliniopsis japonica (Hack.) Hayata Kobayashi 1253 Barker et al. (1995) U31439

Phragmites australis NPB 1132 (BOL) Barker et al. (1995) U29900

Merxmuellera macowani NPB 1008 (BOL) Barker et al. (1995) U31438
Karroochloa purpurea HPL 5360 (BOL) Barker et al. (1995) U31437
Danthonia spicata (I.) P. Beauv. ex EAK V1 (GH) Barker et al. (1995) U31102
Roem. & Schult.
Centropodia glauca HPL 5410 (BOL) Barker et al. (1995) U31100

Eragrostis capensis (Thunl.) Trin. NPB 1 135 (BOL) Barker et al. (1995) U31104

Enneapogon scaber Lehm. NPB 1023 (BOL) Barker et al. (1995) U31103
Eriachne triodioides Domin EAK s.n. (GH) This paper AF352580
Thysanolaena maxima Kew 1979-3225 Warr Barker et al. (1995) U31380

(living)
Gynerium sagittatum Kew 1991-1276 Kall Barker et al. (1995) U31105
(living)
Chasmanthium latifolium (Michx.) H. O. Snow 5944 Barker et al. (1995) U31101
Yates
Pennisetum glaucum (L.) R. Br. No voucher Doebley et al. (1990) L14623
Sorghum bicolor (L.) Moench No voucher Lou et al. (1989) 1515164A
Zea mays No voucher Gaut et al. (1992) Z11973

rpoC2
Joinvillea plicata No voucher Barker et al. (1999) AF001864
Olyra latifolia HPL 5742 (BOL) Barker et al. (1999) U90825
Bambusa vulgaris Schrad. ex J. C. Durban Botanic Garden Barker et al. (1999) U90824
Wendl. (living)
Ehrharta dura Nees ex Trin. NPB 1118 (BOL) Barker et al. (1999) AF064761
Oryza sativa No voucher Hiratsuka et al. (1989) X15901
Lygeum spartum Kew (living) Cummings et al. (1994) L25381
Nardus stricta Kew (living) Cummings et al. (1994) L25382
Anisopogon avenaceus HPL 5590 (BOL) Barker et al. (1999) U92263

Stipa dregeana McDowell s.n. (BOL) Barker et al. (1999) U90826

Briza maxima L. EAK s.n. (GH) Cummings et al. (1994) L25376
Bromus tectorum L. EAK s.n. (GH) Cummings et al. (1994) L25377

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434 Annals of the
Missouri Botanical Garden

Appendix I. Continued.

Genus Species Voucher Reference GenBank #

Aristida congesta Roem. & NPB 1130 (BOL) Barker et al. (1999) U90827

Schult. subsp. barbi-

collis (Trin. & Rupr.)
DeWinter
Stipagrostis zeyheri subsp. zeyheri NPB 1133 (BOL) Barker et al. (1999) U90828

Amphipogon strictus HPL 5634 (BOL) Barker et al. (1999) U94335

Arundo donax NPB 1131 (BOL) Barker et al. (1999) U92264

Moliniopsis japonica Kobayashi 1253 Barker et al. (1999) U95081

Phragmites australis NPB 1132 (BOL) Barker et al. (1999) U95130

Merxmuellera macowanii NPB 1008 (BOL) Barker et al. (1999) U95076
Karroochloa purpurea HPL 5360 (BOL) Barker et al. (1999) U94824
Danthonia spicata EAK V1O (GH) Barker et al. (1999) U93362
Austrodanthonia laevis HPL 5633 (BOL) Barker et al. (1999) U96313
Merxmuellera rangei NPB 960 (GRA) Barker et al. (1999) U95077
Centropodia glauca HPL 5410 (BOL) Barker et al. (1999) U92265

Eragrostis capensis NPB 1135 (BOL) Barker et al. (1999) U96317

Enneapogon scaber NPB 1023 (BOL) Barker et al. (1999) U96319

Spartina alterniflora EAK s.n. (GH) Cummings et al. (1994) L25386

Micraira lazaridis LGC 1157 (ISC) Barker et al. (1999) U96318
Thysanolaena maxima Kew, 1979-3225 Warr Barker et al. (1999) U96315

(living)
Gynerium sagittatum Kew, 1991-1276 Kall Barker et al. (1999) U94392

(living)
Chasmanthiuml latifolium Snow 5944 Barker et al. (1999) U94334
Panicum maximum Jacq. NPB 1125 (BOL) Barker et al. (1999) AF000021
Pennisetum sp. No voucher Cummings et al. (1994) L25383

Sorghum bicolor No voucher Chen et al. (1993) Z14983

Zea mays No voucher Igloi et al. (1990) X86563

Phytochrome B
Flagellaria indica RJS 77 394 (BH) Mathews & Sharrock U61203
(1996)
Joinvillea ascendens Moore 10438 (NY) Mathews & Sharrock U61205

(1996)
Anomochloa marantoidea LGC 1299 (ISC)Mathews et al. (2000) AF137291
Streptochaeta angustifolia LGC 1304 (ISC)Mathews et al. (2000) AF137328
Pharus lappulaceus Aubl. LGC 1,329 (ISC)Mathews et al. (2000) AF137321
Puelia ciliata Kobayashi et al. Mathews
1541 et al. (2000) AF137324
(ISC)
Eremitis sp. nov. LGC & WZ 1343 (ISC) Mathews et al. (2000) AF137304
Pariana radiciflora LGC & WZ 1344 (ISC) Mathews et al. (2000) AF137317
Lithachne pauciflora (Sw.) P. Beauv. LGC 1297 (ISC) Mathews et al. (2000) AF137307
Olyra latifolia XL & LGC 911 (ISC) Mathews et al. (2000) AF137315
Buergersiochlo( bambusoides Dransfield 1382 (K) Mathews et al. (2000) AF137295
Pseudosasa japonica (Sieb. & Zucc. EAK V6 (A) Mathews et al. (2000) AF137323

ex Steud.) Makino ex
Nakai

Chusquea oxylepis (Hack.) Ekman LGC 1069 (ISC) Mathews et al. (2000) AF137298

Streptogyna americana Johnston 433 Mathews et al. (2000) AF137329

Ehrharta erecta Lam. EAK V44 (GH) Mathews et al. (2000) AF137302
Oryza sativa no voucher Dehesh et al. (1991) X57563
Lygeum spartum RJS 3698 (BH) Mathews et al. (2000) AF137309
Nardus stricta BBG: Royl & Schiers s.n. Mathews et al. (2000) AF137313

Anisopogon avenaceus HPL 5590 (BOL) Mathews et al. (2000) AF137290

Nassella viridula Lavin s.n. (MONT) Mathews et al. (2000) AF137314
Brachypodium PI-440176
pinnatum (L.) P. Beauv. (GH) Mathews et al. (2000) AF137294
Melica cupanii Guss. PI-383702 (BH) Mathews et al. (2000) AF137310

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Volume 88, Number 3 Grass Phylogeny Working Group 435
2001 Phylogeny and Classification of Poaceae

Appendix I. Continued.

Genus Species Voucher Reference GenBank #

Glyceria grandis S. Watson JID & RJS s.n. (BH) Mathews et al. (2000) AF137305
Diarrhena obovata LGC & WZ 1216 (ISC) Mathews et al. (2000) AF137301
Phalaris arundinacea L. RJS 3427 (BH) Mathews et al. (2000) AF137320
Bromus inermis Lavin s.n. (MONT) Mathews et al. (2000) U61193
Triticum aestivum L. Mason-Gamer s.n. (GH) Mathews et al. (2000) AF137331
Aristida purpurea subsp. longisetaLavin s.n. (MONT) Mathews et al. (2000) AF137292
Molinia caerulea RJS 3305 (BH) Mathews et al. (2000) AF137312
Phragmites australis Keller s.n. (GH) Mathews et al. (2000) AF137322
Danthonia spicata EAK V1O (GH) Mathews et al. (2000) AF137299

Eragrostis cilianensis (All.) Vignolo Lavin s.n. (MONT) Mathews et al. (2000) U61200
ex Janch.
Sporobolus giganteus Nash PMP 10008 (US) Mathews et al. (2000) AF137327

Thysanolaena maxima Farnsworth s.n. (GH) Mathews et al. (2000) AF137330

Chasmanthium latifolium EAK V13 (A) Mathews et al. (2000) AF137297

Danthoniopsis dinteri (Pilg.) C. E. PI-207548 (GH) Mathews et al. (2000) AF137300

Hubb.
Panicum capillare L. Lavin s.n. (MONT) Mathews et al. (2000) AF137316
Pennisetum alopecuroides EAK s.n. (A) Mathews et al. (2000) AF137318
Miscanthus japonicus Arnold Arboretum 301- Mathews et al. (2000) AF137311

80C (living)
Zea mays Lavin s.n. (MONT) Mathews et al. (2000) AF137332

Chloroplast restriction
site polymorphisms
Flagellaria indica BHC-77394 Soreng & Davis (1998)
Baloskion tetraphyllum Kew-6565-1977 (BH) Soreng & Davis (1998)
Joinvillea ascendens NTBG-800379 Davis & Soreng (1993)
(H. Moore 10438)
Anomochloa marantoid(ea LGC 1299 (ISC) Soreng & D)avis (1998)
Streptochaeta sodiroanaL Hack. PMP 9525 (US) Soreng & Davis (1998)
Pharus latifolius IHC from USZ I)avis & Soreng (1993)
Eremitis sp. USNHG- 153, Soderstrom Soreng & Davis (1998)
2182 (US) or USNHG-
286 (US)
Lithachne humilis BHC from U. S. National Davis & Soreng (1993)
Zoological Gardens
Olyra latifolia PMP 7311 (US) Soreng & Davis (1998)
Pseudosasa japonica BHC-71467 Davis & Soreng (1993)
Chusquea aff. subulata L. G. Clark PMP 9499 (US) Soreng & Davis (1998)
Ehrharta calycina PI-208983 (BH) Soreng & Davis (1998)
Oryza sativa no voucher Hiratsuka et al. (1989)
Leersia virginica RJS 3399 (BH) Davis & Soreng (1993)
Brachyelytrum erectum RJS 3427 (BH) Davis & Soreng (1993)
Lygeum spartum RJS 3698 (BH) Soreng & Davis (1998)
Nardus stricta BBG: seed from Royl & Davis & Soreng (1993)
Schiers s.n. 1988,
Hempel s.n. 1987 (B)
Anisopogon avenaceus HPL 5590 (BOL) Soreng & Davis (1998)
Ampelodesmos mauritanica BBG: Royl & Schiers s.n. Soreng & Davis (1998)
1988 (B)
Stipa barbata PI-229468 (BH) Davis & Soreng (1993)
Nassella viridula PI-387938 (BH) Soreng & Davis (1998)
Piptatherum miliaceum (L.) Coss. PI-284145 (BH) Davis & Soreng (1993)
Brachypodium pinnatum PI-440170 (BH) Davis & Soreng (1993)
Melica altissima PI-325418 (BH) Davis & Soreng (1993)
Glyceria striata JID & RJS s.n. (BH) Davis & Soreng (1993)
Diarrhena obovata Seed from Tiedye 5186 Davis & Soreng (1993)
(DAO)

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436 Annals of the
Missouri Botanical Garden

Appendix I. Continued.

Genus Species Voucher Reference GenBank #

Avena barbata Pott ex Link No voucher Soreng & Davis (1998)
Bromus inermis RJS 3428 (BH), PI- Davis & Soreng (1993)
314071 (BH)
Triticum aestivum L. cv. 'Susqu- RJS s.n. (BH) Soreng & Davis (1998)
ehanna'
Aristida purpurea Allred s.n. (BH) Soreng & Davis (1998)
Amphipogon strictus HPL 5634 (BOL) Soreng & Davis (1998)
Arundo donax FTG-83-130 (BH) Soreng & Davis (1998)
Molinia caerulea RJS 3305 (BH) Soreng & Davis (1998)
Phragmites australis RJS 3884 (BH) Davis & Soreng (1993)
Danthonia californica PI-232247 (BH) Davis & Soreng (1993)
Eragrostis curvula PI-365034 (BH) Davis & Soreng (1993)
Uniola paniculata JID s.n. (BH) Soreng & Davis (1998)
Zoysia sp. JID s.n. (BH) Soreng & Davis (1998)
Distichlis spicata subsp. stricta Allred s.n. (BH) Soreng & Davis (1998)
Spartina pectinata LaDuke s.n. (BH) Soreng & Davis (1998)
Sporobolus giganteus PMP 10008 (US) Soreng & Davis (1998)
Chasmanthium latifolium Cornell University gar- Davis & Soreng (1993)
dens (living)
Panicum virgatum USDA 421520 (BH) Soreng & Davis (1998)
Pennisetum alopecuroides RJS s.n. (BH) Davis & Soreng (1993)
Miscanthus sinensis Andersson var. RJS s.n. (BH) Davis & Soreng (1993)
gracillimus Hitchc.
ITS

Joinvillea plicata Wilson 7126 Hsiao et al. (1999) AF019784

Streptochaeta sodiroana PMP & Annable 9525 Hsiao et al. (1999) AF019785

(US)
Pharus latifolius PMP & Annable 6944 Hsiao et al. (1999) AF019786

(US)
Lithachne humilis Utah State University Hsiao et al. (1999) AF019787

s.n. (living)
Chusquea latifolia LGC & XL 417 (ISC) Hsiao et al. (1999) AF019788

Microlaena stipoides (Labill.) R. Br. Kew 1973-15875 (living) Hsiao et al. (1999) AF019791

Oryza sativa No voucher Takaiwa et al. (1985)

Leersia hexandra Sw. Jacobs 7782 Hsiao et al. (1999) AF019793

Brachyelytrum erectum Intermountain Herbarium Hsiao et al. (1999) AF019794

1669

Lygeum spartum Catalan 1593 Hsiao et al. (1999) AF019797

Nardus stricta Intermountain Herbarium Hsiao et al. (1999) AF019796
203443

Anisopogon avenaceus Dalby 94/01 Hsiao et al. (1999) AF019800

Ampelodesmos mauritanica Kew 150-90.00982 (liv-

Hsiao et al. (1999) AF019799

ing)
Stipa ichu (Ruiz & Pavon) Renvoize & Flores 5301 Hsiao et al. (1999) AF019803
Kunth (K)
Nassella leucotricha (Trin. & Houck s.n. Hsiao et al. (1999) L36520

Rupr.) R. W. Pohl
Piptatherum songaricum (Trin. & Hsiao 199 Hsiao et al. (1999) AF019802

Rupr.) Roshev. ex Ni-

kitina

Brachypodium mexicanum (Roem. & University of Leicester Hsiao et al. (1999) AF019805

Schult.) Link Botanic Gardens 347

Melica californica Scribn. Curto 719 Hsiao et al. (1999) L36518

Glyceria striata Curto 826 Hsiao et al. (1999) L36516

Diarrhena americana P. Beauv. Intermountain Herbarium Hsiao et al. (1999) AF019798
218465

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Volume 88, Number 3 Grass Phylogeny Working Group 437
2001 Phylogeny and Classification of Poaceae

Appendix I. Continued.

Genus Species Voucher Reference GenBank #

Avena Fritz, CN
longiglumis Durieu Z11758
Hsiao et al. (1999)
Bromus mnermis Hsiao 103 L11579
Hsiao et al., (1994)
Hordeum vulgare Hsiao 200 Chatterton et Z11759
al. (1992)
Aristida purpurea Intermountain Herbarium Hsiao et al., 1999
AF019807
209381

Stipagrostis zeyheri subsp. zeyheri NPB 1133 Hsiao et al. AF019845

(1999)
Amphipogon caricinus F. Muell. Macfarlane 2155 Hsiao et al. AF019849
(1998)
Arundo donax Hsiao 196, Evans s.n. Hsiao et at. AF019809
(1999)
Molintia caerulea Kewl973 10386 Hsiao et al. AF109857
(1999)
Phragmites australis Chatterton s. a. Hsiao et at. AF019810
(1999)
Merxmuellera macowant'i Kew 142-83.01715 Hsiao et al. AF019863
(1998)
Karroochloa purpurea HPL 5360 Hsiao et al. AF019874
(1998)
Danthonia califoricn Curto 974 Hsiao et at. AF019813
(1999)
Rytidosperma pumilum (Kirk) H. P. HPL 5747 Hsiao et at. AF019878
(1998)
Linder
Merxmuellera rangei NPB 960 (GRA) AF019862
Hsiao et al. (1998)
Centropodia glauca NPB 967 AF019861
Hsiao et al. (1998)
Eragrostis dielsii Pulg. cx Diels & Jacobs 7195 AF019834
Hsiao et al. (1999)
Pritz.

Spartina gracilis Trin. Intermountain Herbarium AF019844

Hsiao et al. (1999)
194828

Sporobolus airoides (Torr.) Torr. Curto s. n. Hsiao et al. AF019842

(1999)
Eriachne triseta Nees cx Steud. Jacobs 7184 Hsiao et al. AF019818
(1999)
Micratir(L subulifolia F. Mucll. Clarkson 1 0300 Hsiao et al. AF019859
(1999)
Thysanolaena maxima Kew1979-3225 Hsiao et al. AF019854
(1999)
Gynerium sagtttaturn Kewl991-1276Kall Hsiao et al. A FO 1 9853
(1999)
Chasmanthiutm latij6lium ltiterl)iountain Herbarium
Hsia(a et al. A 0O 1 9815
(1999)
216008
PatnicuLm )isalcatl rntr rThunth. Hsitao 160, 1)-19486
Hsiao et al. AF0l 9829
(1999)
Pennisetum setaceum (Forssk.) Chiov. Cutrto 976
Hsiao et at. A FO 1 9833
(1999)
Miscantl hus smiersuis 1va(ns s.n. Hsiao ct al. A VO 19822
(1999)
Zea Hsiao197
mnays L. sub)sp. mexicaLnaL Hsiao et al. A FO 1981 7
(1999)
(Schrad.) Ittis
GBSSI

Aniomochloai marantoiden LGC 1299 (ISC) Mason-Gamer et al. AF079290

(1998)
laippulaceus LGC 1.329 (ISC) Mason-Gamer et al. AF079298
(1998)
Eremitis sp. nov. LGC & WZ 1343 (ISC) Mason-Gamer et al. AF079295
(1998)
Pariana radicflora LGC & WZ 1344 (ISC) Mason-Gamer et al. AF079297
(1998)
Chusquea exasperata L. G. Clark LGC et al. 1003 (ISC) Mason-Gamer et al. AF079293
(1998)
Oryza sativa No voucher Wang et at. (1994) X65183

Lygeum spartum RJS 3698 Mason-Gamer et al. AF079289

(1998)
Melica cupanii PI-383702 (A) Mason-Gamer et al. AF079296
(1998)
Glycerin grandis JID & RJS s.n. Mason-Gamer et al. AF079291
(1998)
Hordeum vulgare No voucher Rohde et al. (1988) X07932
Merxmuellera macowanal NPB 1008 (BOL) This paper AF353520
Karroochloa purpurea HPL 5360 (BOL) This paper AF353519
Austrodanthonia laevis HPL 5633 (BOL) This paper AF353517

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438 Annals of the
Missouri Botanical Garden

Appendix I. Continued.

Genus Species Voucher Reference GenBank #

Merxmuellera rangei NPB 960 (GRA) This paper AF353521
Centropodia glauca NPB 967 (BOL) This paper AF353518
Danthoniopsis dinteri PI-207548 (A) Mason-Gamer et al. AF079251
(1998)
Pennisetum alopecuroides Park Seed 3650 (A) Mason-Gamer et al. AF079288
(1998)
Sorghum bicolor PI-156549 (A) Mason-Gamer et al. AF079258
(1998)
Zea mays No voucher Klosgen et al. (1986) X03935

Appendix II. Matrix of structural characters, as assembled for

matrix appear in groupings according to what was known about the
prepared. Thus, the four outgroups come first, followed by the early
Abbreviations of taxon names and associated underlines are require
are described in Table 4, and are optimized on the cladogram in Fi
two or more states) and subset ambiguities (when one or more state
be assigned to any of the states not eliminated) are as follows: ?
uncertain homology/unassignable to defined states; A = [01]; C
= [234]; K = [01341; L = [14]; N = [29]; Q = [07]; R = [012]; S =

Character numbers 00000000011111111112222222222333333333344444444445555

Taxon 789016789012346789012345678901 234567890123456789023

Flagellaria \01-01AO- _-- _- o -0\ \1111003130-0----??00?-0050- -\000

Elegia 000--0-0- ----- o-0\ ,1100103310-0----??1-0---?0- -???1

Baloskion 070--0-0- ,1100102D2?-0----011-0---TO- -?0?0
Joinvillea 01000110- - ----0\ \1111OA3130-0----???110\140- -1100
Anomochloa 0001011\- \0---\0\ \10110\111?011100?101101140- -0110
Streptochaeta 01010110-\\\\---\0\\\\111101311?010101?10?100110- -0110
Pharus 0000011111010--A0130??111101311?01110101110-1120- -0110
Guaduella 0100011101100--1013011111100221?01???????110A1?O- -???1
Puelia 0100111101110--1013011111101F21?01???????10-1120- -0??1
Eremitis 0100011101010--001301100010\111?011101?1011011\0- -01?1
Pariana 010001110A010--0\1301111110A211?011101??011011DO- -0??1
Lithachne 01000111A1010--11130110011012F1?0111010?01101110- -0111

Olyra 0100011101010--11130110011012F1?0111010101101110- -01?1

Buergersiochloa 010001110101110101301100A1012?1?01???????11011?0- -0??1

Pseudosasa 110011110100A1010130111111013210011101?301101120- -01?1

Chusquea 100011110111A--1013011001101221?0111010?01101100- -01?1

Streptogyna 010011A101001111013011000101F11?0 11101? 00120-0??

Ehrharta
Oryza 010OOO01A101\lA10\11201111110A221?0110010101101020- -0110
Leersia 0100010101\lA10\0120A1000100231?011001010110A020- -?1?0
Phaenosperma OA00011101010--0013010011002D?01110104 0020- -???1
Brachyelytrum 0000010101011101012011001100221?011A01?4110-0010- -?111

Lygeum 000001010\000--1?0----00110\121?0110000111110000- -0111

Nardus 0100010100011101?0----00110\111?0110000111100030- -01??
Anisopogon 0100010101011311013010001100F21001?????1?10-00-0- -0111

Ampelodesmos 00000101010011A1013010001100221?0110000?110-0020- -?1?1

Stipa 01000101010111A101FO10001100J2100110000Kll0-0ORO- -?1?1

Nassella 01000101010111A1012010001100221?0110000Cl10-00\0- -01?1
Piptatherum 010001010101A101013010000100221?01????01110-0020- -?1?1

Brachypodium_d 0100010101001101?1201?001100221?01AO0000110-0OSO- -01?1

Melica_a 01100101010AO--0012100001100231?011000011AO-0090- -01?1

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Volume 88, Number 3 Grass Phylogeny Working 439
Group
2001 Phylogeny and Classification of Poac

Appendix II. Continued.

Character numbers 00000000011111111112222222222333333333344444444445555

Taxon 123456789012 345678901 23456789013458901234567890123

Glyceria-s 0110010101000--1012A00000100231?011000011AO-0000-01?
Diarrhena 01000101010AO--101201000A100221?011AOA01110-0000-01?
Avena 0100010101001E21012010001100221?011AO\1llAO-0070-01?1
Bromus 011001010100A1R1012010001100221?010000001AO-0070-0171
Triticum 010001010000A101012010001100221?01100\001AO-0070-01?1
Aristida 00OA010101011E011120110011002210010110011A100012-11?1

Stipagrostis OA010101010113011A2011001100221?010110?D111000130???1

Amphipogon 01010101010113A1112000001101221?110110?1?11100-0-?1?1
Arundo 110001010100AEA1012001001100221?110110?1?A100020-?111
Molinia 010101010100A101?12A01001100221?0101100111100090-1111

Phragmites \10101010110A1010120010011012210\101100111101020-1111
M_merxmuellera-m_ 0001010101001E11012011001100221101???????11000?0-???1
Karroochloa 0101010101001E110120010011002211110110???1100060-???1
Danthonia 010101010100131101200100110022110101100D11100040-11?1
Austrodanthonia 01010101010013110120010011002211110110???1100020-???1
R-merxmuellera-r_ 0?01010101001E11012001001100221??????????10-0060-???1

Centropodia 0001010101001111012001001100221011?????L?11000630???1

Eragrostis 0\01010101000--1012001001100221?11111001111A000301111
Uniola 0\01010101100--1012001001101221?110110??11110003\?1?1

Zoysia 000A1OOA0001110000 ----0A1OA221?1111100D111100031?1?1

Distichlis 0000010101000--1012001001100221?1111100H?11100030?1?1

Pappophorum 0?010101010A120101200\001100221?\111100??111000E-???l

Spartina 0101010100010--000----001101221?1111100111A100Q31?1?1
Sporobolus 00OAO10101010--O1A200100AA002D1?1111100E11110093Al1?1
Eriachne OA01A101010AA1A101200100A100221?010111??111000?5-????
Micraira 00OAO1A101AAO--100----000101221?0101???Hl1100000-???l

Thysanolaena 1100111101010--101200000A100221?11?????????11010DO-1111

Gynerium 100AA1\101000--101201\000100221?117??????11010\0-???1
Chasmanthiunml 0100010101100--1012001001001221?1111110311100020-1111

Zeugites 010001110101A1OA01200\001101221?111101?1?11000\0-???1

I)anthoniopsis OAO1A1A1AllllE11112001001100221?01?????4111000NL-1??i
Panicum 0100010101110--01120A100110022101101110E111000\3011?1
Pennisetum 010A01010111A1001A200100110A221?1101110311100091-11?1
Miscanthus 0000010111111110012001001100221?110111?211100051-11?1
Zea 010001011A10O--0?12001001101211?\101110311100001-11?1

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 440 Annals of the
Missouri Botanical Garden

Appendix III. Consensus trees for individual data sets and combinations of data sets. Numbers above branch
indicate percent of 500 bootstrap replicates, except for K (all molecular data), for which 1000 replicates were don
Tree statistics are listed in Table 3. The GPWG classification is overlain on each tree for comparison with Figure
-A. Chloroplast restriction sites; strict consensus of seven trees. -B. ndhF; strict consensus of 16 trees. -C. rb
single most parsimonious tree. -D. rpoC2; strict consensus of 33 trees. -E. Phytochrome B; single most parsimoni
tree. -F. ITS; strict consensus of 24 trees. -G. GBSSI, single most parsimonious tree. -H. Structural data; str
consensus of 38,000 trees. -I. Chloroplast data; strict consensus of two trees. -J. Nuclear data; strict consensu
eight trees. -K. All molecular data; strict consensus of six trees.

Flagellaria
Baloskion
Joinvillea

Anomochloa A m h
91 CI Streptochaet7 Anomochlo
Pharus Phar.
Eremitis
100 67 Lithachne Bambus.
Olyra
98
Brachyelytrum
9 8 "-~~~~9 9 Lygeum
Nardus
Anisopogon
7 0 Ampelodesmos
-8 9 6 _ Stipa
88 51 Nassella Po.
62 Piptatherum
81 - I Brachypodium
68 ~ Avena
59 Bromus
1 3 100 Triticum
Diarrhena
X Melica
Glyceria
Aristida - Aristid.
Amphipogon
Arundo
rMolinia
Molinia Arundin.
Phragmites
Danthonia - Danthoni.
95 80 Eragrostis
9.8 Uniola
84 Zoysia Chlorid.
97 98t Spartina
Sporobolus
Distichlis
58j Chasmanthium Centothec.
74 ,- ' Pennisetum
Miscanthus Panic.
Panicum
Pseudosasa
Chusquea Bambus.
72 I Ehrharta
Oryza Ehrhart.
Leersia

Appendix III-Figure A, cp restriction sites

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Volume 88, Number 3 Grass Phylogeny Working Group 441
2001 Phylogeny and Classification of Poaceae

Flagellaria
1 00 Elegia
Baloskion
Joinvillea
96 Anomochloa Anomochlo
Streptochaeta Anmcl
Pharus Phar.
100 10 1Guaduella ] Pue I.
1 0.10~0~~0n
8 1~1Pariana
00 Eremitis
100 7 i:-- Lithachne
63 - -I Olyra Bambus.
1 00 Buergersiochloa
9 4 Pseudosasa
Chusquea
6 9 Streptogyna - Incertae sedis
98 I Ehrharta
Oryza Ehrhart.
1 00- Leersia
Phaenosperma
1 00 Anisopogon
9 5 6 99 Ampelodesmos
98 Stipa
Piptatherum
Nassella
1 00 Melica
72 Glyceria
9 6~96-
Brachypodium
Avena Po.
o88 67 00 Bromus Triticum
Diarrhena

10 1 00
1d00 Lu ygeum
uI ~~ l-- ^~Nardus
Brachyelytrun-
100 1 Aristida ] Arist id.
I Stipagrostis
I Arundo
Molinia Arundin.
1 00- Phragmites
1 00 Merxmuellera m.
I9 9 1 Karroo
Austrodanthonia
' 00 Danthonia
53 - Danthoniopsis Pan i c.

67 ZeugiThysanolaena
ZeugitesCentothec.
Gynerium - Incertae sedis
69 100 Panicum
74 70 Pennisetum Panic.
00-- Miscanthus
Zea
Chasmanthium - Centothec.
1 00 I Merxmuellera r.
Centropodia
99 Eragrostis
Uniola
0 0 0 1 00 Zoysia Chlorid.
Q_ --l62j-- Spartina
9 7 - Sporobolus
Distichlis
Pappophorum
Micraira Incertae sedis

Appendix III-Figure B, ndhF

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442 Annals of the
Missouri Botanical Garden

- Anomochlo.

] Pueli.

Po.

Arist id.

Chlorid.

Incertae sedis

Arundin.

6 4 Thysanolaena
87 Chasmanthium J Centothec.
Gynerium - Incertae sedis
95 1 Pennisetum
1 00[-- Miscanthus Panic.
Zea

Lithachne

Pseudosasa Bambus.
Chusquea
100 Oryza Ehrhart.
Leersia

Appendix III-Figure C, rbcL

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Volume 88, Number 3 Grass Phylogeny Working Group 443
2001 Phylogeny and Classification of Poaceae

Joinvillea

51 Ehrharta
I EtOryza ] Ehrhart.
61 Oryza
Olyra
Bambus.
Pseudosasa Babus.
56
99 Lygeum

88 ~~~~~88 I Nardus
Anisopogon
63 Stipa Po.
8 2 1 Avena
I Bromus
67 Aristida

Stipagrostis
100 Molinia
Phragmites Arundin.
Arundo

Amphipogon
Merxmuellera m.

70 g97 Karroochloa
99 | I Austrodanthonia Dant honi.
73 -,~~~~~~~~73 Danthonia
51 I Merxmuellera r.

63
I Centropodia
100 0 Eragrostis Chlorid.
99-I ' Pappophorum
~I ~ Spartina
Micraira -Incertae sedis

Thysanolaena Cent ot hec.

Chasmanthium

Gynerium -Incertae sedis

80 I Panicum
93 I Pennisetum an Panic.
98 I Miscanthus
I Zea

Appendix III-Figure D, rpoC2

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444 Annals of the
Missouri Botanical Garden

Flagellaria
Joinvillea
Anomochloa

Streptochaeta Anomochlo.
Pharus Phar.
Puelia - Pueli.
Eremitis
Pariana

Buergersiochloa
Lithachne Bambus.
Olyra
Pseudosasa

Chusquea
Ehrharta

EOryza jEhrhart.
Lygeum
Nardus

Anisopogon
Nassella

Melica Po.
Glyceria
Brachypodium
Diarrhena
Avena
Bromus

Triticum

Streptogyna Incertae sedis

Aristida A Arist id.
Danthonia - Danthoni.
Molinia

Phragmites J Arundin.
Eragrostis Chlorid.
Sporobolus i
Thysanolaena
Chasmanthium - Cent ot hec.
Danthoniopsis
Panicum
Pennisetum Panic.
Miscanthus
Zea

Appendix III-Figure E, phy B

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Volume 88, Number 3 Grass Phylogeny Working Group 445
2001 Phylogeny and Classification of Poaceae

Joinvillea
Streptochaeta - Anomochlo.
Pharus - Phar.
Z5- Lithachne -7 Bambu
Chusquea _
Ehrharta

R6Q9 |- Oryza Ehrhart.

L-- eersia
,83 _-4-Brachyelytrum
83 -- 90 Lygeum
Nardus
Brachypodium
67 Melica
Glyceria
Anisopogon
99 Stipa o
g9~ Q ~8 1- Nassella
Piptatherum
6 4 1 Avena
19 L 90 Bromus
Triticum
Ampelodesmos
Diarrhena

76 isti Aristida.
I__| I--- ~idStipagrostis
62 1 Amphipogon - Arundin.
1-00 Spartina Chlorid.
Sporobolus Chorid.
1 8 _ 93 Karroochloa Danthoni.
*--- Austrodanthonia Dant honi.
Arundo Arundin.

Merxmuellera m. - Dan
Merxmuellera r. - Ch o
Danthonia Dant honi.
Molinia Arundin
Phragmites Arundn.
Centropodia Chlorid.
Eragrostis ~J
79 Pac Panicum
__=__ IPennisetum Pa
Miscanthus
Thysanolaena
Chasmanthium Centothec.
Zea Panic.
Gynerium
Eriachne Incertae sedis
Micraira

Appendix III-Figure F, ITS

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446 Annals of the
Missouri Botanical Garden

Anomochloa - Anomochlo.

Pharus - Phar.

100 | Eremitis
Pariana
Barmbus.

Oryza Ehrhart.

98 j Lygeum
Triticum
Po.
64 77
764 7 Glyceria
Melica

Danthoniopsis
61
Pennisetum
63 Panic.
93 | Miscanthus
Zea
67
100 Karroochloa Danthoni.
Austrodanthonia
96
9 95
5 Merxmuellera
Chlorid. r. Chorid.
1 00 Centropodia
Merxmuellera m. - Danthoni.

Chusquea Bambus.

Appendix III-Figure G, GBSSI

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Volume 88, Number 3 Grass Phylogeny Working Group 447
2001 Phylogeny and Classification of Poaceae

Flagellaria
97 = Elegia
Baloskion
Joinvillea
Streptochaeta _ Anomochlo.
Anomochloa
Pharus - Phar.
Pariana
Eremitis Bambus.
Chusquea
Puelia Pue I
-
-Guaduella Puel_
-Pseudosasa
80
LI -Lithachne Bambus
Olyra
Bam b us.

Buergersiochloa
Zeugites - Centothec.
Streptogyna - Incertae sedis
Oryza
LI
Leersia Ehrhart.
Ehrharta
Phaenosperma
Brachyelytrum
Lygeum
Nardus
Diarrhena
86 Melica
Glyceria s
Ampelodesmos
Stipa Po.
Plitarnerum
_ . . .. e r u

Anisopogon
Nassella
Brachvpodium

Triticumo
Triticum
Q A A Ps:',&#io<a

Stipagrostis Aristid.
Phragmites
Molinia
Amphipogon A nd
Arundo
L Thysanolaena -Cent othec.
Gynerium - Incertae sedis
Eragrostis
7 9 . Zoysia
Spartina
Distichlis Chlorid.
Pappophorum
Sporobolus
Uniola
Merxmuellera r.
Centropodia
Micraira - ncertae sedis
Chasmanthium - Cent ot hec.
Panicum
Pennisetum
Miscanthus Panic.
Zea
Danthoniopsis
Merxmuellera m.
Karroochloa Danthoni.
Damnto/a Dant honi.
Danthonia

Austrodanthonia
Eriachne - Incertae sedis

Appendix III-Figure H, structural

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448 Annals of the
Missouri Botanical Garden

Flagellaria
1 00 Elegia
I Baloskion
Joinvillea
99 ___Anomochloa 7 Anomochlo.
Streptochaeta
Pharus Phar.
100 100 =- Guaduella 7 Pueli
I, Puelia
Eremitis
1 00 Pariana
Lithachne
Olyra Bambus.
Buergersiochloa
9 8 Pseudosasa
Chusquea
Streptogyna - Incertae sedis
Ehrharta
Oryza Ehrhart.
Leersia
Phaenosperma
1 000
1 Anisopogon
0 87 Ampelodesmos
62 97 1 Stipa
1 O0 -78,- Nasse
Piptatherum
100 , Melica
Glyceria
9 3 99 Brachypodium Po.
-n 7 6 Avena
,90 7 Bromus
00 Triticum
Diarrhena
93 100 Lygeum
Nardus
9 9 Brachyelytrum
Aristida Aristid
100 Stipagrostis A id.
5 1 Amphipogon
Arundo Arundin.
P- Molinia
Phragmites
51 6 0 - Danthoniopsis Panic.
s^l5 1 Thysanolaena -
-- -a sa nZeugites Centothec.
9 9 Chasmanthiumj
0 Gynerium Incertae sedis
94 1J00 Panicum
73 Pennisetum
Miscanthus
Panic.
8100- Zea
-_ 98Q I , Merxmuellera m.
5 ~5
0 ~uiAustrodanthonia
~~0 81 - Karroochloa Danthoni.
100 Danthonia
9 9 Merxmuellera r.
! Centropodia
8 6 100 Eragrostis
i78 7L Uniola Chlorid.
Pappophorum C .
- 1 00 Zoysia
100 86 Spartina
98 Sporobolus
Distichlis
Micrairaae seis
Eriachne -lncertae sedis

Appendix III--Figure I, all chloroplast

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Volume 88, Number 3 Grass Phylogeny Working Group 449
2001 Phylogeny and Classification of Poaceae

Flagellaria
Joinvillea
6 4 I Anomochloa Anm hlo.
I Streptochaeta Anomo
Pharus -- Phar.
Puelia - Pueli.
9 9 Eremitis
Pariana
97 9 9 Lithachne
Olyra Bam bus.
Buergersiochloa
63 Pseudosasa
87 - Chusquea
92 Ehrharta
Oryza Ehrhart.
Leersia
Brachyelytrum
Lygeum
- 5 9 Q|- Nardus
97 Anisopogon
Ampelodesmos
Piptatherum
Diarrhena
50 97 Avena Po
9 5 Bromus
Triticum
Brachypodium
9 8 Stipa
Nassella
93 Melica
Glyceria
Streptogyna - Incertae sedis
84- Aristida Arist id.
81 { Stipagrostis Aist
Centropodia - Chlorid.
Arundo -Arundin.
Merxmuellera r.
Merxmuellera m. Danthoni.
Danthonia
Amphipogon - A r u n d in.
Spartina -
Sporobolus Chlorid.
8~7~~~~ '~~~7 ---Eragrostis
9 3 Karroochloa Dant
r[ Austrodanthonia Danthon
62 Molinia J'
r! Phragmites A r
Eriachne
Micraira Incertae sedis
Gynerium--
Chasmanthium Centothec.
57 I Thysanolaena Centhc.
Danthoniopsis
o6 "3 Panicum
76 Pennisetum Panic.
83 Miscanthus
I --- Zea

Appendix III-Figure J, all nuclear

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450 Annals of the
Missouri Botanical Garden

Flagellaria
1 00 Elegia
I Baloskion
Joinvillea

100 --Anomochloa Anomochlo.

i Streptochaeta Anomochlo.
Pharus Phar.
100 100 C f PueiGuad ueli.
- Puelia = '
100 Eremitis
100 6 6 -- z Pariana
100 Lithachne
| 100 Olyra Bambus.
9 8 Buergersiochloa
99 Pseudosasa
5 3 Chusquea
7 0 Streptogyna Incertae sedis
| Ehrharta
1 100 Oryza J Ehrhart.
1 100 Leersia
Phaenosperma
1 0
1 000 1 Anisopogon
Ampelodesmos
90 87 5100 Stipa
Nassella
Piptatherum
100 Melica
Glyceria
91 93 Brachypodium Po.
9f8
98 94=Bromus
--|-- Avena
1 n00 Triticum
Diarrhena
100 100 Lygeum
Nardus
1 00 Brachyelytrum
100 Aristida - Arst id
5 3 Stipagrostis A
,97i 7. Merxmuellera m.
100 - Karroochloa Dant honi.
Austrodanthonia
1 00 Danthonia
79 Amphipogon
78 Arundo Arundin.
Molinia
Phragmites
98 Merxmuellera r.
[ Centropodia
83 78 FH 1Z3 8Uniola
7 00 Eragrostis
9 8 Pappophorum Chlorid.
9-" 99 Zoysia
8 4 - Spartina
-- 9 8 ' Sporobolus
Distichlis
100 Eriachne Incertae sedis
I Thysanolaena
9 0 '-Chasmanthium Centothec.
Zeugites
Danthoniopsis - Panic.
Gynerium
550 100 Panicum
Pennisetum Panic.
_ Z96 Miscanthus
100 Zea
Micraira -- Incertae sedis

Appendix III-Figure K, all molecular

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Volume 88, Number 3 Grass Phylogeny Working Group 451
2001 Phylogeny and Classification of Poaceae

Appendix IV. Notes on morphological characters. developed blade, but these are clearly interpretable as
In this section the structural characters are defined and/ losses.
or discussed, numbered as in Table 4, and their 7 (4 steps, CI = 0.25, RI = 0.80). Pseudopetiole p/a:
distribution on the most parsimonious tree is outlined. The
The pseudopetiole is a constriction at the base of the leaf
behavior of each character on the most parsimonious blade.
tree Both states occur in the grasses and in the out-
groups. Loss of the pseudopetiole is a synapomorphy of
is signified by a series of three numbers (number of steps,
the clade that includes all grasses except Anomochlooi-
CI, and RI); p/a refers to presence/absence of a character.
deae, Pharoideae, and Puelioideae (i.e., the BEP + PAC-
CULM CAD clade). In the present cladogram, the pseudopetiole
is interpreted as secondarily gained in Bambusoideae,
1 (4 steps, CI = 0.25, RI = 0.25). Perennating woody
Thysanolaena + Zeugites, and Phaenosperma.
culms p/a: Highly lignified, perennial culms are absent
among outgroups (except for the score of "uncertain" in
SPIKELET
Flagellaria) and in most grasses. While most, if not all,
grasses produce some lignin in their culms, the distinction
8 (1 step, CI = 1.0, RI = 1.0). Floret p/a: The floret
between "woody" and "herbaceous" is usually easy to
was defined for the morphological matrix as a unit of the
draw, and our scoring was based on this qualitative cri-
grass inflorescence consisting of a subtending bract (
terion. Of the taxa in this analysis, presence is an un-
lemma) enclosing a short axillary axis bearing a flower,
ambiguous and unreversed synapomorphy of Bambuseae,
the first appendage of which is an adaxial, usually two-
and an autapomorphy of Arundo, Thysanolaena, and Gy-
keeled bract (= palea). The floret is present only in grass-
nerium; Phragmites is scored as intermediate.
es, but not in all grasses. Of the taxa included in this
2 (14 steps, CI = 0.07, RI = 0.18). Hollow culms analysis,
p/ the floret is regarded as absent in Streptochaeta
a: This character is variable in the grasses (14 steps), and
andof undetermined status in Anomochloa, based on the
polymorphic in at least five of the sampled genera, and
uncertain homologies of their floral bracts and the lack of
many additional ones. Occurrence of a small pore was
an identifiable palea (Judziewicz & Soderstrom, 1989; So-
scored as intermediate. Solid culms are uncommon and
reng & Davis, 1998). These two genera have flowers sub-
scattered in occurrence in the early-diverging lineages and
tended by well-developed bracts, but not in any configu-
the BEP Clade, but are frequent in the PACCAD Clade,
ration that can be compared directly to the above
where they are often associated with C1 photosynthesis.
definition. Gain of the floret is interpreted as a synapo-
There are no unambiguous synapomorphies in this anal-
morphy of the clade of all grasses except Anomochlooi-
ysis and the character is highly homoplasious globally,
deae. Within the spikelet clade, the palea is absent in a
but, as is well known among grass systematists, for many
number of taxa, including some species of Agrostis, An-
small groups of genera and species one state or the other
(ropogoneae, and, in this analysis, Zoysia. All of these
of this character likely is a synapomorphy. taxa, however, have an identifiable lemma and other con-
geners have paleas. Following a strict definition of the
floret, Zoysia was scored as polymorphic for this character,
If the leaf blade is absent, characters 45 and( 46 although
are the phylogenetic context shows that a coimplete
considered inapplicable, but characters 3, 4, an(lfloret
5 arewas present ancestrally.
scored. 9 (2 steps, Cl = 0.50, RIl = 0.50). Spikelet pairs:
Spikelet pairs are infrequent in the grasses, and their or-
3 (3 steps, CI = 0.33, RI = 0.33). ,eaf sheath margins
igin is a synapomorphy of Andropogoneae in this analysis
free/fused: Fused margins are an unreversed synapomor-
(butand
phy of Meliceae, and autapomorphies of Flagellaria note that Danthoniopsis is regarded as polymorphic),
although spikelet pairs are also found in some Paniceae.
Bromus. Fused sheaths are frequent in Poeae and Aveneae
Theirorpresence may also be an autapomorphy of Pharus,
and may provide a tribal or more local synapomorphy,
but since Anomochlooideae and non-grasses are not
may be plesiomorphic. Sampling outside the grasses
scored
would help establish the point of origin of the free leaf for this character, the placement of this transfor-
sheath. mation is ambiguous (i.e., paired spikelets could be in-
terpreted as plesiomorphic anlong the floret-bearing grass-
4 (5 steps, CI = 0.20, RI = 0.76). Adaxial ligule type:
The membranous ligule is the most common state es). Developmentally, spikelet pairing appears to occur in
in the
the same way wherever it appears in the Panicoideae
sample. Transformation to a fringe of hairs is an unrev-
(LeRoux & Kellogg, unpublished obs.), but developmental
ersed synapomorphy of Anomochlooideae, and a synapo-
studies
morphy of the clade of Eriachne plus its sister group (a have not been done on Pharus, so spikelet pairing
is an inference based on adult morphology alone.
set of four subfamilies, Aristidoideae, Danthonioideae,
Arundinoideae, and Chloridoideae), although the charac- 10 (4 steps, CI = 0.25, RI = 0.0). Pedicel p/a: The
ter reverses multiple times within this group. The pedicel ligule is present in the earliest-diverging grass lineages
as a fringe of hairs also is an autapomorphy of Danthon- that have spikelets. Multiple losses occur, but only the
iopsis. autapomorphic loss in Triticum can be placed unambigu-
5 (4 steps, CI = 0.25, RI = 0.25). Abaxial ligule p/a: ously. Loss of the pedicel may be a synapomorphy of Ly-
Most grasses lack an abaxial ligule. Presence is an un- geum + Nardus, but this is ambiguous because this char-
reversed synapomorphy of Bambuseae, and an autapo- acter is scored as ambiguous for Lygeum.
morphy of Puelia, Streptogyna, and Thysanolaena. Abax- 11 (7 steps, CI = 0.14, RI = 0.45). Proximal female-
ial ligules occur sporadically in the PACCAD Clade, and sterile florets: Presence of proximal female-sterile florets
are known in a few Pooideae. is interpreted as an unreversed synapomorphy of Puelioi-
deae and of Panicoideae (including Danthoniopsis, ex-
6 (1 step, CI = 1.0, RI = 1.0). Leaf blade p/a: All
sampled species have a leaf blade, except in Restiona-
cluding Gynerium), and is a potential synapomorphy for
Ehrhartoideae except that this is coded as ambiguous for
ceae, where loss of the blade is a synapomorphy. A few
Leersia
species in some grass genera, such as Ehrharta, lack a and Oryza. Multiple origins occur elsewhere as

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452 Annals of the
Missouri Botanical Garden

Verboom, 1996; Linder & Davidse, 1997) and of Merx-

autapomorphies, e.g., in the traditional Aveneae (includ-
ing Phalarideae), Phragmites, Chasmanthium, Uniola,muellera
and rangei + Centropodia. This state also occurs in
Chusquea, and there are no unambiguous losses once Streptogyna,
such Anisopogon, Bromus, and some Panicoideae.
florets are gained. As noted in the discussion on spikelets,
Awn attachment on the back of the lemma is widespread
some proximal female-sterile florets may be homologous in Aveneae; here it is an autapomorphy of Avena, the only
to glumes, as in Ehrhartoideae or some Bambuseae, taxon from the tribe in this analysis. Among unsampled
whereas others, as in Panicoideae, are clearly derived grasses, dorsal attachment is known from one genus of
from reduction of fertile florets. Meliceae and a few genera of the PACCAD Clade includ-
12 (13 steps, CI = 0.07, RI = 0.47). Number of female-
ing Arthraxon.
16 (6 steps, CI = 0.16, RI = 0.44). Disarticulation
fertile florets per female-fertile spikelet: The plesiomorph-
ic state among the grasses is one. Increase in the number
above glumes: Glumes are considered to be the two empty
of female-fertile florets has occurred multiple times, bracts
but subtending the spikelet, and glumes across the
the placement of these changes is ambiguous, in partspikelet
be- clade were assumed to be homologous even
cause five genera are scored as polymorphic. The though only there is disagreement on this point (see Discus-
unambiguous synapomorphic reduction from multiple sion).
fe- This character is not scored in Anomochlooideae or
in the non-grass outgroups, which lack spikelets and
male-fertile florets to one is for the the clade of Zoysia,
Spartina, and Sporobolus, although this may not hold up
therefore glumes, but the presence of this type of disar-
ticulation in at least some members of the Pharoideae
when sampling density is increased. Among unsampled
taxa, there are numerous additional transformations to(e.g.,
one Leptaspis and Pharus; Soderstrom et al., 1987), and
floret. in both genera of the Puelioideae, argue that this type of
13 (12 steps, CI = 0.08, RI = 0.52). Awn or mucro p/ disarticulation is plesiomorphic in the Spikelet Clade.
a: There are multiple origins of awns and mucros on the Synapomorphic loss of disarticulation above the glumes
lemma, mostly of ambiguous placement. Approximately occurs in Pariana + Eremitis and in the clade within
half the genera of the family have awns, so this is another Panicoideae that consists of Paniceae + Andropogoneae.
example of a locally useful but globally highly homopla- Additional losses, all autapomorphic or potentially so, oc-
sious character. In Streptochaeta, eleven of the twelve cur in Zoysia, Spartina, Phaenosperma, and Melica.
bracts lack awns, whereas one (bract VI) has an awn (Jud- 17 (6 steps, CI = 0.16, RI = 0.37). Germination flap:
ziewicz & Soderstrom, 1989). These bracts have been var- The germination flap, a small flap of tissue at the base of
iously interpreted (Soderstrom, 1981), but the ones most the lemma through which the germinating embryo grows,
closely associated with the flower lack awns, so interpre- is derived independently within the PACCAD and BEP
tation of the single awned bract as a lemma is doubtful, Clades. There are unambiguous independent synapo-
and Streptochaeta consequently is scored as ambiguous for morphic gains of the germination flap in Aristidoideae and
this character. Olyreae; germination flaps also are present in some Pan-
14 (4 steps, CI = 0.50, RI = 0.50). Number of awns icoideae (but placement of the transformation is ambigu-
present: This character is scored for taxa that are poly- ous although no Andropogoneae have germination flaps),
morphic for character 13, but it is inapplicable when char- and the character is also autapomorphic in Oryza and in
acter 13 is scored as state 0 or of questionable homology. Amphipogon.
Danthonia and Austrodanthonia are scored as state 3 to
reflect the basic pattern in these taxa, in which theFLOWER
lem-
mas have nine veins, with the central vein forming a me-
dian, usually articulated or cork-screwed, awn, and the
Characters 19-22 are scored as inapplicable for taxa
third vein out from the median on each side forms a hair- that lack lodicules.
like awn or seta at the apex of its respective lateral lemma 18 (4 steps, CI = 0.25, RI = 0.70). Lodicule p/a: Lod-
lobe. This seta varies from an acute lobe to a long hair- icules, as organs that become turgid at anthesis and force
like extension. Occasionally the lateral lobes are fusedopen the flower, occur in most grasses and are not present
with each other, and presumably with the base of the cen- outside the grasses. The evidence that lodicules are mod-
tral awn. From the basic pattern all kinds of deviations ified tepals is not universally accepted. Anomochloa,
occur, including fusion of the lateral lobes, loss of theStreptochaeta, and non-grasses were scored "uncertain ho-
setae, loss of the median awn, and fusion of the lateral mology" by Soreng and Davis (1998), but these two genera
lobes with the median awn still present as a stout mucro.are scored as lacking lodicules in the present analysis. In
In this analysis, presence of three awns is an unreversedthe Pharoideae, lodicules are present or absent in the male
synapomorphy of the clade of Aristidoideae + Danthon- spikelets and lacking in female spikelets (Clark & Jud-
ioideae, but this state also occurs in Amphipogon and An- ziewicz, 1996). Pharus is scored here as having lodicules.
isopogon and in other genera not sampled here such asThus, the first unambiguous occurrence of lodicules is in
Plectrachne, Triodia, and Pentaschistis, among others. the clade that consists of all grasses except Anomoch-
Presence of numerous awns is an autapomorphy of Pap- looideae. There is an unambiguous synapomorphic loss in
pophorum. Lygeum + Nardus and another in Zoysia + Spartina +
15 (7 steps, CI = 0.28, RI = 0.44). Awn attachment: Sporobolus, plus an autapomorphic loss in Micraira.
This character is scored for taxa that are polymorphic for Among unsampled grasses, 84 taxa lack lodicules; among
character 13, but it is inapplicable when character 13 is these, 60 belong to the PACCAD Clade, and 13 to the
scored as 0 or of questionable homology. Awn attachment Pooideae (Watson & Dallwitz, 1992). Lodicules (whatever
at the apex of the lemma is the most common and wide- their origin) might be plesiomorphic for the family, and
spread state of this character. Attachment in a sinus is an then lost in the Anomochlooideae.
unreversed synapomorphy of Danthonioideae (although it 19 (5 steps, CI = 0.20, RI = 0.71). Number of lodi-
appears to be attached at the apex of the lemma in some cules: Three lodicules are present at the point of first un-
instances because of fusion of the lateral lobes with the ambiguous occurrence of lodicules (see char. 18), and this
base of the awn or loss of the lateral lobes; Linder plesiomorphy
& is retained in Pharoideae and Puelioideae.

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Volume 88, Number 3 Grass Phylogeny Working Group 453
2001 Phylogeny and Classification of Poaceae

Bambusoideae and Streptogyna also have three lodicules,of the inner whorl: The posterior stamen of the inner whorl
while Ehrhartoideae have two. Transformation to two lod-
is present in all outgroups and among the earliest-diverg-
icules may be a synapomorphy of Ehrhartoideae, but can-ing lineages in the grasses, so its presence is a plesiom-
not be inferred unambiguously because the earliest-di-orphy for the grasses. Loss of this stamen is a synapo-
verging lineages of Pooideae also have two lodicules, asmorphy of the BEP + PACCAD clade, but it is regained
do all taxa of the PACCAD Clade that have been scored. at least three (possibly four) times in Ehrharta, Oryza (but
Thus two lodicules may be a synapomorphy of the not BEPLeersia), Pseudosasa, and Pariana. The absence of this
+ PACCAD group, with a reversal to three lodicules in
stamen in Leersia, coupled with its presence in Oryza and
the Bambusoideae/Ehrhartoideae group, and re-reversal Ehrharta,
to is equally consistent with independent gains in
the latter two, or a gain in the ancestor of Ehrhartoideae
two lodicules in the Ehrhartoideae. Alternatively, two lod-
followed by a secondary loss in Leersia. This stamen is
icules might have been retained in Ehrhartoideae (follow-
not
ing the transformation from three to two in the origin ofgained elsewhere in the family.
the BEP + PACCAD group) while Streptogyna and Bam- 24 (6 steps, CI = 0.16, RI = 0.54). Anterior stamen
busoideae independently experienced reversals to three; pair of the inner whorl: Except for the loss of this pair in
still other transformation sequences also are possible. Anomochloa, while the posterior stamen is retained, the
Within Pooideae, an unambiguous transformation from distributions
two of states of these two characters (23 and 24)
lodicules to three is a synapomorphy of the clade that are identical. Thus, as with the posterior stamen of the
includes Anisopogon, Phaenosperma, Ampelodesmos, inner and whorl, this stamen pair is unambiguously interpreted
as plesiomorphically present at the point of origin of the
Stipeae, but within this group there is yet another unam-
biguous transformation back to two lodicules in Nassellagrasses, lost as a synapomorphy of the BEP + PACCAD
(while Stipa is polymorphic). clade, and regained three or four times in the Bambuso-
ideae/Ehrhartoideae, possibly with a secondary loss in
20 (uninformative). Fusion of anterior pair of lodicules:
Lodicules are unfused at the first point at which theyLeersia.
are
unambiguously present (see char. 18), and in almost all 25 (8 steps, CI = 0.12, RI = 0.12). Anterior stamen
of outer whorl: This stamen, though absent in Restiona-
grasses. The anterior two are fused in Melica, but the char-
acter is polymorphic in Glyceria, so the transformation ceae, is present in Flagellaria, Joinvillea, and all early-
may be a synapomorphy of this pair of genera, but diverging
the grass lineages, and thus is plesiomorphically
precise placement is ambiguous. Elsewhere, Molinia present
also within the grasses, and lost independently in Res-
is polymorphic. tionaceae and various grass lineages. There are seven au-
21 (5 steps, CI = 0.20, RI = 0.82). Distally membra- tapomorphic losses within the grasses (in Streptogyna,
nous portion of lodicule: The earliest lodicules apparently
Leersia, Eremitis, Glyceria, Piptatherum, Micraira, and Gy-
had a distally membranous portion (see char. 18), and nerium),
this plus polymorphisms in Biuergersiochloa, Diar-
state is retained in early-diverging lineages. Within rhena,
the Eriachne, Zoysia, Sporobolus, and Thysanolaena.
13EP Clade, loss of this membranous portion is an unrev-The loss in Restionaceae is the only unambiguous syna-
ersed synapomorphy of Meliceae. Most elements ofpornorphicthe loss in the taxon sample.
PACCAD Clade lack a distally membranous portion of the 26 (2 steps, CI = 0.50, RI = (.50). Posterior stamien
pair of outer whorl: This stamen pair, like the anterior
lodicule, including various early-diverging lineages, but
Micraira, because it lacks lodicules, is not scored for this
stamen of the outer whorl, is present in all early-diverging
character. Thus, transformation to this state may be a grass
syn- lineages arnd in all outgroups except Restionaceae.
apomorphy of the entire PACCAD Clade, or of the subset Thus, like the anterior stanmen and like all three stamens
that includes all members except Micraira. Withinof thethe inner whorl, this pair is plesiomorphically present
PACCAD Clade, a distally membranous lodicule in Aris- in the study sample as well as in grasses, and as with the
tidoideae, Gynerium, and Merxmuellera macowanii anterior im- stamen of the outer whorl, all absences are inter-
plies at least three additional steps in this character,preted
in- as losses. Except for a few unscored taxa within
cluding either three independent transformations to the thisgrasses, plus an autapomorphic loss in Chasmanthium
lodicule type, or two independent gains including one andina polymorphism in Sporobolus, presence of this pair
the common ancestry of Aristidoideae and Danthonioi- of stamens is constant within the grasses.
deae, followed by a loss in the ancestor of Danthonia, 27 (1 step, CI = 1.0, RI = 1.0). Anthers tetrasporan-
Karroochloa, and Austrodanthonia. Polymorphism in Pan- giate, dithecal, vs. bisporangiate, monothecal: The pres-
icum and Leersia implies two additional transformations,ence of tetrasporangiate, dithecal anthers is interpreted as
a gain of the membranous portion of the lodicule within a plesiomorphy of the entire taxon sample, and of the
the former, and a loss within the latter. grasses. The only transformation to bisporangiate, monoth-
22 (3 steps, CI = 0.33, RI = 0.83). Lodicule vascu-
ecal anthers is an unambiguous synapomorphy of Restion-
larization: Lodicules were originally vascularized aceae.
(see
char. 18). In the BEP Clade, a single unreversed loss of28 (12 steps, CI = 0.08, RI = 0.31). F
vascularization is inferred within Pooideae, after diver-
The presence of one style (see char. 29) c
gence of Brachyelytrum from the rest of the subfamily,as
but either a fusion or reduction in numb
absence of lodicules in the Lygeum + Nardus group
with state 1 of character 29 are scored
means that this transformation could have occurred before character 28. Unfused styles in Flagella
or after divergence of this group from the rest of the Pooi- resentatives of Restionaceae, and fused
deae. In the PACCAD Clade, an independent transfor- chaeta, Pharus, and Puelia together sugg
mation to faint vascularization is an autapomorphy of Am- mation to the fused state occurred near
phipogon. The state also occurs in Thysanolaena, but the grasses, but polymorphism in Joinvillea
association of the latter with Zeugites, which is not scored state in Anomochloa prevent unambigu
for this character, prevents an unambiguous placement of this transformation. Reversal to unfuse
that transformation. preted as an autapomorphy in Guadue
23 (5 steps, CI = 0.20, RI = 0.66). Posterior stamen ersed synapomorphies (i.e., lacking secon

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454 Annals of the
Missouri Botanical Garden

fused styles) of Pooideae and Ehrhartoideae (except for are observed to be present only in the four sam-
synergids
polymorphism in Oryza). Within the PACCAD Clade, pled taxa of the Danthonioideae, and absent in all other
fused styles appear to be plesiomorphic, with one or taxa
morethat have been examined (Verboom et al., 1994).
transformations to the nonfused state, and multiple Thus, rever-presence of haustorial synergids is an unambiguous
sals to the fused state (e.g., in Phragmites, Uniola, andand
unreversed synapomorphy of Danthonioideae, but
Spartina). continued investigation is warranted.
29 (6 steps, CI = 0.33, RI = 0.50). Number of stigmas:
The plesiomorphic state for the grasses, as well as for the FRUIT AND EMBRYO
entire taxon set, is three, with autapomorphic transfor-
mations to two in Baloskion and, among earliest-diverging Characters 35-38 describe features of the typical grass-
grass lineages, to one in Anomochloa. Transformation to type embryo. They are inapplicable for non-grass genera,
two stigmas is a synapomorphy of the clade that includes which lack the grass-type embryo (i.e., state 0 of char.
all grasses except Anomochlooideae and Pharoideae (i.e., 34). Data sources include those listed by Soreng and Da-
the Bistigmatic Clade), and there are additional transfor- vis (1998) plus Klak (unpublished). These characters can
mations to one in Eremitis and in Lygeum + Nardus, and be difficult to score, and the literature contains conflicting
to three in Pseudosasa. Another transformation to one ap- reports for some taxa.
pears to occur in Eremitis, but this is the result of a mis- 33 (5 steps, CI = 0.20, RI = 0.76). Hilum shape: This
coding, as there are actually two stigmas in Eremitis (V. character is recognized as a feature of the caryopsis, and
Hollowell, pers. comm.). Puelia is actually polymorphic thus is inapplicable for non-grasses. Among grasses, taxa
for this character, having two or three stigmas (the species with a short hilum less than one-third the length of the
in this analysis has two). Other polymorphisms (see data grain are scored as ambiguous. All groups except the
table) signify additional transformations. All members of PACCAD Clade have a long hilum that is greater than
the PACCAD Clade have two stigmas. one-third the length of the grain in our sample. This may
30 (8 steps, CI = 0.25, RI = 0.50). Highest order of thus be a synapomorphy of grasses (i.e., the plesiomorphic
stigmatic branching: Only one order of stigmatic branch- state for the caryopsis), but because the character is treat-
ing occurs in Flagellaria, Joinvillea, Anomochlooideae, ed as inapplicable outside the grasses there is no observed
and Pharoideae, and this state therefore appears to be transformation at the origin of the family. Nonlinear hila
plesiomorphic for the grasses and for the entire taxon sam- are reported from the Olyreae and the Poeae/Aveneae in
ple, with the various states in Restionaceae interpretable the BEP Clade. There are five character transformations
as apomorphic within that family. Transformation to two within the PACCAD Clade, but lthe placements of two of
orders of branching appears to be a synapomorphy for the these are ambiguous. All Centothecoideae and most Pan-
clade that includes all grasses except Anomochlooideae icoideae have a nonlinear hilum that is less than 1/3 the
and Pharoideae (the Bistigmatic Clade), and this state, length of the grain, but the hilum is long-linear and great-
once established, is constant in Puelioideae and nearly so er than 1/3 the length of the grain in Danthoniopsis, and
in the PACCAD Clade (exceptions being the presence of this is interpreted as one origin of this state in the common
state one in Zea, and polymorphism in Sporobolus). Within ancestor of the clade, followed by a reversal in Danthon-
the Bambusoideae/Ehrhartoideae, transformation to state iopsis. Elsewhere in the PACCAI) Clade, the only unam-
one is an autapomorphy of Streptogyna and a synapomor- biguous transformation of this character is as a synapo-
phy of Pariana + Eremitis, while a transformation to state morphy of Karroochloa + Austrodanthonia, a subset of
3 is an autapomorphy of Leersia, and polymorphisms occur Danthonioideae. This state also occurs in all taxa of Arun-
in unsampled Olyreae. Within the Pooideae, there is an dinoideae and Chloridoideae for which there are obser-
autapomorphic transformation to state one in Nardus, a vations, except in Molinia. Thus, it is interpretable either
synapomorphic transformation to state three in Meliceae, as having arisen twice (once in Amphipogon + Arundo,
and polymorphism in Phaenosperma. and once in Chloridoideae), or as a synapomorphy of
31 (3 steps, CI = 0.66, RI = 0.0). Number of locules: Arundinoideae + Chloridoideae, with reversion to a long-
All grasses have one locule with one ovule, while three linear hilum in Molinia or in Molinia + Phragmites (not
locules, each with one ovule, are found in Flagellaria and scored for Phragmites).
Joinvillea, although there is a strong tendency to abort one 34 (1 step, CI = 1.0, RI = 1.0). Grass-type embryo p/
or two of the ovules in both of these genera. A transfor- a: The grass-type embryo is lateral, peripheral to the en-
mation from three locules to one may be a synapomorphy dosperm, and differentiated in fruit (Reeder, 1957; Cron-
of the grasses. This transition has also occurred in Res- quist, 1981; Sendulsky et al., 1987). This embryo type is
tionaceae, where the basal condition is three locules with absent outside the grass family and present in all grasses
numerous reductions to a single functioning locule, as in for which observations are available (unobserved in Merx-
Elegia in our sample (Linder, 1992a, b). Although not muellera rangei), and thus interpreted as an unambiguous
sampled in this study, Anarthriaceae have three locules and unreversed synapomorphy of the grasses.
each with one ovule, but the fruit is 1-seeded, and Ec- 35 (7 steps, CI = 0.14, RI = 0.66). Epiblast p/a: Be-
deiocoleaceae have two locules, each with one ovule, and cause this character is inapplicable for non-grasses, its
the fruit is 1-2-seeded. Thus, reduction in both number origin is not unambiguously fixed, but available data for
of locules and number of ovules that develop in the fruit the earliest-diverging lineages within the grasses (except
are common in the Poales; Centrolepidaceae, however, Streptochaeta) indicate presence of an epiblast, and thus
have uniloculate, uniovulate ovaries that are apparently presence is interpretable as a plesiomorphy within the
monocarpellary (Dahlgren et al., 1985). family. Loss of the epiblast is an unambiguous synapo-
morphy of the PACCAD Clade, but there are also three
EMBRYOGENY autapomorphic losses outside of the PACCAD Clade in
Streptochaeta, Ehrharta, and Bromus, plus a polymor-
32 (1 step, CI = 1.0, RI = 1.0). Haustorial synergids phism in Brachypodium. Within the PACCAD Clade the
p/a: Data are unavailable for many taxa, but haustorial epiblast is secondarily gained in the Centothecoideae (but

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Volume 88, Number 3 Grass Phylogeny Working Group 455
2001 Phylogeny and Classification of Poaceae

there is no observation for Thysanolaena) and is a syna- group of Eriachne, the clade that includes Aristidoideae,
pomorphy for either the Chloridoideae or a subset of that Danthonioideae, Arundinoideae, and Chloridoideae.
clade. The precise point of origin within the Chloridoideae 39 (uninformative). Endosperm lipid p/a: Observations
is ambiguous because there is no observation for Merx- are unavailable for several taxa. Of those taxa that are
muellera rangei or Centropodia. Within the Chloridoideae scored, including Baloskion, only Avena has lipid in the
the epiblast is lost in Uniola. This character is highly endosperm. Thus, absence of lipid in the endosperm is
homoplasious within the family. plesiomorphic for the grass family and for the taxon set
36 (3 steps, CI = 0.33, RI = 0.81). Embryo scutellar as a whole, with the presence of lipid in Avena an auta-
tail p/a: The scutellar tail is present in Anomochlooideae pomorphy. Among unsampled grasses, all reports of en-
and Pharoideae, throughout the PACCAD Clade (wherever dosperm lipid are from the Poeae-Aveneae. Liquid and
observations are available) and in most taxa of the Bam- semi-liquid endosperm are indicative of the presence of
busoid/Ehrhartoid clade, absent in most Pooideae, and un- lipid, but "semi-solid" and solid states do not imply ab-
observed in Puelioideae. Despite the variation just de- sence of lipid (Terrell, 1971; Rosengurtt et al., 1972).
scribed, plus the inapplicability of this character outside 40 (12 steps, CI = 0.33, RI = 0.20). Starch grain syn-
the grasses and the absence of data for some critical taxa, dromes: Scoring here follows Tateoka's (1962) classifica-
the balance of evidence suggests that the scutellar tail is tion with one exception. Tateoka scored Brachyelytrum as
a plesiomorphy of the grasses. Within the Bambusoid/Ehr- having simple Panicum-type grains, but emphasized a ma-
hartoid clade, loss of the scutellar tail is unambiguously jor size difference, and we recognize Brachyelytrum-type
interpreted as an unreversed synapomorphy of Oryzeae. A as a separate state (see also Campbell et al., 1986). Wat-
more complex pattern is present in Pooideae, where the son and Dallwitz (1992) distinguished between starch
scutellar tail is usually absent, but is present in Phaenos- grains "simple only" (coded here as [034]) or "compound"
perma, and there are polymorphisms or conflicting reports (coded here as [12]). Polymorphisms, ambiguity of state
for Brachyelytrum, Diarrhena, and Avena. These polymor- delimitation, and lack of observations together preclude
phisms in the matrix prevent unambiguous optimization of unambiguous optimizations of many character-state trans-
the character in Pooideae. Loss of the scutellar tail may formations in this multistate character, but some patterns
be a synapomorphy of Pooideae or of all Pooideae except are evident. First, the Festuca-type grain (state 1) is pre-
Brachyelytrum; presence of the scutellar tail in Phaenos- sent in Baloskion (the only non-grass that is scored) and
perma may be either a unique reversal or a synapomorphy is widespread in early-diverging grass lineages, among
which other types are not observed. This pattern suggests
for Phaenosperma and Anisopogon (which is not scored).
that this starch grain syndrome is plesiomorphic for the
37 (2 steps, CI = 0.50, RI = 0.95). Embryo mesocotyl
grass family and for the taxon set as a whole. The Triti-
internode, negligible vs. elongated: The embryo mesocotyl
cum-type syndromne (state 0) occurs in most "core" Pooi-
internode is negligible in length in all early-diverging
d(eae (represented here by Brachypodiunm, Arena, Bromus,
grass lineages for which scores are available (e.g., An-
and TriticuLm) that are collectively the sister group of Diar-
ornochlooideae, Pharoideae), so although this character is
rhena, and state ( may lbe either a synapomorphy of this
inapplicable for the non-grass outgroups the internode is
group (reversed, however, in Arena) or a parallelism that
likely to have been negligible at the origin of the grass-
arises separately in Brachypodium and in the ancestor of
type embr-yo. All taxa that have been scored in the PAC-
Bromus + Triticum. The Panicum-type syndrome (state 3)
CAD Clade have an elongated internode. 'Transformation
may be a synapomlorphy of Bambuseae, of Stipa + Nas-
from a negligible to an elongated interrno(e is either a sella, and of all Panicoideae except Danthoniopsis, or of
synapomorphy of the entire PACCAD Clade or of the en- the entire PACCAD Clade. If the latter is true, then there
tire clade except Micraira, for which no observation is
is a reversal to the Festuca-type in the clade of Eriachle
available.
plus the set of four subfamilies that is its sister; the Fes-
38 (4 steps, CI = 0.25, RI = 0.85). Embryonic leaf tuca-type is also a potential synapomorphy of Thysanolae-
margins meeting vs. overlapping. The margins of the em-
na + Zeugites, or an autapomorphy of Zeugites. The Bra-
bryonic leaf meet in Anomochloa but overlap in Strepto-
chyelytrum-type syndrome occurs in Phaenosperma and
chaeta, Pharus (unobserved in Puelioideae), and early-Brachyelytrum. Available information suggests that Stipa
diverging lineages of both the BEP and PACCAD Clades. may also have this state (see Soreng & Davis, 1998).
Thus, although the character is inapplicable in the non-
SEEDI ING
grass outgroups, overlapping leaf margins are plesiom-
orphic at the origin of the grass-type embryo, with an au-41 (4 steps, CI = 0.25, RI = 0.70). Lamina of first
tapomorphic transformation to margins meetingseedling in leaf p/a: The lamina of the first seedling leaf is
Anomochloa, and with parallel synapomorphic transfor- absent in Flagellaria and Anomochlooideae, and present
mations in both major lineages. Margins are overlappingin Restionaceae and Pharoideae, while the character is
in all observed taxa in the bambusoid/ehrhartoid alliance,
unobserved in other non-grass taxa and other early-di-
as well as in Brachyelytrum and Phaenosperma of the verging lineages within the grasses. Consequently, opti-
Pooideae (also, Diarrhena is polymorphic). Given this dis-
mization of this character is ambiguous in this region of
tribution, transformation to the margins meeting is inter-
the tree. However, presence of the lamina is unambigu-
preted as a synapomorphy of all Pooideae except Bra- ously established by the point of divergence of Pharoideae
chyelytrum, with a reversal either in Phaenosperma orfrom
in the lineage that includes most other grasses; it is
the ancestor of Phaenosperma and Anisopogon (there ispresent
no in the PACCAD Clade and in Pooideae, but is lost
observation for the latter). All observations for Panicoi-
twice within the BEP Clade, as a synapomorphy of Ory-
zeae and as a synapomorphy of Bambusoideae.
deae and Centothecoideae, plus Eriachne, are of leaf mar-
gins overlapping, while all observations for the other four
VEGETATIVE ANATOMY
subfamilies of the PACCAD Clade are of leaf margins
meeting. Thus, transformation to the latter state is an un-42 (uninformative). Differentiation of leaf epidermal
ambiguous and unreversed synapomorphy of the sister cells into long and short cells: Differentiation is absent in

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456 Annals of the
Missouri Botanical Garden

Flagellaria, inapplicable in Restionaceae (blades absent),

phism in Eragrostis (Van den Borre, 1994; Van den Borre
and present in Joinvillea and all grasses (except for a& few
Watson, 1994).
that are polymorphic). This differentiation is therefore 45
es- (8 steps, CI = 0.12, RI = 0.46). Arm cells p/a: Arm
tablished by the time of divergence of Joinvillea fromcells
theare invaginated chlorenchyma cells that, when pre-
grasses, but the point of origin is ambiguous. sent, reach their maximum development in the layer of
43 (6 steps, CI = 0.16, RI = 0.72). Multicellularchlorenchyma
mi- beneath the upper surface of the leaf. Var-
crohairs p/a: Presence of multicellular microhairs oniation
the in arm cells in the Poaceae is known but has not
abaxial surface of the leaf blades in Joinvillea, Anomoch-
been investigated, and only presence/absence was scored
looideae, and Guaduella, and their absence in Restiona-
for this analysis. Presence in Anomochloa, Pharoideae,
ceae, Pharoideae, and Puelia, make it difficult to place
and Puelioideae (including a polymorphism in Guaduella),
the origin (or origins) of multicellular microhairs, butand absence in Streptochaeta, combined with absence out-
they
appear to have been present in the common ancestor side
of the Poaceae, together suggest a first occurrence of
Joinvillea and the grasses, and are inferred to havearm beencells near the origin of the family, but optimization of
lost independently (among the aforementioned taxa) the in
transformation to arm cells at the point of origin of the
Pharoideae and Puelia. Multicellular microhairs are uni- family is ambiguous. Placement of additional gains and
versally present within the PACCAD Clade in our sample, losses is complicated by a widespread occurrence in the
except for an autapomorphic loss in Merxmuellera rangei bambusoid and ehrhartoid clades, polymorphy within Ehr-
and a polymorphism in Spartina. The score for M. maco- harta and Leersia, total absence in Pooideae, and sporadic
occurrence in the PACCAD Clade (in Thysanolaena, Gy-
wanii was inferred from reports for the rest of the genus;
Ellis (1981) reported the absence of microhairs on nerium,the and Phragmites). This overall distribution is con-
abaxial epidermis but did not investigate the adaxial sistent
epi- with a variety of optimizations that imply multiple
origins and losses. Some taxa with arm cells lack fusoid
dermis, where they are most likely to occur. We note, how-
ever, that multicellular microhairs have not been detected
cells, and vice versa, but the occurrence of both cell types
on the abaxial leaf surface in some species of 40 PACCAD is correlated with broad leaf blades and the forest habitat.
genera, but many of these genera are polymorphic for this 46 (4 steps, CI = 0.25, RI = 0.76). Fusoid cells p/a:
Fusoid cells are large, clear, cigar-shaped empty cells that
character (Watson & Dallwitz, 1992). In contrast with their
flank each vascular bundle and can occupy up to 30% of
widespread occurrence throughout most of the family, mul-
the leaf blade volume. Although their function is still un-
ticellular microhairs occur in only two genera of the Pooi-
deae, Lygeum and Nardus. Either microhairs were lost known,
in they appear to form gas spaces rather than liquid
the common ancestor of the subfamily, followed by a sec-spaces and may play some role in plotosynthesis (Clark,
ondary gain in the common ancestor of Lygeum and Nar- 1991). Fusoid cells are absent outsi(e the Poales and,
among the families sampled in this analysis, are also ab-
dus, or were lost twice, once in Brachyelytrum, the other
time in the ancestor of all pooids except Brachyelytrum,sent in Flagellariaceae. They are present in Joinvillea and
Lygeum, and Nardus. Some taxa reported to lack multi- all three of the early-diverging lineages within the grasses.
cellular microhairs on the abaxial surface of the leaf Thus, presence of fusoid cells may be a synapomorphy of
Joinvillea
blades may have such hairs on the adaxial leaf surface or and Poaceae, but the precise point of origin of
fusoid cells is ambiguous in the present analysis, in part
elsewhere on the plant, particularly lemmas or lodicules,
and more detailed examination should be undertaken to because the character is scored as inapplicable in Res-
verify this. Only the clade within Pooideae that is tionaceae.
the Elsewhere in the grasses, fusoid cells occur
only in Bambusoideae and Streptogyn.a. Fusoid cells are
sister of Lygeum + Nardus lacks multicellular microhairs
absent in Ehrhartoideae, Pooideae, and the PACCAD
entirely, but even in this clade, unicellular microhairs
have been reported in several genera of Stipeae (WatsonClade, and this pattern is interpretable either as a syna-
& Dallwitz, 1992). pomorphic loss in BEP + PACCAD (followed by second-
44 (3 steps, CI = 0.33, RI = 0.71). "Chloridoid-type"
ary gain in Streptogyna and Bambusoideae), or parallel
losses in Ehrhartoideae, Pooideae, and the PACCAD
microhairs p/a: Tateoka et al. (1959) distinguished micro-
hairs with short and wide apical cells as "Chloridoid- Clade. Fusoid-like cells are known in some Paniceae, but
type," as they are mainly restricted to subfamily Chlori-these appear to be derived from laterally extended bundle
doideae. This type of hair is contrasted with sheath cells and thus are not homologous to fusoid cells.
"panicoid-type" microhairs, which have relatively longer
and thin-walled terminal cells and are widespread amongCHROMOSOMES
non-Chloridoid grasses. This distinction has been recog-
nized in subsequent studies (Johnston & Watson, 1976; 47 (23 steps, CI = 0.34, RI = 0.44). Base chromosome
Clayton & Renvoize, 1986; Watson & Dallwitz, 1992). Our number: This multistate character varies among taxa, is
scoring of presence vs. absence of chloridoid-type micro-scored as ambiguous in some, and is polymorphic in oth-
hairs implies that the two types are clearly distinguish- ers, so the positions of most transformations cannot be
able, but in fact there is a continuum of variation between reconstructed unambiguously. However, the base number
them (Van den Borre, 1994; Van den Borre & Watson,x = 12 in Pharoideae, Puelioideae, the BEP Clade, and
1994; E. A. Kellogg, unpublished data). In future analysesthe PACCAD Clade, suggests early establishment of this
this character should be considered very carefully, asstate. If the base numbers 11 (in Streptochaeta) and 18
many taxa may actually be intermediate or polymorphic. (in Joinvillea and Anomochloa) are derived from 12, then
This character is inapplicable for taxa scored 0 for char-x = 12 may predate the origin of the grass family, but
acter 43. Absence of chloridoid microhairs is plesiom- other reasonable interpretations also are possible. Never-
orphic for the family. This type of hair is gained in Ly- theless, our data support the interpretation that x = 12
geum, in Amphipogon, and as a synapomorphy in was established prior to divergence of Pharoideae and
Chloridoideae as traditionally circumscribed (i.e., exclud-Puelioideae from the BEP + PACCAD lineage, and that
ing Centropodia and Merxmuellera rangei). This gain inthis base number was maintained in some sublineages of
the Chloridoideae is unreversed, except for a polymor-both the BEP and PACCAD Clades. This number is main-

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Volume 88, Number 3 Grass Phylogeny Working Group 457
2001 Phylogeny and Classification of Poaceae

Arundinella, some species of Microstegium, Arthraxon,

tained (or re-evolved) in Streptogyna, Ehrhartoideae, and
some Bambusoideae, and transformations to other base and in some species of Danthoniopsis, which is here
numbers occur within the Bambusoideae (e.g., x = 11 inscored as polymorphic.
Olyreae). Within Pooideae, the occurrence of x = 10 in 49 (1 step, CI = 1.0, RI = 1.0). PCK-type carbon
Lygeum, Diarrhena, and some Meliceae suggests that this fixation, p/a: This syndrome arises once, as an unambig-
number was established early in the history of this sub-uous transformation from the "normal" NAD-ME C4 syn-
family (with x = 11 in Brachyelytrum possibly derived drome in a subclade of the Chloridoideae. Zoysia and
from x = 10 as well, but also possibly derived directly Spartina exhibit PCK-type carbon fixation, and Sporobolus
from x = 12 in the common ancestor of Pooideae and the is polymorphic for presence/absence of this character.
bambusoid/ehrhartoid lineage). x = 12 in Phaenosperma,
Ampelodesmos, and some Stipeae is interpreted here as INDEL
a IN PHYTOCHROME B
secondary transformation from x = 10, but placement of50 (2 steps, CI = 0.50, RI = 0.92). 3-bp deletion in
these lineages as early-diverging groups within Pooideae,
phytochrome, p/a: The deleted genotype (state 1) occurs
and the occurrence of x = 12 in other early-diverging in all sampled taxa of the PACCAD Clade, while the un-
lineages, suggests that this state may be a plesiomorphydeleted genotype (state 0) occurs in all other sampled
retained from its original establishment near or before the
grasses. Joinvillea has a 3-bp deletion and Flagellaria a
point of origin of the family. Transformation to x = 7 is a
12-bp deletion in this region. Sesleria (not included in the
synapomorphy of the clade that includes Brachypodium, present taxon sample) also has a 3-bp deletion (Mathews
Avena, Bromus, and Triticum, which suggests that all other
et al., 1995). The deletion occurs in a region of exon I
numbers within the tribes represented by this samplecharacterized
of by extensive length and nucleotide vari-
genera (including x = 5 in some Brachypodium, and var-
ability, and it seems likely that grasses outside the PAC-
ious numbers in Aveneae and Poeae) are derived from x
CAD Clade have a synapomorphic insertion and that the
= 7. Poeae are not sampled in this study, but they woulddeletion in Sesleria is apomorphic. Under this reconstruc-
undoubtedly be placed within the x = 7 clade. In the
tion, the deleted genotype in the PACCAD Clade would
PACCAD Clade, the base number x = 12 occurs in sev-
be synapomorphic, but the absence of data for Micraira
eral disparate taxa and is interpreted as the plesiomorphic
precludes unambiguous optimization of the transformation,
state of this clade. Among the many other base numbers which is either a synapomorphy of the entire PACCAD
in the PACCAD Clade, there are a few unambiguous Clade au- (including Micraira) or of the subclade that consists
tapomorphic transformations (e.g., to x = 9 in Molinia and
of all taxa except Micraira.
Sporobolus), but only one unambiguous synapomorphic
transformation, to x = 11, in Aristidoideae. CIHIOROPLAST GEN)ME STRUCTURE

BIOCHEMISTRY 51 (1 step, CI = 1.0, RI = 1.0). 6.4 kb inversion in

the chloroplast genome, p/a: Absence of the inversion in
48 (7 steps, Cl = 0.57, RI = 0.75). Carbon fixation
Flagellaria and Baloskioli (no infolrmation for Elegia),
couple(l
pathways: All of the non-glass outgroups andl all grasseswith presence in Joinvillea and all grasses that
outside the PACCAD Clade share the C3 photosynthetic
have been sampled, allows unambiguous optimization of
pathway. Taxa with all five C, subtypes, as wellthis
as addi-
character as a synapomorphy of Joinvillea plus Po-
tional C3 taxa, occur within the PACCAI) Clade. aceae.
These
are intermixed to such an extent that this character would 52 (1 step, CI = 1.0, RI = 1.0). trnT
l)e homoplasious even if all subtypes of C, carbon fixationchloroplast genome, p/a: Absence of t
had been scored as a single state. One unambliguous pointgellaria and Joinvillea (no information
of origin of C, carbon fixation is the transformation toRestionaceae in the present study), co
NADP-ME decarboxylation (state 1) as a synapomorphyin all grasses that have been sampled
of Panicoideae (although recent studies on the phylogeny ous optimization of this character as
of Panicoideae show that even this is ambiguous (GiussaniPoaceae. Although this character has
et al., in press)). The occurrence of NAD-ME decarbox-Elegia or Baloskion, it has been score
ylation (state 3) in Panicum is interpreted as a secondaryof Restionaceae, Chondropetalum (Doy
transformation from NADP-ME. Outside of the Panicoi- absence of the inversion in that genu
deae and the Chloridoideae (discussed below), the occur- the interpretation that this inversion i
rence of two different types of C4 decarboxylating enzymesPoaceae.
in taxa with and without mestome sheaths (states 2, 3, and53 (3 steps, CI = 0.33, RI = 0.71). 15 bp ndhF in-
5, in Aristida, Stipagrostis, and Eriachne, respectively) re-
sertion, p/a: This insertion was previously reported as pre-
quires three additional transformations, but various sent
se- in all sampled grasses except Anomochlooideae,
quences of transformation among states can explain the Pharoideae, and Oryzeae (though present in Ehrharteae),
and absent outside the Poaceae (Clark et al., 1995). New
variation observed in these three genera. Finally, the pre-
dominant occurrence of the NAD-ME type of decarbox- sequences reported here confirm this distribution except
ylation in Chloridoideae, including Centropodia but notfor the presence of the insertion in Elegia. Thus, the in-
Merxmuellera rangei (which has C, photosynthesis), sug-sertion arises independently as an autapomorphy of Elegia
gests a synapomorphic gain of this syndrome in the and an- as a synapomorphy of the Bistigmatic Clade (all grass-
cestor of Chloridoideae, followed by a return to C3 pho-
es except Anomochlooideae and Pharoideae); it is second-
tosynthesis in Merxmuellera rangei, but multiple gains arily
of lost (i.e., deleted) in the ancestor of (or within) the
the NAD-ME subtype also are possible. Reversal fromOryzeae.
C4 Examination of this character in other Restion-
to C3 also occurs in Eragrostis walteri (van den Borre,aceae and related families such as Anarthriaceae, Ecdeio-
1994). State 4, the NADP-ME Arundinella-type, occurs coleaeae,
in and Centrolepidaceae is warranted.

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