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Biodiversity and taxonomy of the pleomorphic genus Alternaria

Article in Mycological Progress · January 2016

DOI: 10.1007/s11557-015-1144-x

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Mycol Progress (2016) 15:3
DOI 10.1007/s11557-015-1144-x

REVIEW

Biodiversity and taxonomy of the pleomorphic genus Alternaria

Daniel P. Lawrence 1 & Francesca Rotondo 2 & Philipp B. Gannibal 3

Received: 24 May 2015 / Revised: 8 November 2015 / Accepted: 13 November 2015

# German Mycological Society and Springer-Verlag Berlin Heidelberg 2015

Abstract The genus Alternaria, alternarioid hyphomycetes, Keywords Fungi . Systematics . Alternarioid
comprise a biologically, ecologically, and morphologically hyphomycetes . Plant pathogens . Taxonomic section
rich group of fungi that has suffered from taxonomic flux for
many years. The taxonomy of these fungi has been predomi-
nately based on conidial characters, which includes shape, Introduction
color, septation, and patterns of secondary sporulation, and
to lesser extent on host association, biochemistry, and metab- Alternarioid hyphomycetes have been classified into no less
olites. Recent phylogenetic studies have made significant than 14 genera which typically produce phaeodictyospores or
changes to the systematic taxonomy, the accurate identifica- phaeophragmospores. The taxonomy of these genera has been
tion of a taxon or group of taxa, within Alternaria by elevating debated for many years, and several cycles of classification
26 clades to the subgeneric taxonomic status of section. This and subsequent revisions have occurred. Before the advent of
paper aims to serve as an overview of the historical and con- molecular technologies, these genera were classified based
temporary taxonomic status of the alternarioid hyphomycetes upon their morphological characteristics (Simmons 1954,
with special reference to biology, morphology, and phyloge- 1971, 1983, 1990a, 1992; Joly 1964). The morphological
netic biodiversity. Additionally, we propose to synonymize classification of alternarioid hyphomycetes reached its pinna-
the genus Pseudoalternaria with Alternaria and elevate this cle with the work of E.G. Simmons (Simmons 1967, 1971,
well-supported clade to the taxonomic rank of section, 1989, 1992, 2007) in which he defined the alternarioid mor-
Pseudoalternaria sect. nov., bringing the total number of sec- pho-species, and defined the distinctive traits for each of the
tions to 27 in order to produce a stable and accepted taxonomy species described. In recent years, phylogenetic investigations
for this diverse genus. (Lawrence et al. 2013, 2014; Pryor and Bigelow 2003; Runa
et al. 2009; Woudenberg et al. 2013) have supported the main
morphological groups identified by Simmons.
Alternarioid hyphomycetes occupy diverse ecological
Section Editor: Roland Kirschner modes ranging from saprobes, to endophytes, to pathogens.
* Philipp B. Gannibal
Most of the alternarioid species are considered to be cosmopol-
[email protected] itan saprobes that are ubiquitous through natural and man-made
environments. As plant pathogens, Altenaria spp. are well
1
known for their ability to produce a wide spectrum of second-
Department of Plant Pathology, University of California,
Davis, CA 95616, USA
ary metabolites (Andersen et al. 1995, 2001, 2002, 2005;
2
Andersen and Thrane 1996; Christensen et al. 2005; Frisvad
Department of Plant Pathology, The Ohio State University, Ohio
Agricultural Research and Development Center, Wooster, OH 44691,
et al. 2008; Serdani et al. 2002; Walton and Panaccione 1993).
USA These metabolites include various plant pathogenesis related
3
Laboratory of Mycology and Phytopathology, All-Russian Institute
toxins, both host and non-host specific (Fujiwara et al. 1988;
of Plant Protection, Shosse Podbelskogo 3, Saint Petersburg 196608, Markham and Hille 2001; Meronuck et al. 1972; Nishimura
Russia and Kohmoto 1983; Otani et al. 1995; Robeson and Strobel
3 Page 2 of 22 Mycol Progress (2016) 15:3

1981; Thuleau et al. 1988; Wolpert et al. 2002) and mycotoxins The third stage (1930s–1960s): revisions of Alternaria and
that can contaminate food products (Alexander et al. 2011; Macrosporium Several attempts were made to delimit these
Fernández-Cruz et al. 2010; Lau et al. 2003; Logrieco et al. genera and Stemphylium to determine their taxonomic status.
1990, 2003; Ostry 2008). Small-spored Alternaria spp. (e.g., Every attempt to define the genus Alternaria has encountered
A. alternata) also have a prominent role in inducing allergenic the problem of treating numerous taxa which superficially re-
symptoms and cause severe asthma pathologies (Bush and semble the type species of Alternaria, Macrosporium, or
Portnoy 2001; Esch et al. 2001; Salo et al. 2006). Here, we Stemphylium. Wiltshire’s (1933) main conclusion was that
present a detailed description of the main characteristics defin- Macrosporium should be suppressed as a nomen ambiguum in
ing the alternarioid hyphomycetes, including a thorough treat- favor of Alternaria. However, this conclusion was not
ment of their taxonomic and natural history, ecology, and im- immediately and unconditionally accepted. Neergaard (1945)
pact on human activity. Throughout this review, we hope to proposed three morphological Alternaria groups, calling them
highlight the necessity to recognize the complexity and biolog- sections, based upon conidial catenation: section Longicatenatae
ical diversity of this important group of fungi. typified by A. tenuis (= A. alternata) with 10 or more catenulate
conidia; section Brevicatenatae typified by A. tenuissima with
short chains of 3–5 conidia; and section Noncatenatae typified
by A. brassicae with conidia borne singly or rarely producing a
Taxonomic history and confusion between Alternaria secondary conidium. Joly (1964) classified species of Alternaria
and allied genera into three sections based primarily on conidial color, rigidity, or
lateral symmetry: section Claroseminae with light to translucent
The genus Alternaria comprises a group of fungi in the family yellowish colors; section Brunneoseminae with brown to
Pleosporaceae (Pleosporales, Dothideomycetes, reddish-brown darkly pigmented conidia; and section Rigidae
Ascomycota). Alternaria was established by Nees in 1816 with conidia that have a rigid appearance with a dearth of lon-
and since then its taxonomy has been disputed. Taxonomy gitudinal septa. The above-mentioned classification schemes did
of Alternaria and related genera has gone through five stages. not follow the rules of nomenclature, were not widely adopted,
Here, we give brief characteristics of each stage. and are not used today.

The first stage (1816–1850s): assessing alternarioid hypho- The fourth stage (1960s–2000s): Emory Guy Simmons
mycete biodiversity During that time, four genera, Alternaria (1920–2013) Simmons undertook a complete reappraisal
Nees 1816, Brachycladium Corda 1838, Macrosporium Fr. and revision of all names and taxa related to the genus
1832, and Ulocladium Preuss 1851 that have direct relation- Alternaria. Simmons studied very thoroughly and carefully
ships to alternarioid hyphomycetes, were described. An allied probably all published descriptions, all type herbarium sam-
genus, Stemphylium Wallr. 1833, was also described at this ples and living strains. At the same time, other mycologists
time. In the beginning, the genera Alternaria, described a number of new species (approx. 150 legitimate
Macrosporium, and Stemphylium were confused, while names), but the number of Simmons’s taxonomic novelties
Brachycladium and Ulocladium were consigned to oblivion. (approx. 200) is the largest in the history of Alternaria.
Only a few species were described during the first stage of
Alternaria taxonomic assessment. The type species of At this time, the genus Alternaria and other morphologi-
Alternaria was A. tenuis Nees 1816, but the first validly pub- cally similar genera that produce pigmented or dark-colored
lished species name was Torula alternata Fr., 1832. muriform spores were called “phaeodictyosporic hyphomy-
cetes”. Until the 1970s, all phaeodictyosporic hyphomycetes
were divided into three large genera: Alternaria,
The second stage (1850s–1930s): description of new spe- Macrosporium, and Stemphylium. The generic boundaries
cies Almost 400 specific epithets appeared during this pe- were formidably confusing. A fourth genus, Ulocladium,
riod. Approximately 300 species names were described was disregarded by taxonomists for a period of more than
under the generic name Macrosporium. By the end of the 100 years. This stage resulted in substantial revision of those
period, the first attempt to revise the taxonomy and genera and resulted in abolition of Macrosporium in 1969
nomenclature of Alternaria and Macrosporium was because the type species of the genus, M. cheiranthi, was
published by Elliott (1917) in which he classified them into considered to be an Alternaria species (Simmons 1992). The
morphological groups based on conidial characteristics and genera Alternaria, Stemphylium, and Ulocladium were typi-
proposed six morphological Alternaria groups with a rep- fied by Simmons in 1967. The type specimen of Torula
resentative species typifying each group. This produced alternata Fr. 1832 was identified by Simmons as synonymous
the first signs of the increasing nomenclatural problems with Nees 1816 description of A. tenuis; therefore, he declared
within the alternarioid hyphomycetes. A. alternata as the type for the genus (Simmons 1967). Later,
Mycol Progress (2016) 15:3 Page 3 of 22 3

several new genera were segregated from Alternaria: that the informal groups proposed by Simmons and others
Alternariaster E.G. Simmons 2007, Chalastospora E.G. were morphological groups that did not follow the rules of
Simmons 2007, Embellisia E.G. Simmons 1971, Nimbya nomenclature and had no relationship to phylogeny. All minor
E.G. Simmons 1989, and Teretispora E.G. Simmons 2007. details of conidial shape were utilized by Simmons for taxo-
The genus Prathoda Subram. 1956 was resurrected by nomic purposes. To date, perhaps all available morphological
Simmons in 2007 (by transferring Alternaria longissimi to traits have been inventoried and utilized for alternarioid hy-
Prathoda), and approximately 280 Alternaria species were phomycete taxonomy. Simmons has made major contribu-
considered as legitimate and recognizable. Simmons began tions in this area and is credited for studying Alternaria and
to promote a practice of utilizing Alternaria representative other phaeodictyosporic hyphomycetes for over 50 years and
strains for taxonomy and identification. publishing many articles and an identification manual
Differentiation of the aforementioned taxa was based on a (Simmons 2007). Simmons has to his credit approximately
number of exclusive morphological traits, particularly conid- 150 new Alternaria species and 25 new combinations. At this
ial shape (Simmons 1967, 1992, 2007). Previous work re- stage, order was established in the nomenclature of
vealed that various culturing conditions could greatly influ- alternarioid hyphomycetes. Up to the end of the 2000s, the
ence conidial morphology (Leach and Aragaki 1970; Zitter Alternaria nomenclature system intended to reflect maximum
and Hsu 1990). For this reason, Simmons and Roberts morphological diversity, to catalog biodiversity, and to allow
(1993) delineated optimal standardized growing conditions for morphological identification (Gannibal 2012).
to produce consistent and reproducible sporulation patterns
of alternarioid hyphomycetes. Furthermore, some novel traits The fifth stage (2003–2015): molecular phylogenetic tax-
were utilized, e.g., three-dimensional sporulation pattern, onomy This stage has employed a comprehensive DNA-
shape of juvenile conidia, width of septa, etc. Several morpho- based approach for the analysis of alternarioid hyphomycete
logical Alternaria species-groups (complexes) were described biodiversity. Both morphological and molecular data have
by Simmons (1992) and typified by a representative species. been the basis for several taxonomic revisions. The first mo-
Simmons defined a species-group as a group of taxa that pro- lecular phylogenetic analysis of Alternaria and other closely
duce similar patterns of sporulation and share a high degree of related phaeodictyosporic hyphomycete genera, Stemphylium
conidial morphological characters only and have no relation- and the former genus Ulocladium, was conducted by Pryor
ship to phylogeny or nomenclatural rules. Examples include and Gilbertson (2000). That study provided robust phyloge-
the A. alternata species-group with taxa that produce small netic support for the sister relationship of Stemphylium and
catenate conidia such as A. alternata, and the A. porri species- Alternaria, and also provided strong support for several pre-
group with taxa that produce large, long tapering apical beak, viously described morphological species-groups (i.e., the
and typically non-catenate conidia such as A. porri. Simmons alternata-, porri-, brassicicola-, and the infectoria species-
and Roberts (1993) further subdivided the small-spored groups) as discrete phylogenetic species-groups based on the
catenulate species of Alternaria into six morphological analysis of internal transcribed spacer (ITS) and 18S mtSSU
groups. Group 1 was characterized as producing a modest (mitochondrial small subunit) molecular markers. Pryor and
spore size with moderate to short conidial chains of 5–10; Gilbertson (2000) also described the radicina species-group,
Group 2 with A. gaisen as the representative producing a larg- which was supported by morphological and molecular data as
er and more robust spore with moderate to short conidial cat- a clade nested amongst the Alternaria lineage.
enation (5–10); Group 3 taxa produced short (50–70 μm) to
very long (100–150 μm) conidiophores that produced copious Subsequent studies, which included morphological and
amounts of secondary sporulation by the elongation of molecular data, have elucidated additional Alternaria lineages
subconidium conidiophores; Group 4 produced short bushy which included the sonchi species-group (Hong et al. 2005),
clumped conidiophores with extensive secondary sporulation, the alternantherae species-group (Lawrence et al. 2012) where
represented by A. alternata; Group 5 produced moderately three taxa were transferred from the genus Nimbya to
long to long chains of conidia, 10–15(20), with rare to no Alternaria, and the panax- and gypsophilae species-groups
secondary braches; and Group 6 with A. infectoria as the rep- (Lawrence et al. 2013). A total of nine Alternaria species-
resentative, producing clumps of secondary and tertiary groups were identified: the alternata-, alternantherae-,
branching chains with a complex three-dimensional structure. brassicicola-, gypsophilae-, infectoria-, panax-, porri-,
Simmons also developed additional morphological species- radicina-, and sonchi species-groups. Alternaria species-
groups based solely upon colony and conidium characteris- groups were defined as a group of taxa that shared a high
tics, including the A. infectoria species-group, the degree of conidial morphological characters, and that cluster
A. tenuissima species-group, the A. cheiranthi species-group, as discrete strongly supported monophyletic groups based up-
and the A. brassicicola species-group (Simmons 1995; on molecular phylogenetic approaches utilizing DNA se-
Simmons and Roberts 1993). Again, it should be emphasized quence data. On the generic level, the alternarioid
3 Page 4 of 22 Mycol Progress (2016) 15:3

hyphomycetes were enlarged by the resurrection of the genus the total number of sections to 27 by synonymizing the genera
Brachycladium (Inderbitzin et al. 2006) and typification of Allewia E.G. Simmons 1990, Brachycladium, Chalastospora,
three new genera Undifilum B.M. Pryor, Creamer, Chmelia Svob.-Pol. 1966, Crivellia Shoemaker & Inderb. 2006,
Shoemaker, McLain-Romero & Hambl. (Pryor et al. 2009), Embellisia, Lewia M.E. Barr & E.G. Simmons 1986, Nimbya,
Sinomyces Yong Wang & X.G. Zhang (Wang et al. 2011), and Pseudoalternaria, Sinomyces, Teretispora, Ulocladium,
Pseudoalternaria D.P. Lawr., Gannibal, Dugan & Pryor Undifilum, and Ybotromyces Rulamort 1986 with Alternaria
(Lawrence et al. 2014). These new genera were erected to (Woudenberg et al. 2013, 2014). Figure 1 depicts a consensus
accommodate morphological and phylogenetic novelties. cladogram of Alternaria sections based upon seven nuclear loci
Continued phylogenetic analyses of Alternaria have utilized from Lawrence et al. (2013, 2014), Woudenberg et al. (2013),
nuclear rDNA (ribosomal DNA) and the intervening ITS and Grum-Grzhimaylo et al. (2015).
regions, mtSSU, and many protein-coding genes Given the overlap of morphological features among
[glyceraldehyde-3-phosphate dehydrogenase (gpd), endo- Alternaria species/sections and the morphological plasticity
polygalacturonase, Alternaria major allergen Alt a 1, beta-tu- of some species, phylogenetic species recognition is now be-
bulin, translation elongation factor 1-alpha (TEF 1-α), the sec- coming standard within the genus. Several loci have been
ond largest subunit of RNA polymerase II (RPB2), calmodulin, shown to be more informative than others for species delimi-
chitin synthase, Tsr1, plasma membrane ATPase, actin, and 1,3, tation (Lawrence et al. 2013). Within Alternaria, the utility of
8–trihydroxynaphthalene (THN)] to produce phylogenetic hy- ITS for species identification, which is the universal barcoding
potheses at different phylogenetic scales. Most studies have gene for Fungi (Nilsson et al. 2014), has been hotly debated
provided strong support for the above-mentioned phylogenetic because several morphological species (e.g., A. alternata and
species-groups; however, no studies were able to resolve the A. tenuissima) are either 100 % identical or nearly so.
order of divergence of the described species-groups (Andrew Statistical tests of phylogenetic informativeness performed
et al. 2009; Hong et al. 2005; Lawrence et al. 2012; Pryor et al. by Lawrence et al. (2013) revealed that the plasma membrane
2009; Pryor and Gilbertson 2000). ATPase, calmodulin, and Alt a 1 loci were the most
Previous evolutionary studies have shown that an increase in
taxon and loci sampling may increase statistical support for key
phylogenetic nodes (Rokas and Carroll 2005). Lawrence et al.
(2013) analyzed 10 nuclear protein-coding loci for the ability to
resolve species-group relationships. In that study, the authors
revealed that two loci, beta-tubulin and TEF 1-α, were unable
to resolve relationships (polytomous) among Alternaria species-
groups likely due to their slow tempo of molecular evolution,
which is useful for high-level phylogenetic studies (Baldauf and
Palmer 1993; Cheney et al. 2001; Stiller and Hall 1997). In that
same study, the authors revealed a phenomenon that is common-
ly encountered in fungal molecular systematics, substitution sat-
uration of the third codon position of protein-coding genes
(Hansen et al. 2005; Liu et al. 1999; Matheny et al. 2007;
Miller and Huhndorf 2005; Sung et al. 2007). They revealed
for the first time that three loci, RPB2, Tsr1, and chitin synthase,
possessed statistically significant transition substitution satura-
tion at the third codon position, causing these loci to be phylo-
genetically uninformative for high-level Alternaria phylogenetic
studies (Lawrence et al. 2013). The phylogenetic utility of five
protein-coding loci (gpd, Alt a 1, actin, plasma membrane Fig. 1 Phylogeny, taxonomy, and mating system of alternarioid
ATPase, and calmodulin) from Lawrence et al. (2013) provided hyphomycetes. Cladification derived from manual combination of four
the first strongly supported phylogenetic hypothesis among phylogenetic trees based on analysis of sequences of seven nuclear genes
(Lawrence et al. 2013, 2014; Woudenberg et al. 2013; Grum-Grzhimaylo
Alternaria lineages. Lawrence et al. (2013) elevated eight phy- et al. 2015). Type of mating system: 1 heterothallism, only one of two
logenetic Alternaria species-groups to the taxonomic status of idiomorph of MAT1 locus present in a genome; 2 homothallism, both
section each with a type specimen. Similarly, 18 additional phy- idiomorphs of MAT1 locus present in a genome; ns not studied (data for
logenetic groups have been elevated to the status of section sect. Infectoriae obtained from Andersen et al. 2009; data for sect.
Nimbya obtained from Johnson et al. 2002; data for sect. Crivellia
within Alternaria, and we propose an additional section, section obtained from Inderbitzin et al. 2006; data for Stemphylium obtained
Pseudoalternaria D.P. Lawr., Rotondo & Gannibal sect. from Inderbitzin et al. 2005; other data obtained from Gannibal and
nov. (based on the study by Lawrence et al. 2014), bringing Kazartsev 2013 and Gannibal, unpublished)
Mycol Progress (2016) 15:3 Page 5 of 22 3

informative. The Alt a 1 locus unreliably amplifies some spe- of Alternaria and sister to Pleospora Rabenh. ex Ces. & De
cies within sect. Infectoriae, therefore we suggest that the Not. 1863, therefore Paradendryphiella is not discussed.
most suitable genetic markers for molecular identification of Below is an updated description of the genus Alternaria
species within the genus Alternaria are the plasma membrane which also includes a brief review of the morphology and
ATPase and calmodulin loci (Lawrence et al. 2013). phylogenetic position of each section that comprises the
alternarioid hyphomycetes.
Colonies effuse, usually gray, greenish, dark olivaceous,
Morphology and molecular phylogeny of Alternaria dark blackish-brown or black. Mycelium immersed and usu-
sections ally surface; hyphae colorless, olivaceous-brown or brown.
Stroma rarely formed. Setae and hyphopodia absent.
Alternaria species are characterized as alternarioid hyphomy- Conidiophores macronematous, mononematous, simple or ir-
cetes that produce darkly pigmented multi-celled conidia that regularly and loosely branched, pale brown or brown, solitary
are typically dictyosporous, some phragmosporous, or in fascicles. Conidiogenous cells integrated, terminal be-
catenulate, some borne singly (Fig. 2) (Inderbitzin et al. coming intercalary, polytretic, sympodial, or sometimes
2006; Lawrence et al. 2014; Preuss 1851; Pryor et al. 2009; monotretic, cicatrized. Conidia solitary or in chains, dry, ba-
Simmons 1971, 1989, 2007; van Zinderen 1940). The genus sically ovoid, obovoid, cylindrical, narrowly ellipsoid or
Alternariaster is not included in this review because a recent obclavate, beaked or non-beaked, pale or medium
study revealed that this genus resides in the Leptosphaeriaceae olivaceous-brown to brown, smooth or verrucose, with trans-
and not the Pleosporaceae (Alves et al. 2013). The genus verse and with or without oblique or longitudinal septa. Septa
Paradendryphiella Woudenberg et al. 2013 was recently can be thick, dark and rigid and an internal cell-like structure
erected to accommodate the former species Embellisia can be formed. Species with meristematic growth are known.
annulata which has been shown to consistently cluster outside Ascomata small, solitary to clustered, erumpent to (nearly)

Fig. 2 Conidia of a Alternaria alternantherae EGS 52–039 (sect. A. calycipyricola EGS 52–072 (sect. Panax), n A. mouchaccae EGS
Alternantherae), b A. arborescens EGS 39–128 (sect. Alternaria), c 31–061 (sect. Phragmosporae), o A. linariae CBS 109156 (sect. Porri),
A. brassicicola BMP 0325 (sect. Brassicicola), d A. abundans BMP p A. arrhenatheri BMP 1942 (sect. Pseudoalternaria), q A. chartarum
1928 (sect. Chalastospora), e A. cheiranthi EGS 41–188 (sect. BMP 0359 (sect. Pseudoulocladium), r A. selini EGS 35–178 (sect.
Cheiranthus), f A. embellisia EGS 38–073 (sect. Embellisia), g Radicina), s A. cinerariae EGS 33–169 (sect. Sonchi), t A. leucanthemi
A. proteae EGS 39–031 (sect. Embellisioides), h A. limicola BMP 2239 EGS 17–063 (sect. Teretispora), u A. atra BMP 0353 (sect.
(sect. Euphorbiicola), i A. eureka EGS 36–103 (sect. Eureka), j Ulocladioides), v A. alternariae BMP 0352 (sect. Ulocladium), w
A. infectoria EGS 27–193 (sect. Infectoriae), k A. japonica BMP 0332 Alternaria sp. BMP 0951 (sect. Undifilum)
(sect. Japonicae), l A. scirpicola EGS 19–016 (sect. Nimbya), m
3 Page 6 of 22 Mycol Progress (2016) 15:3

Fig. 2 (continued)

superficial at maturity, globose to ovoid, dark brown, smooth septum lacking a septal plate and perforated by cytoplasmic junc-
or setose, apically papillate, ostiolate. Papilla short, blunt. tions) and euseptate (septum formed from a septal plate). Conidia
Peridium thin. Hamathecium of cellular pseudoparaphyses. are large (80–112×18–20 μm) and transversely septate with no
Asci few to many per ascoma, (4–6–)8-spored, basal, bitunicate, or 1–2 longitudinal or oblique septa, sometimes slightly constrict-
fissitunicate, cylindrical to cylindro-clavate, straight or some- ed at some transverse septa (Fig. 2a). Lumina of transverse sec-
what curved, with a short, furcate pedicel. Ascospores muriform, tions are octagonal to rounded. The conidial beak is unbranched,
ellipsoid to fusoid, slightly constricted at septa, yellow-brown, long filiform (100–470×2–4 μm), septate or aseptate, sometimes
without guttules, smooth, 3–7 transverse septa, 1–2 series of with terminal swelling. Section Alternantherae is strongly sup-
longitudinal septa through the two original central segments, ported as the sister group to sect. Alternaria.
end cells without septa, or with one longitudinal or oblique sep-
tum, or with a Y-shaped pair of septa. Section Alternaria D.P. Lawr., Gannibal, Peever & B.M.
Type: Alternaria alternata Nees (1816). Pryor 2013
Taxonomic position: Eukarya: Fungi: Ascomycota: Type species: Alternaria alternata (Fr.) Keissl.
Pezizomycotina: Dothideomycetes: Pleosporomycetidae: This section was named by Lawrence et al. (2013), since it
Pleosporales: Pleosporaceae: Alternaria includes the type for the genus. This version is correct according
to ICBN Arts 22.1 and 22.2. Woudenberg et al. (2013) generated
Section Alternantherae D.P. Lawr., Gannibal, Peever & an orthographic variant ‘Alternata’, which is contradictory to the
B.M. Pryor 2013 ICBN rules and should not be in use because the name of the
Type species: Alternaria alternantherae (Holcomb & subdivision that contains the type species must repeat the generic
Antonop.) name unaltered. Section Alternaria consists of approximately 60
Section Alternantherae is comprised of four species species that are commonly referred to in the literature as small--
(A. alternantherae, A. celosiicola, A. gomphrenae, and spored Alternaria (e.g., A. alternata, A. arborescens, A. gaisen,
A. perpunctulata) that were separated from the former genus and A. tenuissima). Primary conidiophores are curved or straight,
Nimbya based on morphological and phylogenetic data. short to very long, simple or branched with one to several termi-
Primary conidiophores are short to moderately long (70–125× nal conidiogenous loci. Conidia are borne in moderately long to
4–5 μm) and possess one to a few conidiogenous loci, the long chains that are simple or branched. Conidia are small or
conidiogenous tip may be slightly enlarged. Conidia are solitary moderate in size, 20–35(60)×8–12 μm, obclavate, long ellipsoid
or rarely paired, narrowly ellipsoid, sometimes subcylindrical, or ellipsoid, transversely septate 3–7(11), with slight constriction
rarer narrow ellipsoidal, or near obclavate, distoseptate (a thin at some septa, and 1–2 longitudinal septa in one or a few
Mycol Progress (2016) 15:3 Page 7 of 22 3

transverse divisions. Most conidia gradually narrow into a ta- 30×3–5 μm), commonly flask-shaped arising from surface
pered apical beak or secondary conidiophore (Fig. 2b). Apical hyphae or from lateral branches of rope-like aerial hyphae
beak (5–10 μm sometimes up to 35 μm) is generally shorter than with one to several conidiogenous loci (Crous et al. 2009).
the conidial body. Secondary conidiophores may be formed api- Conidia are ovoid, narrowly ellipsoid to ellipsoid with no
cally or laterally and are short to moderately long, with one or a apical beak, no to multiple (1–3) transverse septa with no
few conidiogenous loci. Ascomata of A. alternata are typically or rare longitudinal septa. Conidia are small (18–22(35)×
small (170–200×190–240 μm) solitary or clustered, erumpent, 3–4(6)μm), rarely solitary, generally in long chains up to
globose to ovoid, smooth, dark brown, apically papillate, 15 units. Secondary conidiophores are usually absent, but
ostiolate. Asci are relatively straight (170–190×23–30 μm), may be formed apically or laterally with one to a few
(4–6–) 8-spored, bitunicate, fissitunicate, cylindrical to conidiogenous loci. Molecular phylogenetic studies
cylindro-clavate in shape. Ascospores are 37–43×13–14 μm, strongly suggest that sect. Chalastospora is sister to sec-
ellipsoid to fusoid with slight constriction at some septa, 3–7 tions Infectoriae and Pseudoalternaria (Crous et al. 2009;
transverse septa, 1–2 longitudinal septa in central segments, Hong et al. 2005; Lawrence et al. 2012, 2013, 2014.
end cells with no septa or one longitudinal or oblique septum Interestingly, two species A. abundans (Fig. 2d) and
or Y-shaped pair of septa, brown, eguttulate, smooth A. armoraciae (see Woudenberg et al. 2013), do not resem-
(Ariyawansa et al. 2015). Section Alternaria shares a close evo- ble other species in this clade, but rather species formerly
lutionary relationship with sections Alternantherae, described as Embellisia sensu lato, with the production of
Euphorbiicola, and Porri. mostly phragmoconidia that are typically short and not
elongated as in other species in this clade.
Section Brassisicola D.P. Lawr., Gannibal, Peever &
B.M. Pryor 2013 Section Cheiranthus Woudenb. & Crous 2013
Type species: Alternaria brassicicola (Schwein.) Wiltshire Type species: Alternaria cheiranthi (Lib.) P.C. Bolle
Section Brassicicola consists of five described species Section Cheiranthus consists of two species (A. cheiranthi
(A. brassicicola, A. conoidea, A. mimicula, A. septorioides, and A. indefessa) which are characterized as producing short to
and A. solidaccana). Primary conidiophores are short to mod- moderately long primary conidiophores that may be simple or
erately long (15–150×5–6 μm), simple or branched with one branched with one or multiple conidiogenous loci. Conidia are
or several apical conidiogenous loci. Chains of conidia are dictyosporous, ovoid to broadly ellipsoid with slight to strong
long to moderately long, simple or branched. Conidia are el- constrictions at some transverse septa, catenate in short to long
lipsoid, ovoid or somewhat obclavate, small to moderate chains that are simple or branched (Fig. 2e). Secondary conidi-
(20–95×7–22 μm) in size, typically with solitary apical and ophores may be formed apically or laterally with one
sometimes with solitary lateral secondary conidiophores that conidiogenous locus. Previous phylogenetic studies have placed
are shorter than the conidium body and have only one these species sister to the ovoid catenate sect. Pseudoulocladium
conidiogenous locus (Fig. 2c). Conidia are septate with slight and to the obovoid noncatenate sect. Ulocladioides (Runa et al.
to strong constrictions at transverse septa and no or a few or 2009; Lawrence et al. 2012, 2013; Woudenberg et al. 2013).
many longitudinal septa. The apical cell of a terminal co-
nidium is wide and rounded. Chlamydospores may ap- Section Crivellia (Shoemaker & Inderb.) Woudenb. &
pear. Based on a five protein-coding gene analysis sect. Crous 2013
Brassicicola is most closely related to sections Panax, Type species: Alternaria penicillata (Corda) Woudenb. &
Gypsophilae, Sonchi, Radicina, Porri, Euphorbiicola, Crous
Alternaria, and Alternanatherae (Lawrence et al. 2013). Section Crivellia is comprised of two species
(A. papavericola and A penicillata), both are important patho-
Section Chalastospora (E.G. Simmons) Woudenb. & gens of opium poppy (Czyzewska and Zarzycka 1960;
Crous 2013 Milatovic 1952). Alternaria papavericola is characterized by
Type species: Alternaria cetera E.G. Simmons unbranched primary conidiophores (20–30×4–5 μm) with de-
The genus Chalastospora was conceived by Simmons velopment of conidiogenous loci (2–4) at the apex. Conidia are
(2007) by which he re-classified Alternaria cetera, origi- small, cylindrical (17–70×4–8 μm) with tapered apices, solitary
nally isolated from Elymus scrabus, as Chalastospora or rarely short-catenate from the apical pore, characterized by
cetera because the conidia “have alternarioid qualities only transverse septa (3–6) and absence of longitudinal septa.
in the most tenuous sense” (Simmons 2007). Production of microsclerotia has not been observed in culture.
Section Chalastospora currently consists of six species, Alternaria penicillata is characterized by the formation of
A. abundans, A. armoraciae, A. breviramosa, A. cetera, macro- and microconidiophores. Macroconidiophores (400–
A. malorum, and A. obclavata. Primary conidiophores are 600×20–35 μm) are generally straight, branched at the terminal
solitary, smooth, and brown in color, short to long (10– region and arise from a globose cell (20–30 μm in diameter) or
3 Page 8 of 22 Mycol Progress (2016) 15:3

from a basal group of cells that resemble a microsclerotium. culture (Simmons 1971, 1983). Phylogenetic studies sug-
Microconidiophores (30–40×4–6 μm) are simple, branched to- gest that sect. Embellisia is most closely related to
ward the apex and arise from an undifferentiated mycelium. s ec t i on s Phr a gm os p or a e, S od a , C ha l a s t o s p o r a ,
Conidia are cylindrical (17–30×5–7 μm) with transverse septa. Pseudoalternaria, and Infectoriae.
Microsclerotia (20–100×25–75 μm) are produced in artificial
media and on natural substrates. Alternaria penicillata forms Section Embellisioides Woudenb. & Crous 2013
ascocarps (320–400×220–300 μm) that are solitary or clustered, Type species: Alternaria hyacinthi (de Hoog & P.J. Mull.
globose to depressed globose, interdispersed with dark Bis) Woudenb. & Crous
microsclerotia and macroconidiophores. Asci are numerous with Section Embellisioides consists of six species
ellipsoidal uniseriate or biseriate ascospores (20–25×6–9 μm). (A. botryospora, A. hyacinthi, A. lolii, A. planifunda,
The phylogenetic position of sect. Crivellia within the genus A. proteae, and A. tumida) obtained from plants or rhizo-
Alternaria is not certain. sphere. Conidiophores simple, short or moderately long,
straight or often with multiple, geniculate, sympodial pro-
Section Dianthicola Woudenb. & Crous 2013 liferations. Conidia are solitary or in short chains, obovoid
Type species: Alternaria dianthicola Neerg. to ellipsoid, rarely short subcylindrical (Fig. 2g). Apical
Section Dianthicola is comprised of three species and basal cells are wide rounded or short conical.
(A. dianthicola, A. elegans, and A. simsimi) that produce simple Conidia have several transverse and longitudinal septa;
or branched primary conidiophores which may or may not pro- transverse septa can be thick, dark and rigid in contrast to
duce apical proliferations. Conidial shapes vary from narrowly the external wall. Some mature conidia can have no longi-
ovoid to narrowly ellipsoid with multiple transverse septa and tudinal or oblique septa. Apical or lateral, short secondary
few longitudinal septa with a filiform beak or apical secondary conidiophores may occur. Chlamydospores and a sexual
conidiophores that are solitary or in short chains. Based on a morph may occur. Pseudothecia, if present, are ovoid to
three protein-coding gene analysis, sect. Dianthicola is sister to spheroid, dark, thin-walled, papillate towards the apex as
sect. Ulocladioides (Woudenberg et al. 2013). asci mature, markedly setose. Asci are subellipsoid to
subcylindrical, straight to somewhat inequilateral,
Section Embellisia (E.G. Simmons) Woudenb. & Crous bitunicate, usually 8-spored. Immature ascospores are
2013 subellipsoid and slightly inequilateral; mature ascospores
Type species: Alternaria embellisia Woudenb. & Crous are ellipsoid to subclavate, with multiple transverse septa,
The genus Embellisia was established to separate an discontinuous series of longitudinal septa through major
atypical species of Helminthosporium Link 1809, H. allii central spore compartments, and with or without a longi-
Campan., originally isolated from garlic, based solely on tudinal septum in terminal cells. Phylogenetic data support
conidial and conidiophore morphology (Simmons 1971). the sister relationship with sect. Eureka.
Simmons noted that H. allii produced conidiophores as
successive sympodial proliferations which were inconsis- Section Euphorbiicola Woudenb. & Crous 2014
tent with the erect growth of Helminthosporium conidio- Type species: Alternaria euphorbiicola E.G. Simmons &
phores and were more similar to conidiophores produced Engelhard
by Curvularia Boedijn 1933, Bipolaris Shoemaker 1959, Section Euphorbiicola consists of two species,
Drechslera S. Ito 1930, Alternaria, and Ulocladium A. limicola and A. euphorbiicola. Conidia are character-
(Alcorn 1988, 1991; Shoemaker 1959, 1962; Simmons ized as ovoid to obclavate, medium to large, disto- and
1967). Section Embellisia consists of three species, euseptate, catenulate in short to moderately long chains,
A. chlamydosporigena, A. embellisia, and A. tellustris, terminal conidia have no or a simple long apical beak
which produce large populations of phragmoconidia with (Fig. 2h). Conidia possess multiple transverse septa (some
a very low percentage of dictyoconidia as opposed to the constriction at some transverse septa) and some longitu-
strict production of phragmoconidia produced by dinal septa. Secondary conidiophores may be produced
Curvularia, Bipolaris, and Drechslera. Additionally, the apically or laterally. Section Euphorbiicola is sister to
conidia of sect. Embellisia possess distinctly dark, rigid sect. Porri (Woudenberg et al. 2014).
and thickened transverse septa as compared to the external
wall (Fig. 2f). Conidia are variously swollen, usually Section Eureka Woudenb. & Crous 2013
straight elliptical or oblong elliptical with a small popula- Type species: Alternaria eureka E.G. Simmons
tion that may be smoothly curved or sigmoid and typical- Section Eureka consists of six species (A. anigozanthi,
ly borne singly. Conidiogenous sites at conidiophore A. cumini, A. eureka, A. geniostomatis, A. leptinellae, and
geniculations are umbilicate, hyphal coils and intra- A. triglochinicola) that were isolated from plants or rhi-
hyphal proliferating chlamydospores are produced in zosphere. Primary conidiophores simple or branched,
Mycol Progress (2016) 15:3 Page 9 of 22 3

short to long, straight or geniculate, with one or several sections Alternaria, Alternantherae, Euphorbiicola, and
conidiogenous pores. Conidia are solitary or in short Porri (Lawrence et al. 2013; Woudenberg et al. 2014).
chains. Juvenile conidia are subspheroid, ovoid to
subcylindrical (Fig. 2i). Mature conidia are obovoid, Section Infectoriae Woudenb. & Crous 2013
ellipsoid, narrowly ellipsoid, cylindrical, obclavate, or Type species: Alternaria infectoria E.G. Simmons
carrot-like. Apical cell is hemispherical to conical. Section Infectoriae currently consists of approximately 25
Conidia have several transverse and no or many longitu- species (e.g., A. ethzedia, A. graminicola, A. infectoria, and
dinal septa; transverse septa can be thick, dark and rigid A. metachromatica) with 11 taxa known to produce a sexual
in contrast to the external wall. Conidia may have con- morph previously known as Lewia. Primary conidiophores are
strictions near several central septa. Sometimes conidia simple or branched, short to long (20–150×3–4 μm) with (1)2–6
produce solitary apical or lateral secondary conidiophores apical conidiogenous loci. Conidia are obclavate, long-ellipsoid
that are usually not longer than the length of the body and sometimes subcylindrical, small (12–30×1–10 μm) to moderate
have one to a few conidiogenous loci. Conidium color is in size (30–60×6–15 μm) (Fig. 2j). Conidial body has (1)4–
yellowish or dilute brown to medium brown and oliva- 7(10) transverse and 1–2(3) longitudinal septa in 1–4 transverse
ceous brown. The outer wall is smooth; punctulate orna- sections with slight constriction near some transverse septa.
mentation is rarely visible. Chlamydospores are abundant Conidial chains are moderately long to long and branched due
on vegetative hyphae or absent. They are intercalary or to secondary sporulation and polytretic conidiogenous cells.
terminal, swollen, thick-walled. Ascomata, if present, are Apical secondary conidiophores are long (10–60 μm), genicu-
spheroid to ovoid, thin-walled, dark, apically papillate by late with multiple (2–3(8)) conidiogenous loci. Lateral secondary
the time asci begin to mature, conspicuously setose. Asci conidiophores are rare. Ascomata, if present, smooth walled, asci
are subcylindrical to subellipsoid, straight to somewhat subcylindrical or subellipsoid with 5(−7) transverse septa and 1–
inequilateral, bitunicate, usually 8-spored. Juvenile asco- 2 longitudinal septa in series in central segments, one or no
spores are subellipsoid and slightly inequilateral; mature longitudinal or oblique septum in terminal cells. Based on
ascospores are subclavate to ellipsoid, with transverse multi-locus analyses sect. Infectoriae is strongly supported as
septa, discontinuous series of longitudinal septa through the sister group to sect. Pseudoalternaria (Lawrence et al. 2014).
major central spore segments, and with or lacking a lon-
gitudinal septum in terminal cells. Molecular data support Section Japonicae Woudenb. & Crous 2013
the sister relationship with the morphologically similar Type species: Alternaria japonica Yoshii
sect. Embellisioides. Section Japonicae consists of two species (A. japonica and
A. nepalensis) isolated from the Brassicaceae. Primary conid-
Section Gypsophilae D.P. Lawr., Gannibal, Peever & iophores are short to long, simple or sometimes branched con-
B.M. Pryor 2013 taining a single conidiogenous locus. Conidia are short to
Type species: Alternaria gypsophilae Neerg. long-ovoid with transverse and longitudinal septa, constric-
Section Gypsophilae consists of eight species tions at most transverse septa, in short chains (Fig. 2k). An
(A. axiaeriisporifera, A. ellipsoidea, A. gypsophilae, apical conidiogenous locus may give rise to a secondary co-
A. juxtiseptata, A. nobilis, A. saponariae, A. vaccariae, nidiophore. The precise phylogenetic position of sect.
and A. vaccariicola) that have only been isolated from Japonicae within Alternaria is not certain; however, it clusters
plants in the Caryophyllaceae. Primary conidiophores more closely with taxa that were previously classified as
are short or long (up to 250 × 5–6 μm), simple or occa- Alternaria and Ulocladium than to other lineages (Lawrence
sionally branched, with one or a few conidiogenous et al. 2013; Woudenberg et al. 2013).
loci. Conidia are formed in simple chains or in
branching chains of 3–7 units. Conidia are ellipsoid or Section Nimbya (E.G. Simmons) Woudenb. & Crous
globose, broadly or narrowly ovoid with the basal co- 2013
nidium usually obclavate. Conidia are small or large Type species: Alternaria scirpicola (Fuckel) Sivan.
(40–70 to 125–176 × 15–30 μm) with many transverse The genus Nimbya was conceived by Simmons (1989)
(10–15(19)) and longitudinal septa, conspicuous con- to segregate the atypical species of Sporidesmium
striction at some transverse septa. Apex of conidium scirpicola Fuckel, a pathogen of river bulrush. The taxon-
may be rounded, cylindrical, conical, or produce a sec- omy of Sporidesmium Link 1809 has historically been
ondary conidiophore. Apical secondary conidiophores problematic as the type, S. scirpicola, has been previously
may be short or longer than conidial body with 1–2(4) classified as Clasterosporium scirpicola (Fuckel) Sacc.,
conidiogenous loci. Conidia may produce a single short Cercospora scirpicola (Fuckel) Zind.-Bakker, and
lateral secondary conidiophore with a single Alternaria scirpicola (Fuckel) Sivanesan (Fuckel 1863;
conidiogenous locus. Section Gypsophilae is sister to Saccardo 1886; Sivanesan 1984; van Zinderen 1940).
3 Page 10 of 22 Mycol Progress (2016) 15:3

Currently, section Nimbya consists of four species Primary conidiophores are relatively short or moderately
(A caricis, A. scirpicola, A. scirpinfestans, and long, usually simple, sometimes geniculate bearing one
A. scirpivora). Alternaria scirpicola typically produces or a few conidiogenous loci. Conidia are solitary or in
multi-celled apically tapering conidia that may be solitary short or moderately long chains usually simple or some-
or in short chains of 2–8 units. Conidia are distoseptate times with short branches (Fig. 2n). Juvenile conidia are
which become partially or fully euseptate at maturity and subspherical, ellipsoid, ovoid or cylindrical with rounded
possess multiple transverse septa (6–13) with conspicuous base and apex. Mature conidia are ellipsoid, ovoid or
constriction near some transverse septa, and extremely somewhat cylindrical, straight or curved, or limaciform,
rare longitudinal septa which are key characters that clear- septate, sometimes with solitary apical and seldom with
ly separate sect. Nimbya from other closely related sec- solitary lateral secondary conidiophores that usually are
tions of Alternaria (Fig. 2l). Section Nimbya conidia are not longer than the length of the body and have one to a
extended obclavate or subcylindrical, moderate in size few conidiogenous loci. Some transverse septa are dark-
30–130×6–22 μm with an extended cone-shaped apical ened and induce slight to conspicuous constriction. Some
beak (20–100 μm). Primary conidiophores are generally conidia remain with no longitudinal or oblique septa but
simple, 20–150 μm, with 1–4 conidiogenous loci with other part of conidia has 1–2(4) longisepta in some or
close geniculations. The sexual state has long been recog- many transverse segments. Some conidia produce an
nized as Macrospora Fuckel 1870 and is morphologically oblique septum in the basal segment. Conidium color is
similar but distinct as compared to the former teleomorphs yellowish or dilute brown to medium brown. The outer
Lewia (sect. Infectoriae), Allewia (sections Embellisioides wall is smooth. Chlamydospores are abundant or absent.
and Eureka) (Simmons 1986, 1990a; Vieira and Barreto They are intercalary or terminal, solitary, swollen, thick-
2005), and the teleomorph of Stemphylium spp., walled. One to all cells on conidia can also become
Pleospora (Crivelli 1983). Section Nimbya is most closely chlamydosporic (enlarged, swollen, thick-walled) making
related to sections Embellisia, Phragmosporae, Soda, conidia asymmetrical. Thus, each species is able to pro-
Chalastospora, Pseudoalternaria, and Infectoriae. duce swollen cells, on hyphae, on conidia or on both,
hyphae and conidia (at least some conidial cells become
Section Panax D.P. Lawr., Gannibal, Peever & B.M. rounded with relatively deep constriction). All strains of
Pryor 2013 all species in this section are known from soil, seawater,
Type species: Alternaria panacis (= A. panax) Whetzel or seawater plants and animals. Only one isolate,
Section Panax currently consists of seven species pri- A. didymospora, was collected from another substrate,
marily isolated from the Araliaceae (A. araliae, equine nasal mucosa. No species or strains were evident-
A. avenicola, A. calcipyricola, A. dendropanacis, ly associated with living land plants. Phylogenetic anal-
A. eryngii, A. panacis, and A. photistica) (Deng et al. yses suggest that sect. Phragmosporae is sister to sec-
2015). Primary conidiophores are short to moderately tions Soda, Chalastospora, Pseudoalternaria, and
long (100–200×6–8 μm) with one to a few conidiogenous Infectoriae (Lawrence et al. 2013).
loci. Conidia are arranged in short to moderately long
simple or branched chains. Conidia are obclavate, long Section Porri D.P. Lawr., Gannibal, Peever & B.M.
obclavate or ellipsoid to ovoid, medium-sized (65– Pryor 2013
80 μm) and conspicuously constricted near several trans- Type species: Alternaria porri (Ellis) Cif.
verse septa and have several or many longitudinal septa Section Porri consists of 63 species (e.g., A. dauci,
(Fig. 2m). Apex of conidium is rounded conical or cylin- A. macrospora, A. porri, and A. solani) (Woudenberg
drical and may produce a short or long secondary conid- et al. 2014). Primary conidiophores are short to rarely
iophore with one to several conidiogenous loci. Some long (up to 250 μm), simple or branched with one or a
conidia may produce one to several lateral secondary co- few conidiogenous loci. Conidia are generally solitary or
nidiophores with a single conidiogenous locus. in short to moderately long chains. Conidia are moderate-
Phylogenetic analyses suggest that sect. Panax is sister ly large (40–110×10–25(30)μm), broad ovoid ellipsoid,
to a monotypic lineage (A. thalictrigena) and sect. obclavate, subcylindrical or obovoid, disto- and euseptate
Teretispora (Woudenberg et al. 2013). with longitudinal septa and slight constriction near some
transverse septa (5–9 to 8–13). Most mature conidia pro-
Section Phragmosporae Woudenb. & Crous 2013 duce a long (80–300(400) μm) filamentous apical beak
Type species: Alternaria phragmospora Emden that is simple or branched and septate or aseptate
Section Phragmosporae consists of six species (Gannibal 2015) (Fig. 2o). The apical beak may develop
(A. chlamydospora, A. didymospora, A. limaciformis, into secondary conidiophores. Conidia may produce api-
A. molesta, A. mouchaccae, and A. phragmospora). cal or lateral secondary conidiophores with no filiform
Mycol Progress (2016) 15:3 Page 11 of 22 3

beak. Lateral secondary conidiophores may arise from the smooth, may produce a false beak (secondary conid-
beak or conidial body. Section Porri consistently clusters iophore).
sister to sections Euphorbiicola, Alternaria, and
Alternantherae (Woudenberg et al. 2014; Lawrence et al. Section Pseudoulocladium Woudenb. & Crous 2013
2013). Type species: Alternaria chartarum Preuss
Section Pseudoulocladium is comprised of four species
Section Pseudoalternaria D.P. Lawr., Rotondo & (A. aspera, A. chartarum, A. concatenata, and A. septospora)
Gannibal, sect. nov. MycoBank no. MB812913 that are characterized as producing simple or branched prima-
= Pseudoalternaria D.P. Lawr., Gannibal, F.M. Dugan & ry conidiophores with short, geniculate, sympodial prolifera-
B.M. Pryor, Mycological Progress 13:272. (2013) 2014, nom. tions with multiple conidiogenous loci. Conidia are predomi-
inval. nately ovoid or obovoid, non-beaked, in simple or branched
Type species: Alternaria arrhenatheri D.P. Lawr., Rotondo chains (Fig. 2q). Apical secondary conidiophores produce
& Gannibal, sp. nov. multiple conidiogenous loci while lateral secondary conidio-
= Pseudoalternaria arrhenatheri (as “arrhenatheria”) D.P. phores typically only form one conidiogenous locus.
Lawr., Gannibal, F.M. Dugan & B.M. Pryor, Mycological Phylogenetic analyses support the sister relationship with sect.
Progress 13:272. (2013) 2014, nom. inval. Ulocladioides.
Section Pseudoalternaria consists of two species
(A. arrhenatheri and A. rosae) that produce primary Section Radicina D.P. Lawr., Gannibal, Peever & B.M.
conidiophores that are simple or branched, Pryor 2013
multigeniculate, short to long (9–75(150+) μm) and Type species: Alternaria radicina Meier, Drechsler & E.D.
may produce several lateral branches. Secondary conid- Eddy
iophores short to long, simple to multiple geniculations Section Radicina consists of five species
and conidiogenous loci that may form apically or lat- (A. carotiincultae, A. petroselini, A. radicina, A. selini,
erally. Conidia are ovoid or elliptical, relatively small and A. smyrnii) isolated from the Apiaceae. Primary co-
(10–33 × 5–10 μm), catenulate, medium brown to gold- nidiophores are straight, simple or branched, short or
en brown with 3–5 transverse septa and at most one to long, with multiple geniculations, with 1–4 aggregated
two longitudinal septa in 1–2 transverse segments, conidiogenous loci at the apex. The sporulation pattern
smooth to conspicuously granulate (Fig. 2p). Sexual resembles clusters or clumps of conidia. Conidia are sol-
state is unknown. Section Pseudoalternaria is strongly itary or in short chains of 2–3. Conidia are wide ovoid or
supported as the sister group to sect. Infectoriae short ellipsoid, subcylindrical or rarely subspheroid,
(Lawrence et al. 2014). moderate in size (30–80(96)×15–38 μm), with several
Alternaria arrhenatheri D.P. Lawr., Rotondo & Gannibal, transverse septa (3–12) and a few longitudinal septa
sp. nov. MycoBank no. MB813314 (1–3) (Fig. 2r). The apical cell of the conidium is round-
Etym.: arrhenatheria (Latin) referring to host of isola- ed, hemispherical, or conical. Some conidia produce a
tion (Arrhenatherum elatius). Holotype specimen (LEP solitary short apical secondary conidiophore.
140372), dried WPDA culture of the strain 564692- Phylogenetic analyses suggest that sect. Radicina and
12FD, is kept in the Mycological herbarium of VIZR, sect. Gypsophilae share a close evolutionary relationship
Saint Petersburg, Russia. (Lawrence et al. 2013).
Colony diameter 63 mm in 7 days at 25 °C on
WPDA, tan to light brown, rapidly growing. Section Soda Bilanenko, Georgieva & A.A. Grum-
Sporulation aggregated appearing granular to the naked Grzhim. 2015
eye. Mycelium subhyaline to light brown, hyphae Type species: Alternaria kulundii Bilanenko, Georgieva &
smooth, branched, septate, 3.75–5 μm wide. Primary A.A. Grum-Grzhim.
conidiophores aggregated on agar surface or arising Section Soda consists of three species (A. kulundii,
from arachnoid vegetative aerial hyphae, simple or A. petuchovskii, and A. shukurtzii) isolated from highly
branched, medium brown, septate, smooth, 8.75– alkaline soda lake soils in Kulunda Steppe in Western
37.5 × 3.75–5 μm (M = 18.05 × 4.8 μm, n = 30), simple Siberia Russia. Primary conidiophores are branched,
with single apical pore. Secondary conidiophore short short to moderately long with a single conidiogenous
to long, simple to multiple geniculations with one to locus. Secondary conidiophores may be lateral or apical
several conidiogenous loci. Conidia 17.5–32.5 × 7.5– with a single conidiogenous locus, conidiogenous apex
10 μm (M = 20.8 × 8.55 μm, n = 50), mainly catenulate, may be enlarged. Conidia borne singly or in short to
ellipsoid to obclavate, medium brown to golden long chains that are simple or branched, narrowly ellip-
brown, 3–4 transverse septa, 1–2 longitudinal septa, soid to long-ovoid somewhat obclavate, moderate to
3 Page 12 of 22 Mycol Progress (2016) 15:3

large (60–120 × 7–30 μm) with many transverse conidiogenous loci. Conidia are obovoid or sub-spherical
(7–11(−18)) and no to several longitudinal septa with (14–40×7–21 μm) with no beak and transverse (1–7) and
conspicuous constrictions at some basal transverse septa. longitudinal (1–3) septa (Fig. 2u). Conidia arise in clusters
Chlamydospores and microsclerotia may develop in when conidiophore development is closely geniculate.
culture. The analysis by Grum-Grzhimaylo et al. (2015) Phylogenetic studies suggest that sect. Ulocladioides is sister
suggests that sect. Soda is sister to sections to sections Pseudoulocladium, Dianthicola, and Cheiranthus.
Chalastospora, Pseudoalternaria, and Infectoriae.
Section Ulocladium (Preuss) Woudenb. & Crous 2013
Section Sonchi D.P. Lawr., Gannibal, Peever & B.M. Type species: Alternaria botrytis (Preuss) Woudenb. &
Pryor 2013 Crous
Type species: Alternaria sonchi J.J. Davis The epitype of the former genus Ulocladium is Alternaria
Section Sonchi is comprised of two species (A. cinerariae botrytis CBS 197.67. Additionally, two former Ulocladium
and A. sonchi) from multiple hosts in the Asteraceae. Primary species, U. alternariae (originally isolated from Daucus
conidiophores are moderately long (less than 100 μm) to long carota) and U. oudemansii (unknown source), have consis-
(up to 250 μm), simple or branched, with 1–3 conidiogenous tently clustered outside of the core Ulocladium group (sect.
loci. Conidia are solitary or in short chains, subcylindrical, Ulocladioides) in previous phylogenetic studies (Hong et al.
broadly ovoid, broadly ellipsoid or obclavate, moderately 2005; Pryor and Bigelow 2003; Pryor and Gilbertson 2000;
large to large (70–150×15–30 μm), with 3–7 to 8–12 trans- Runa et al. 2009). Morphological examination of
verse septa which may be slightly or sufficiently constricted U. alternariae and two new isolates of Ulocladium-like taxa
and 1–3 longitudinal septa in (1–4(7)) transverse sections from China revealed divergent conidiophore and conidial
(Fig. 2s). The apex of the conidium is blunt and consists of a morphologies as compared to the core Ulocladium group
broadly tapering apical cell or short strong beak or secondary (sect. Ulocladioides) (Wang et al. 2011). The Chinese group
conidiophore. The secondary conidiophore is short one-celled detailed distinct morphological features (production of simple
or may be as long as or longer than the conidium body. The conidiophores with a single apical pore or one or two short,
analysis by Woudenberg et al. (2013) placed sect. Sonchi as uniperforate, geniculate sympodial proliferations) that sepa-
the sister group to two monotypic lineages, A. brassicae and rated U. alternariae and the two novel taxa from the core
A. helianthiinficiens, respectively. Ulocladium group (conidiophore geniculations often
multiperforate and closely to widely spaced) and erected the
Section Teretispora (E.G. Simmons) Woudenb. & Crous genus Sinomyces (Wang et al. 2011). Woudenberg et al.
2013 (2013) synonymized Sinomyces with Alternaria and placed
Type species: Alternaria leucanthemi Nelen these species in sect. Ulocladium. Section Ulocladium con-
This section is comprised of only one species, A. leucanthemi, sists of four species (A. alternariae, A. botrytis, A. capsici-
isolated from Leucanthemum maximum, Asteraceae (Gannibal annui, and A. oudemansii) and is characterized as producing
2012; Simmons 2007). Primary conidiophores are simple and simple or branched septate primary conidiophores that are
bear few conidiogenous loci (1–3). Cylindrical conidia (80– short to moderate (10–60×3–5 μm) with a single apical pore
130(160)×17–23(30) μm) are generally solitary, and character- occasionally with 1–2 uniperforate geniculations. Conidia are
ized by the presence of both transverse septa (7–14(17)), and obclavate to fusoid, obovoid to ellipsoid, or obovoid to broad-
longitudinal septa (3–7) (Fig. 2t). According to the phylogenetic ly ellipsoid with 2–6 transverse and 1–3 longitudinal septa,
study by Woudenberg et al. (2013) Teretispora clustered with and moderate in size (18–39×11–17 μm) (Fig. 2v). Section
Alternaria and Ulocladium species and was re-circumscribed as Ulocladium clusters sister to A. argyranthemi and A. thlaspis
a section within the genus Alternaria. (two monotypic lineages) that together are sister to sections
Crivellia, Undifilum, Nimbya, Embellisia, Soda,
Section Ulocladioides Woudenb. & Crous 2013 Chalastospora, Pseudoalternaria, and Infectoriae (Lawrence
Type specimen: Alternaria cucurbitae Letendre & Roum. et al. 2013).
Section Ulocladioides currently consists of ten species
(e.g., A. atra, A. cucurbitae, multiformis, and A. obovoidea) Section Undifilum (B.M. Pryor, Creamer, Shoemaker,
that were previously classified as Ulocladium species. Here, McLain-Romero & Hambl.) Woudenb. & Crous 2013
briefly summarized, are the characteristic morphological traits Type species: Alternaria bornmuelleri (Magnus) Woudenb.
observed by Simmons and Roberts (1993) and reassessed by & Crous
Gannibal (2012). Section Ulocladioides 3-dimensional spor- The genus Undifilum was erected to differentiate two spe-
ulation pattern is usually characterized by simple or branched cies, Embellisia oxytropis and Helminthosporium
conidiophores (5–200×3–5 μm). Secondary conidiophores, bornmuelleri (originally isolated from the Fabaceous plants
when present, are short and characterized by several Oxytropis kansuensis and Securigera varia, respectively), as
Mycol Progress (2016) 15:3 Page 13 of 22 3

morphologically and phylogenetically distinct from other defined in a phylogenetically supported framework. Clear
alternarioid hyphomycetes (Pryor et al. 2009). Section phylogenetic concordance between anamorph and teleomorph
Undifilum consists of four species (A. bornmuelleri, genera has been established and unites both classifications
A. cinerea, A. fulva, and A. oxytropis) that are extremely slow into one natural system based on the principle “one fungus –
growing on culture media, often requiring more than 30 days one name” (Taylor 2011). As we previously mentioned, phy-
to attain a colony diameter of 5 mm. Primary conidiophores of logenetic analyses have shown that the sexual morphs of the
A. bornmuelleri are produced in clustered groups, rarely sol- alternarioid hyphomycetes, and currently all asexual
itary, moderate in length and wider at the base (10)20–50× alternarioid hyphomycetes, should be placed in the
10–12 μm (basally) 6–8 μm (apically). Conidia are ovate to Pleosporaceae (Inderbitzin et al. 2006; Pryor and Bigelow
obclavate to long ellipsoidal to cylindrical, generally widest at 2003; Woudenberg et al. 2013; Zhang et al. 2012).
the second cell from the base, longer conidia are slightly Considerable molecular phylogenetic studies, together with
narrowed at the apex, broadly rounded at both ends, thin the connection between teleomorphic genera and alternarioid
walled, transverse segments divided by (2)3–4(5) dark brown hyphomycetes, have allowed the true placement of the latter
transverse septa, small to moderate in size (29)39–50(55)× within the modern systematics of fungi. Pleosporaceae is the
10–12(15)μm, catenate but in short chains (Fig. 2w). Upon largest family in the Pleosporales (Dothideomycetes,
conidial germination the germ tube is wavy and unbranched Ascomycota) and is comprised of 36 teleomorphic genera
for three to four spore lengths. Section Undifilum is more and approximately 770 species (Kirk et al. 2008).
closely related to sections Ulocladium, Crivellia, Nimbya, During the taxonomic history of Alternaria, several ascomy-
Embellisia, Soda, Chalastospora, Pseudoalternaria, and cetous genera were considered to be its sexual state. Those con-
Infectoriae than to other Alternaria sections based on a five- troversial taxonomies have caused several misidentifications.
gene combined dataset (Lawrence et al. 2013). The genera Clathrospora Rabenh. 1857, Comoclathris Clem.
1909, Leptosphaeria Ces. & De Not. 1863, and Pleospora were
Monotypic lineages described as having Alternaria asexual morphs (Domsch et al.
1980; Ellis 1971; Ellis and Ellis 1985; Simmons 1954;
Multi-locus phylogenetic analyses have identified eight spe- Whitehead and Dickson 1952; von Arx and Muller 1950) and
cies (listed below) that do not cluster with strong support among these Pleospora was often mentioned as the sexual state
among the 27 described sections of Alternaria, thus additional of Alternaria. Furthermore, the name Pleospora was ambigu-
sections may be described in future studies as more/new ously used when Dendryphion Wallr. 1833, Diplodia Fr. 1834,
Alternaria species/isolates are molecularly characterized. Phoma Fr. 1821, and Stemphylium-like asexual morphs were
Alternaria argyranthemi E.G. Simmons & C.F. Hill, described (Sivanesan 1984). Simmons (1986) established that
Mycotaxon 65:32. 1997. the name Pleospora should be used for the sexual state of
Alternaria brassicae (Berk.) Sacc., Michelia 2 (no.6): 129. Stemphylium. The genus Lewia was described to morphologi-
1880. cally group Alternaria-related teleomorphs. Later, the connec-
Alternaria dennisii M.B. Ellis, Mycol. Pap. 125: 27. 1971. tion with Lewia was repeatedly well-established (Kwaśna and
Alternaria helianthiinficiens E.G. Simmons, Walcz & R.G. Kosiak 2003; Simmons 1986, 2007). The type species of Lewia,
Roberts, Mycotaxon 25: 204. 1986. L. scrophulariae, previously was mentioned as belonging to the
Alternaria peucedani S.H. Yu, Mycobiology 42:1. 2014. genera Sphaeria Haller 1768, Leptosphaeria, and Pleospora. At
Alternaria soliardae E.G. Simmons, CBS Biodiversity Ser. least one Lewia species was identified by Whitehead and
(Utrecht) 6: 374. 2007. Dickson (1952) as a species of Pyrenophora Fr. 1849
Alternaria thalictrigena K. Schub. & Crous, Fungal Planet (Kwaśna and Kosiak 2003). For Ulocladium, Bonar (1928)
No. 12: 2. 2007. and Farr et al. (1989) mistakenly proposed its sexual state as
Alternaria thlaspis (E.G. Simmons & J.C. David) D.P. Lasiobotrys Kunze 1823 (Venturiaceae). However, molecular
Lawr., Rotondo & Gannibal comb. nov. MycoBank phylogenetic studies have clearly shown that these fungi belong
MB812914. in the Pleosporaceae (Inderbitzin et al. 2006; Pryor et al. 2009;
Basionym: Embellisia thlaspis E.G. Simmons & J.C. David, Pryor and Bigelow 2003; Runa et al. 2009; Wang et al. 2011).
Mycoscience 41: 533. 2000. Allewia, Crivellia, Lewia, and Macrospora were consid-
ered teleomorphs of some alternarioid hyphomycetes.
Simmons (1986, 1990b) elucidated that Lewia and Allewia
Asexual–sexual connections were the sexual morphs of Alternaria and Embellisia, respec-
tively. Macrospora was connected with the former anamor-
Taxonomic achievements and current nomenclature rules phic genus Nimbya (Simmons 1989). Similarly, the genus
have abolished the form phylum Deuteromycota. The place- Crivellia was shown to be the se xual m orp h of
ment of all mitosporic (imperfect) fungal “species” should be Brachycladium (Inderbitzin et al. 2006). Currently, one sect.
3 Page 14 of 22 Mycol Progress (2016) 15:3

Alternaria, ten sect. Infectoriae, two sect. Panax, one sect. Anamorph–teleomorph connections for several sections
Embellisioides, one sect. Eureka, four sect. Nimbya and one within the alternarioid hyphomycetes has clearly been demon-
sect. Crivellia sexual species have been described. However, strated by single conidium-to-ascospore and ascospore-to-
the names of the conidial state for Lewia chlamidosporiformans conidium studies. The distinct and robust morphological differ-
and L. sauropodis were not defined and the descriptions of ences among ascomata and ascospores of sections Crivellia,
conidia were not provided (Vieira and Barreto 2005; Zhang Embellisioides, Eureka, Infectoriae, and Nimbya support the
and David 1996). demarcation of these taxa as well-defined morphological sec-
The genus Pleospora and sections Alternaria, tions. Additionally, molecular phylogenetic data support the sep-
Embellisioides, Eureka, Infectoriae, and Nimbya share some aration of these taxa as discrete phylogenetic clades.
morphologically similar features but each also possesses dis-
tinct ascomata and ascospore characters. Section Infectoriae
species are characterized by small ascomata and ascospores, Taxonomic conclusions
when compared with those produced by Pleospora (Simmons
1986). The morphological characteristics described by The field of systematics consists of three broad areas, taxonomy
Simmons (1990b) for the former genus Allewia (sections which includes naming and cataloguing taxa, classification of
Embellisioides and Eureka) fall into ranges of variability of organisms in a hierarchical fashion from domain to the species-
sect. Infectoriae (Simmons 1986). The ability to form differ- level or lower, and evolutionary biology by which phylogenetic
ent conidial states was fundamental to distinguish these genera relationships among taxa are deduced. The name of a taxon or
(Simmons 1990b). However, ascostromata of both A. proteae group of taxa is perhaps one of the most important aspects of
(sect. Embellisioides) and A. eureka (sect. Eureka) are con- systematic biology because this is how information about an
spicuously setose, while those of sections Alternaria and organism or group of organisms is communicated and allows
Infectoriae are smooth. for predictions about the biology of said organisms. Scientific
Unfortunately, E.G. Simmons did not perform his own de- names of fungi may change over time as increased knowledge
scription of Macrospora (sect. Nimbya), which was originally is obtained regarding an organism’s biology which may include
described by Fuckel in 1870. However, Fuckel observed that morphological characters, host and geographical associations,
the type species, M. scirpicola, was characterized by larger and DNA-based phylogenetic position. As for many fungal
ascomata and ascospores, with asci broadly obovate-saccate groups, a polyphasic classification scheme, which includes
compared to the subcylindrical or subellipsoid asci produced the above-mentioned biological and molecular characters,
by sect. Infectoriae and sections Embellisioides and Eureka should be utilized when classifying fungal taxa in order to
(Simmons 1989). convey as much biological information as possible.
Section Crivellia differs from other sexual morphs of the The taxonomy and classification of alternarioid taxa have
alternarioid hyphomycetes by producing ascospores with few- been largely based on morphological characters of conidia and
er numbers of transverse septa. Mature sect. Infectoriae, sec- conidiophores and to a lesser extent on host associations
tions Embellisioides and Eureka, and sect. Nimbya ascospores (Simmons 1989, 2007; Zhao and Zhang 2005). DNA-based
have 5(−7) transverse septa (up to 9 in sections Embellisioides molecular phylogenetics have supported as well as over-
and Eureka) and 1–2 series of longitudinal septa through the turned some of these classification schemes (Alves et al.
central spore segments, terminal cells without septa, or with 2013; Inderbitzin et al. 2006; Lawrence et al. 2012, 2013,
one longitudinal or oblique septum. Mature sect. Crivellia 2014; Pryor et al. 2009; Runa et al. 2009; Wang et al. 2011;
ascospores only produce three transverse septa, with one lon- Woudenberg et al. 2013). Mycologists as well as other biolog-
gitudinal septum in either or both central cells, but not in ical scientists seek congruence between morphological char-
terminal cells. acters and molecular phylogenetic hypotheses that result in
Phylogenetic data (Lawrence et al. 2014) revealed that phylogenetic clades. The resolution of alternarioid hyphomy-
the types of section Infectoriae and several other sections cetes groups is largely supported by morphological characters
including Chalastospora, Embellisia, Phragmosporae, albeit that some conidial characters have been shown to over-
and Nimbya are closely related. However, two former lap to some degree between distantly and closely related
Lewia species, A. avenicola and A. photistica, have been groups.
placed in sect. Panax (Woudenberg et al. 2013). These For instance, some members of sect. Alternaria as
two groups of former Lewia species are characterized by circumscribed by Lawrence et al. (2013) share some sim-
similar conidial sizes and shapes, but A. avenicola and ilar conidial characters with some members of sect.
A. photistica connected with sect. Panax are able to pro- Infectoriae even though they are distantly related
duce ascomata under pure culture conditions, while only (Lawrence et al. 2013, 2014). Significant biological dif-
protoascomata with no mature ascospores were found in ferences exist between the two groups such as the pro-
cultures of sect. Infectoriae (Andersen et al. 2009). duction of biological compounds including mycotoxins
Mycol Progress (2016) 15:3 Page 15 of 22 3

and other secondary metabolites that are not produced on epidemics. Most of Rotem’s conclusions are contemporary
reciprocally (Andersen et al. 2002; Andersen and and generally accepted.
Thrane 1996; Christensen et al. 2005), the presence of Alternaria species demonstrate a variety of ecological char-
mating-type genes where members of sect. Alternaria acteristics and forms of interactions with hosts, including plant
are heterothallic (Arie et al. 2000; Berbee et al. 2003) parasites, saprobes and endophytes. Some cause serious eco-
and members of sect. Infectoriae are presumed to be ho- nomically important crop diseases. Occasionally, Alternaria
mothallic based on ascospore-to-conidium and conidium- spp. are detected as endophytes or human and animal patho-
to-ascoma studies of some known sexual taxa in this gens. The diversity of plant and human mycoses induced by
section (Simmons 1989, 2007). Alternaria and possible pathogenicity factors were briefly
Some authors have suggested collapsing certain genera reviewed by Lawrence et al. (2008). The interesting and ob-
based on morphological characters, namely Alternaria and scure contemporary question is an origin of such diversity, i.e.,
Ulocladium sensu lato (sections Ulocladioides and evolution of parasitic features in alternarioid hyphomycetes.
Pseudoulocladium) as a single genus, Alternaria (Joly Pathogenicity in alternarioid hyphomycetes correlates with
1964). Pryor and Gilbertson (2000) also suggested that species their phylogeny. Several large groups contain predominantly
of Ulocladium should be synonymized with Alternaria, based plant pathogens or saprobes. Several relatively small
on molecular phylogenetics of three individual loci. However, Alternaria sections (e.g., sect. Nimbya) consist mainly of path-
extended phylogenetic analyses have revealed that sections ogens restricted to plants in one or two families. The pathoge-
Ulocladioides and Pseudoulocladium are well-supported sec- nicity and specialization of several groups were poorly studied
tions distinct from other Alternaria lineages (Lawrence et al. or were not studied at all (e.g., sections Chalastospora and
2013; Runa et al. 2009; Woudenberg et al. 2013). Even though Embellisia). Here, we present a brief description of four eco-
some morphological overlap exists between them (i.e., logical groups of the alternarioid hyphomycetes characterized
A. septospora and A. chartarum conidia are predominately by different substrate association and pathogenicity.
ovoid, a character associated with sect. Alternaria). Runa
et al. (2009) hypothesized that this incongruence may be the Plant pathogens Alternaria sect. Porri (large-spored species)
result of a loss of the fundamental obovoid shape of sect. is the largest group of phytopathogens, with approximately 63
Pseudoulocladium conidia or that these taxa (A. septospora species, that infect numerous plants from different families.
and A. chartarum) preceded the development of the diagnostic The greatest diversity of large-spored species has been found
obovoid conidium shape as evidenced by the strongly sup- on the Asteraceae, while a smaller number of species have
ported bifurcation of the A. septospora and A. chartarum been described on the Solanaceae and other plant families
clade and the core obovoid sect. Ulocladioides. (Simmons 2007). Usually, one phytopathogenic fungal spe-
The efforts of Lawrence et al. (2013) and Woudenberg cies is associated with one host-plant species or a small group
et al. (2013) have greatly improved the taxonomic nomen- of taxa in a single genus. Phylogenetic analyses suggest that
clature of the alternarioid hyphomycetes by increasing the these specific host-pathogen associations within different
taxonomic resolution of an important and pleomorphic plant families have occurred multiple times throughout the
group of fungi. The improved taxonomy will allow both evolution of this clade.
specialists and non-specialists to easily identify taxa that A number of small Alternaria sections contain patho-
reside in this large and hyperdiverse group of fungi that genic species associated with one restricted group of
are perhaps the most commonly encountered fungi by plants. Both species in sect. Crivellia are pathogens of
mycologists and plant pathologists. Undoubtedly, future poppy. Four species in sect. Nimbya have a connection
studies will identify and describe additional taxa and sec- with only the Cyperaceae. Similarly, all three species in
tions as novel alternarioid hyphomycetes are discovered sect. Alternantherae are associated with Amaranthaceae,
from natural and man-made environments. eight species from sect. Gypsophilae were found only on
Caryophyllaceae, five species from sect. Radicina are
pathogens of Apiaceae, and both species from sect.
Sonchi are pathogens of Asteraceae. Here, we consider
Ecology and life cycle of Alternaria only species for which the phylogenetic position has been
elucidated. It is likely that, when the intrageneric position
Ecological features of Alternaria species have been reviewed of all Alternaria species is delimited, and as additional
several times (Kwaśna 1992; Scheffer 1992; Thomma 2003). species and sections are defined, the fungal section–plant
The most scrupulous review was performed by Rotem (1994), family connection will likely degenerate. An example of a
who predominately concentrated on all available information small section with no strong plant family association is
on overseasoning, effect of temperature and wetting on spor- sect. Brassicicola. Alternaria brassicicola, the common
ulation and infection processes, and on the effect of weather noxious pathogen of Brassicaceae, is nested in one section
3 Page 16 of 22 Mycol Progress (2016) 15:3

with four rare species found on plants of the Resedaceae and A. oxytropis, produce the toxic compound swaisonine
and Solanaceae, in soil or on latex drying on wounded (Baucom et al. 2012), which causes a neurological disease,
trunks of Hevea sp. locism, of grazing animals, resulting in economic losses in
livestock (James 1989). Probably, sect. Undifilum species as
Saprobes The most common saprobes among the alternarioid compared to other Alternaria species have some specific ad-
hyphomycetes are within sections Alternaria, Infectoriae, and aptations characteristic for “true” endophytes.
Ulocladioides, totaling more than 120 species. Many of these
alternarioid hyphomycetes can be recovered from predomi- Human pathogens Several Alternaria species mainly attrib-
nantly lifeless substrates of plant origin including dead plants, uted to A. alternata or A. infectoria and a number of
paper, and food (Rotem 1994). However, they can also be uncharacterized Alternaria isolates have been associated with
isolated from living plants, usually from senescent or dam- infections of the cornea, oral and sinus cavities, respiratory
aged tissues, and cause important yield losses. Very often, tract, skin, and nails (Arrese et al. 1996; Barbasso et al.
saprobic as well as pathogenic species inhabit seeds, especial- 2005; Barnes et al. 2007; Cascio et al. 2004; Dubois et al.
ly seeds formed in dry fruits with no thick pulpy pericarp, e.g., 2005; Mirkin 1994; Neumeister et al. 1994; Romano et al.
seeds of Poaceae, Brassicaceae, Apiaceae, etc. Frequently, 2001). Alternaria species have importance as emerging hu-
species within sect. Alternaria are isolated from plant organs man invasive pathogens in immuno-compromised patients
primarily infected by other phytopathogens. Usually, such (Morrison and Weisdorf 1993; Vartivarian et al. 1993). The
species are described in the literature as A. alternata or species Alternaria molesta was described from a skin lesion of
A. tenuissima. However, artificial inoculations with small- a porpoise, Phocaena phocaena (Simmons 2007). Species
spored Alternaria species are rarely successful in completing residing in sect. Ulocladioides have also been recorded as
Koch’s postulates. Yet, a number of cases supporting agents of keratitis (Badenoch et al. 2006).
A. alternata and A. tenuissima pathogenicity on several plants
have been reported: cucumber, pistachio, hazelnut, noni, blue- Life cycle The life cycle of Alternaria consists of only an
berry, apple, amaranth, and some weeds (Blodgett and Swart asexual haploid phase or both sexual and asexual phases
2002; Harteveld et al. 2013; Hong et al. 2006; Hubballi et al. (haplo–diploid cycle). Generally, the asexual haploid phase
2011; Karunakara Murthy et al. 2003; Pryor and Michailides with conidial reproduction is dominant. An overwhelming
2002; Rotondo et al. 2012; Vakalounakis 1990; Milholland majority of alternarioid hyphomycetes have presumably lost
1973). There are a few exceptional cases, when A. alternata- the ability to reproduce sexually. Nevertheless, many
like strains are narrowly specialized strong pathogens and alternarioid hyphomycete lineages have retained genetic de-
produce host-specific toxins due to possessing clusters of con- terminants of the heterothallic mating system—two indepen-
ditionally dispensable genes located on supernumerary chro- dent idiomorphs (~alleles) of MAT1 locus. Homothallic spe-
mosomes. These cases are described in a subsequent section. cies contain both idiomorphs in a single genome.
Ascomata production in pure culture under laboratory con-
Endophytes There are some cases where Alternaria species ditions has been documented in seven species: two sect.
have been isolated from asymptomatic plant tissues. Several Nimbya species (A. scirpinfestans and A. scirpivora), one sect.
studies have demonstrated the ability of Alternaria species to Embellioides species (A. proteae) and one sect. Eureka species
live endophytically without inducing pathogenesis inside (A. eureka), two sect. Panax species (A. avenicola and
leaves of tomato, wheat, maple, tropical epiphytic orchid, am- A. photistica) and one species in sect. Infectoriae
aranth, and some other plants (Blodgett et al. 2000; Chen et al. A. hordeicola (Johnson et al. 2002; Kwaśna and Kosiak
2011; Larran et al. 2001, 2007; Ma et al. 2010; Qi et al. 2009). 2003; Kwaśna et al. 2006; Simmons 1990a, 2007).
A study investigating the pathogenicity of A. infectoria-like Alternaria calycipyricola, sect. Panax, can produce
strains isolated from apple leaves also indicated a true endo- protoascomata on agar media (Roberts 2007).
phytic lifestyle for some specimens (Serdani et al. 2002). Only All species with a known sexual state (excluding the
normally saprobic species were revealed as endophytes. Since recently described sexual state of A. alternata) are pre-
this result was found by several studies in different plants, it sumably homothallic. This is supported by observations
cannot be attributed to methodological mistakes. Further in- of cultures (Andersen et al. 2009; Johnson et al. 2002)
vestigations are necessary to better understand the type of or by PCR assays of mating-type genes (Gannibal and
interactions between plant and fungus in this system. Is the Kazartsev 2013; Gasich et al. 2013; Inderbitzin et al.
endophytic phase just a sluggish latent period for disease in- 2006). Two species, A. alternata (sect. Alternaria) and
duced by a weak pathogen, and/or is pathogenesis initiated A. penicillata (sect. Crivellia), have preserved the
due to the health state of the host? heterothallic mating system for sexual reproduction.
Three endophytic species within sect. Undifilum, from the Interestingly, another species from the same lineage
Fabaceae (Astragalus and Oxytropis), A. cinereum, A. fulva, (sect. Crivellia), A. papavericola, has been shown to be
Mycol Progress (2016) 15:3 Page 17 of 22 3

homothallic (Inderbitzin et al. 2006). In sect. Panax a The genus Alternaria represents a good model to investigate
heterothallic species without an identified sexual state as and characterize the distribution of these compounds
well as homothallic species producing ascomata has been (Logrieco et al. 1990, 2003; Lou et al. 2013; Ostry 2008;
found (Gannibal, unpublished). Scott 2001; Thomma 2003). In recent years, several studies
The ratio of recombination and clonality is a genetic basis have been carried out to evaluate Alternaria mycotoxin prev-
for adaptation of fungi to environmental pressures. This ratio alence and their potential dangers concerning human con-
depends on the ecological niche and ecological strategy of the sumption in food and foodstuffs (Fernández-Cruz et al.
organism. Homogenous conditions in agroecosystems (e.g., 2010; Kocher 2007; Lau et al. 2003; Ostry et al. 2004; Scott
monoculture crops) seem to promote a decrease in the role et al. 2006; Scott 2001; Solfrizzo et al. 2004, 2005).
of sexual recombination in parasitic host-specialized fungi Beyond noting that Alternaria species can produce myco-
(Taylor et al. 1999). At the same time saprobic species live toxins and their effects on humans, the Alternaria toxin litera-
in more mutable conditions and continually adapt to environ- ture lays critical groundwork in understanding the ecological
mental changes spurred primarily via sexual recombination. and evolutionary implications of fungal toxins. Of particular
In alternarioid hyphomycetes, almost all species with interest are those studies elucidating the role and characteristics
a known sexual state are homothallic. On the contrary, of HSTs (Markham and Hille 2001; Nishimura and Kohmoto
all heterothallic species have no sexual reproduction 1983; Otani et al. 1995; Wolpert et al. 2002) and non-HSTs
with only two exceptions as mentioned above. Thus, it (Fujiwara et al. 1988; Meronuck et al. 1972; Robeson and
can be proposed that the evolution of alternarioid hy- Strobel 1981; Thuleau et al. 1988) w ith plants.
phomycetes reduced recombination and this may have Chemotaxonomic studies, based on secondary metabolites pro-
occurred in two possible ways: (1) conversion from het- files, have been successfully utilized to discriminate species
erothallism to homothallism i.e., replacement of out- within the genus Alternaria (Andersen et al. 1995, 2001,
breeding with inbreeding, and (2) total lack of the abil- 2002, 2005; Andersen and Thrane 1996; Christensen et al.
ity to begin or complete the sexual cycle. In the latter 2005; Frisvad et al. 2008; Serdani et al. 2002). Many non-
case, the genetic system of determination of mating was HSTs have been identified, but only a few of the modes of
preserved but does not function properly. The fusion of action have been elucidated, and they are not directly involved
MAT1-loci leading to homothallism seems to be an ir- in the infection process (Lawrence et al. 2008; Thomma 2003).
reversible process. Homothallic species have been found Instead, HSTs are a determinant for the development of a
in several distant lineages. Therefore, we hypothesize few destructive diseases, and they generally display severe
that homothallism has evolved several times indepen- effects on a rather narrow host species range (Howlett 2006;
dently within the alternarioid hyphomycetes. Several Kohmoto and Otani 1991; Markham and Hille 2001;
groups of homothallic species with a sexual state have Nishimura and Kohmoto 1983; Otani et al. 1995; Scheffer
heterothallic ancestors without a known sexual state. To and Livingston 1984; Walton and Panaccione 1993; Wolpert
our knowledge, no examples of sexual species deriving et al. 2002). Toxins that are produced by these pathotypes are
from asexual fungi have been documented except for chemically diverse, ranging from low molecular weight sec-
A. alternata. In fact, the most common plant pathogenic ondary metabolites to peptides. Tsuge et al. (2013) presented a
Alternaria species (sect. Porri) have no known sexual detailed review of the HST-producers belonging to
state, but there are also many saprobic species lacking A. alternata sensu lato. That work covers all the aspects in-
the sexual state (e.g., sect. Brassicicola). Do they all volved in the different HST pathosystems, describing chemi-
have clonal population structure? Truly, it seems to be cal structures, role in pathogenesis, mode of action, and their
clonal in some species, but it has been revealed that molecular genetics. In the present review, we summarize the
A. brassicicola and A. alternata have a means for gen- main steps of the HSTs characterization and how this has been
erating and maintaining significant genotypic variation utilized to investigate evolutionary processes and phylogenet-
providing ecologic plasticity (Bock et al. 2002; Bock ic relationships among Alternaria HST-producers.
et al. 2005; Stewart et al. 2013). Is it parasexual recom- The comparison between pathogenic and non-pathogenic
bination or by another cryptic means? This is still not A. alternata species has demonstrated that pathogenicity is
clearly understood. strictly related to the presence of small supernumerary chro-
mosomes, termed conditionally dispensable chromosomes
(CDCs) (Ajiro et al. 2010; Akagi et al. 2009; Akamatsu
Alternaria toxins et al. 1997, 1999; Hatta et al. 2002; Ito et al. 2004; Johnson
et al. 2000; Masunaka et al. 2005; Miyamoto et al. 2009,
Traditionally, fungal toxins are classified on the basis of their 2010; Tanaka et al. 1999). Gene clusters responsible for the
host specificity, and assigned to two main classes: non-host- synthesis of HSTs have been identified for the pathogenic
specific toxins (non-HSTs) and host-specific toxins (HSTs). variants of A. alternata and are less than 2 Mb in size.
3 Page 18 of 22 Mycol Progress (2016) 15:3

Moreover, it has been demonstrated that four of the seven especially when morphological overlap exists (Travadon et al.
A. alternata pathotypes (Japanese pear, apple, strawberry 2015; Lawrence et al. 2015). Simmons advocated using type
and tangerine), multiple copies of the toxin biosynthetic genes and representative strains for accurate morphological species
are necessary to initiate pathogenesis (Barnes et al. 2007; identification. Many of Simmons’ morphological species have
Harimoto et al. 2007; Hatta et al. 2002; Ito et al. 2004; been corroborated using molecular data as unique and/or
Johnson et al. 2001; Masunaka et al. 2000, 2005; Ruswandi emerging species while others have been rejected
et al. 2005; Tanaka et al. 1999; Tanaka and Tsuge 2000) (Woudenberg et al. 2014). To date, multiple locus sequencing
similar to pathosystems in other plant pathogenic is required to clearly delimit species within several Alternaria
Dothideomycete fungi such as Cochliobolus carbonum, HC- sections (e.g., sections Alternaria, Brassicicola, and
toxin producer (Ahn and Walton 1996), and Pyrenophora Ulocladioides). The use of the universal barcode (ITS) is not
tritici-repentis, a PtrToxB producer (Lamari et al. 2003). informative for many Alternaria species, therefore we recom-
The AAL toxin biosynthetic genes clustered on CDCs mend the use of more phylogenetically informative loci, plas-
have also proven to be useful in elucidating the evolution ma membrane ATPase and calmodulin (Lawrence et al. 2013),
and differentiation of pathogenesis of A. alternata tomato and comparison of type or representative isolates for accurate
pathotype strains (Akagi et al. 2009). CDCs have been species identification within Alternaria. By employing these
used to demonstrate that horizontal gene transfer (HGT) strategies, the systematics of Alternaria will be greatly im-
occurs in fungal species, both inter- and intra-kingdom proved by limiting the inadvertent addition of erroneous no-
transfers have been documented (Akagi et al. 2009; menclatural data with sequence data in GenBank by providing
Friesen et al. 2006; Hu et al. 2012; Milani et al. 2012; accurate and clearly annotated specimen data for all.
Richards et al. 2006; Rosewich and Kistler 2000; Schmitt
and Lumbsch 2009; Syvanen 1985). Hu et al. (2012), Acknowledgments This work was supported in part by the Russian
Science Foundation (grant # 14-26-00067). We thank Barry M. Pryor
utilizing next generation sequencing of the Alternaria
for supplying images for Fig. 2.
arborescens genome, were able to provide evidence of
HGT and hypothesized a model of how the transfer may
have occured. They demonstrated HGT utilizing phyloge-
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