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A mycorrhizal revolution
Grace A Hoysted1, Jill Kowal2, Alison Jacob3,
William R Rimington2,3,4, Jeffrey G Duckett2,
Silvia Pressel2, Suzanne Orchard5, Megan H Ryan5,
Katie J Field1 and Martin I Bidartondo3,4

It has long been postulated that symbiotic fungi facilitated plant Ascomycota and Basidiomycota (Figure 1 [1,2]); these
migrations onto land through enhancing the scavenging of mutually beneficial partnerships are thought to have
mineral nutrients and exchanging these for photosynthetically played a key role in plant terrestrialisation and diversifi-
fixed organic carbon. Today, land plant–fungal symbioses are cation [3,4]. Such associations are termed ‘mycorrhizas’
both widespread and diverse. Recent discoveries show that a (fungus-roots) in vascular plants, or ‘mycorrhiza-like’ in
variety of potential fungal associates were likely available to the rootless non-vascular plants with intracellular fungal
earliest land plants, and that these early partnerships were structures such as coils and/or arbuscules that are similar
probably affected by changing atmospheric CO2 to those formed in rooted species [5]. In exchange for up
concentrations. Here, we evaluate current hypotheses and to 20% of photosynthetically-fixed, organic carbon-based
knowledge gaps regarding early plant–fungal partnerships in compounds (C) [6,7], mycorrhizal fungi may provide their
the context of newly discovered fungal mutualists of early and plant partners with up to 80% of the nitrogen (N) and
more recently evolved land plants and the rapidly changing 100% of the phosphorus (P) required for plant growth and
views on the roles of plant–fungal symbioses in the evolution proliferation [8–12].
and ecology of the terrestrial biosphere.
The first plants to colonise Earth’s land surfaces in
Addresses the Ordovician period (475 Ma) were thought to
1
Centre for Plant Sciences, Faculty of Biological Sciences, University of
Leeds, Leeds LS2 9JT, UK
have formed associations with arbuscular mycorrhizal
2
Department of Life Sciences, National History Museum, London SW7 Glomeromycotina fungi thereby gaining access to fun-
5BD, UK gal-acquired mineral nutrients in return for plant carbo-
3
Comparative Plant & Fungal Biology, Royal Botanic Gardens, Kew, hydrates [13] and/or lipids [14,15] in a manner similar to
Richmond TW9 3DS, UK
4 modern arbuscular mycorrhizal associations [7]. Thus, the
Department of Life Sciences, Imperial College London, London SW7
2AZ, UK first fungal symbionts may well have co-evolved with, and
5
UWA School of Agriculture and Environment, and Institute of facilitated the transition of, rootless plants from water
Agriculture, The University of Western Australia, 35 Stirling Hwy, Crawley onto land [16,17] and subsequent terrestrial diversifica-
(Perth), WA 6009, Australia tion [3,4]. This hypothesis has been strongly supported by
Corresponding author: Hoysted, Grace A ([email protected])
cytological [18], molecular [19,20] and physiological evi-
dence [4] alongside fossilised examples of early plants
containing fungal structures bearing strong morphological
Current Opinion in Plant Biology 2018, 44:1–6 similarity to modern mycorrhizas [21]. However, recent
This review comes from a themed issue on Biotic interactions findings are now challenging the long-standing assump-
Edited by Sebastian Schornack and Caroline Gutjahr tion that the symbionts of early land plants were solely
Glomeromycotina fungi; instead they suggest that Mucor-
For a complete overview see the Issue and the Editorial
omycotina fungi have also played a major role [2,22].
Available online 29th December 2017
https://doi.org/10.1016/j.pbi.2017.12.004 Despite advances in our knowledge of non-vascular plant-
1369-5266/ã 2017 The Authors. Published by Elsevier Ltd. This is an –fungal partnerships in liverworts and hornworts, there
open access article under the CC BY-NC-ND license (http://creative- remains a significant gap regarding the occurrence, fre-
commons.org/licenses/by-nc-nd/4.0/).
quency, identity, appearance and function of Mucoromy-
cotina associations in later-derived vascular plant
lineages, including modern angiosperms, that have been
of key significance in the development of Earth’s terres-
Introduction trial atmosphere and biota to the present day. More
Amongst the most important symbioses in nature after recently, an ascomycete fungus facilitating the growth
mitochondria and plastids are those between plants and of a non-mycorrhizal flowering plant under P-limited
soil-dwelling filamentous fungi. The vast majority of conditions was reported [23]; the study uncovers a previ-
extant land plants, including most crops, form intimate ously unappreciated role of root fungal microbiota in
symbioses with fungi in the phyla Mucoromycota, nutrient cycling and highlights the diversity in plant–

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2 Biotic interactions

Figure 1

Current Opinion in Plant Biology

The mycorrhizal status of the main land plant groups in relation to fungal phylogenetic diversity. Dashed lines indicate currently unresolved
phylogenetic positions and asterisks signify uncertain mycorrhizal status with only one report of mycorrhizal formation in each case [57,38].

fungal nutritional interactions. Here we provide an over- root-covering mantle and intercellular penetration where
view of the recent leaps in understanding of the interac- hyphae form a network between cortical cells known as a
tions between early land plants and symbiotic fungi in both Hartig net [7,30]. The remarkable versatility of these
the Glomeromycotina and Mucoromycotina [2,24], with ancient and diverse fungi may be attributed to life history
emphasis on the role, evolution and distribution of Mucor- traits of the Endogonales, for example, facultative sapro-
omycotina symbionts across the land plant tree of life. trophy. However, more traits remain to be uncovered to
understand further the evolutionary and ecological sig-
Changing views on non-vascular plant nificance of these fungi.
symbioses with fungi
The symbioses between non-vascular plants and Mucor- The potential significance of Mucoromycotina fungi
omycotina fungi have, in the last few years, received in land plant evolution was first recognised when Endo-
increasing attention. Unlike the strictly biotrophic and, gone-like fungi were found to associate with the likely
to our current knowledge, asexual Glomeromycotina, e.g. earliest-diverging extant land plant lineage, Haplomi-
the model mycorrhizal fungus Rhizophagus irregularis, triopsida liverworts ([26] Figure 1). This discovery gen-
Mucoromycotina encompasses saprotrophic, biotrophic, erated the alternative hypothesis that a relict association
and putatively sexual lineages of fungi, including only with Mucoromycotina, apparently lost through land
poorly studied genera like Endogone and Sphaerocreas [25]. plant evolution, might have played a significant part in
Until recently, the biology of the Endogonales was largely ancestral mycorrhizal-like symbioses [26,31]. This
unknown [26,27]. In addition to endomycorrhizal asso- hypothesis was further supported by fossil evidence fol-
ciations, some members of Endogone can form ectomycor- lowing re-examination of the Early Devonian Rhynie
rhizal associations with trees [28,29], characterised by a Chert plant Horneophyton lignieri [32]. In addition to

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 A mycorrhizal revolution Hoysted et al. 3

Glomeromycotina-like fungal structures in the aerial axes taxonomically and functionally diverse, but also poten-
of H. lignieri, structures indicative of Mucoromycotina tially transient in nature, with plant and fungal partners
colonisation also appeared to be present within the plant’s shifting according to environmental conditions [2].
distinctive corm [32]. These fungal structures also
showed similarities to symbiotic features in fossilised Hornworts are an ancient plant phylum (300–400 Mya)
Glomites rhyniensis colonising Nothia aphylla [33]. These that in some phylogenies are the sister group of the
findings place Mucoromycotina as potential key players in earliest vascular plants [37–39]. Molecular evidence of
the initial colonisation of Earth’s landmasses [32]. How- fungi in hornworts was limited [26] until the extensive
ever, structure does not always translate into function, study by Desirò et al. [31] revealed that these plants also
particularly in fossils. A new cytological study showing have various symbiotic options. Hornworts were shown to
intracellular colonisation of non-vascular plants with the form both single and dual associations with Glomeromy-
broad-host range oomycete Phytophthora palmivora [34] cotina and/or Mucoromycotina, or to ‘opt out’ of symbio-
suggests that branched haustoria-like structures and pro- ses altogether, suggesting the same may be true for other
lific intracellular hyphal growth could be interpreted as early-diverging plant lineages such as the liverworts and
mycorrhizal-like if fossilised. Nonetheless, it is clear that indeed, the first land colonists [26,31,40]. However,
fungal associations in early land plants were much more functional studies testing for nutritional mutualism
varied than previously assumed and likely included between fungi and hornworts have yet to be performed.
diverse mutualists and pathogens. Recent works show
that in addition to the Halomitriopsida liverworts, many Changing views on vascular plant symbioses
extant non-vascular plants such as complex and simple with fungi
thalloid liverworts [35], hornworts [31], and early- Research into early diverging vascular plant-Mucoromy-
diverging vascular plants [27], harbour both Mucoromy- cotina symbiosis is in its infancy. Fungi have long been
cotina and Glomeromycotina, sometimes simultaneously recognised to be present within lycopods [41,42], how-
in the same host plant. ever, until recently their identity had been unclear
[32,40,43]. Molecular analyses have now shown that
The earliest divergent lineage of liverworts, the Haplo- Mucoromycotina associations, both single and in combi-
mitriopsida, form apparently exclusive partnerships with nation with Glomeromycotina, occur in this earliest
Endogonales [26]. The first study on the cytology and diverging clade of extant vascular plants [27], but, as
functioning of liverworts with Mucoromycotina demon- with hornworts, there is still no functional evidence of
strated a nutritional mutualism between partners, with mutualism in lycopod-fungal symbioses. In ferns, the
plant-fixed carbon detected in the fungus and fungus- most diverse early-diverging vascular plants, molecular,
acquired nutrients (15N and 33P) in the plant [22]. These microscopical and physiological data have documented
findings clearly demonstrate that the nutritional role arbuscular mycorrhizas [1,4,44]. Recent analysis of fern-
played by Mucoromycotina in Haplomitriopsida is analo- fungal symbioses showed that although many ferns asso-
gous to that of Glomeromycotina in complex thalloid ciate with Glomeromycotina, at least one — Anogramma
liverworts [18]. Additional experiments tested the car- leptophylla — can be colonised by Mucoromycotina and
bon-for-nutrient exchange responses of liverwort-fungal Glomeromycotina [27]. So far, there is evidence of
associations against a simulated Palaeozoic decline in mutualistic nutrient exchange with Glomeromycotina
atmospheric CO2 concentration, representative of the for only two ferns, Ophioglossum and Osmunda [4,45].
conditions experienced by early land plants [36]. In
liverwort-Mucoromycotina symbioses, the amount of The presence of Mucoromycotina in some early diverging
33
P gained from the fungus by the plant, per unit of vascular plants supports the idea that plants across the
carbon delivered by the plant to the fungus, was either evolutionary tree are much more symbiotically versatile
unaffected or even increased in response to declining than hitherto assumed. However, with few exceptions,
CO2, similarly to vascular plant-Glomeromycotina sym- occurrence and knowledge of fungal associations across
bioses [4], but in direct contrast to observations in liver- pteridophytes is based solely on light microscopy [44], a
wort-Glomeromycotina associations [4]. Differences in technique which may overlook Mucoromycotina co-col-
CO2 responsiveness between Mucoromycotina-plant onisation [26]. Cytological, molecular and physiological
and Glomeromycotina-plant symbioses, and between approaches are urgently needed to further understand the
vascular-plant and non-vascular plant symbioses, likely nature and functioning of these fungal partnerships in
provided physiological niches ensuring the persistence of lycopods and ferns.
both symbioses to the present [2]. The subsequent
discovery that some early diverging thalloid liverworts Fine root endophytes
form simultaneous (dual) symbioses with nutritionally Fungi known as fine root endophytes (Glomus tenue)
mutualistic Glomeromycotina and Mucoromycotina colonise bryophytes and ferns [46–49] as well as the roots
[26] lent weight to this view, with the intriguing possi- of vascular plants [50]. Whilst their colonisation mor-
bility that early plant–fungal symbioses were not only phology is distinctive from that of the arbuscular

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4 Biotic interactions

Figure 2 Box 1 Outstanding questions

 How widespread are Glomeromycotina and Mucoromycotina in

plant fossils?
 How is the colonisation and function of Mucoromycotina-plant
symbioses controlled — by genetics, environment, or both?
 To what extent do fine root endophytes (FRE), other Mucoromy-
cotina associations and Glomeromycotina associations overlap in
nature?
 Why are FRE rarely observed without the presence of arbuscular
mycorrhizal Glomeromycotina?
 Are Mucoromycotina associations with hornworts, lycopods, ferns
and angiosperms mutualistic, both when present alone and when
in dual symbiosis with Glomeromycotina?
 Do arbuscular mycorrhizal signals and colonisation pathways
overlap with Mucoromycotina symbioses?

Developing methods to target and study fine root endo-

phytes in a comparative context is imperative.

Future directions
Current Opinion in Plant Biology
The presence of symbioses with Glomeromycotina and
Mucoromycotina in non-vascular and early vascular
plants, in conjunction with evidence for Mucoromycotina
Colonisation by fine root endophytes within the roots of Lotus
subbiflorus (Fabaceae). Bar 100 mm. nutritional mutualisms in early-diverging liverworts
[26,31], strengthens the hypothesis that Mucoromyco-
tina aided pioneering land plants. Genetic studies of
mycorrhizal fungi, the ability to produce arbuscules plant–fungal symbioses [2,24] are revealing extensive
(Figure 2) led to their initial classification as Glomus molecular and chemical crosstalk between the partners.
within the arbuscular mycorrhizal fungi [50]. However, To date, strigolactones from roots and lipochitooligosac-
recent research by Orchard et al. [51] suggests that fine charides from fungi have been implicated in the estab-
root endophytes are members of the Mucoromycotina, lishment of arbuscular mycorrhizas [59,60]. However,
related to several Mucoromycotina identified from liver- the molecular basis for the functioning of Mucoromyco-
worts and lycopods by Field et al. [22,35] and Rimington tina fungal partnerships, including those of fine root
et al. [27,40]. This makes fine root endophytes the only endophtyes, in non-vascular and vascular plants, has
known fungi to produce arbuscules outside of Glomer- yet to be investigated (Box 1). Given that many model
omycotina. A meta-analysis by Orchard et al. [50] showed plants are not symbiotic (e.g. Arabidopsis, Marchantia
that fine root endophytes, which are likely a species polymorpha, Physcomitrella), molecular and functional anal-
group, are globally distributed across many ecosystems ysis of targeted symbiotic liverworts, lycopods, ferns and
and colonise numerous vascular plant families [50]. In angiosperms will go a long way toward elucidating the
Australia and New Zealand they are prevalent within the nature and dynamics of ancient and widespread Mucor-
roots of crop and pasture species, where colonisation omycotina symbioses, informing the interpretation of
levels may be high and match those of arbuscular mycor- fossils [61], and our understanding of how lineages of
rhizal fungi [50]. Fine root endophytes have been asso- fungi and plants co-evolved on land and transformed their
ciated both with disturbed or extreme environments and environments.
early successional plant establishment [46,50,52–56] and
may provide growth benefits to the host plant [50,57], yet Acknowledgements
little is understood about the relationships between these This work was supported by a Natural Environment Research Council
standard grant to KJF, SP (NE/N00941X/1) and MIB (NE/N009665/1).
fungi and plants. Even less is known of the evolutionary MHR is funded by ARC Future Fellowship FT140100103. KJF is funded
relationships between fine root endophytes and the arbus- by a BBSRC Translational Fellowship (BB/M026825/1).
cular mycorrhizal fungi, for example, how they evolved to
co-exist within plant species and even individual root References and recommended reading
segments [50]. Putative fine root endophytes were Papers of particular interest, published within the period of review,
have been highlighted as:
recently identified in fossilised (permineralised) Permian
specimens of root mantle from the tree fern Psaronius  of special interest
 of outstanding interest
[58], raising questions about the evolutionary relationship
between fine root endophytes and the arbuscular mycor- 1. Wang B, Qiu YL: Phylogenetic distribution and evolution of
rhial fungi, and when arbuscules first evolved.  mycorrhizas in land plants. Mycorrhiza 2006, 16:299-363.

Current Opinion in Plant Biology 2018, 44:1–6 www.sciencedirect.com

 A mycorrhizal revolution Hoysted et al. 5

Most extensive survey to date of mycorrhizal types in plants (i.e. arbus- 22. Field KJ, Rimington WR, Bidartondo MI, Allison KE, Beerling DJ,
cular, ectomycorrhizal, ericoid, orchid, etc.).  Cameron DD, Duckett JG, Leake JR, Pressel S: First evidence of
mutualism between ancient plant lineages (Haplomitriopsida
2. Field KJ, Pressel S, Duckett JG, Rimington WR, Bidartondo MI: liverworts) and Mucoromycotina fungi and its response to
 Symbiotic options for the conquest of land. Trends Ecol Evol simulated Paleozoic changes in atmospheric CO2. New Phytol
2015, 30:477-486. 2015, 205:743-756.
Comprehensive critical review of fungal endosymbioses in non-vascular Demonstration of nutritional exchange between Mucoromycotina and the
plants. earliest diverging non-vascular plants, and fulfilment of Koch’s
postulates.
3. Selosse MA, Le Tacon F: The land flora: a phototroph–fungus
partnership? Trends Ecol Evol 1998, 13:15-20. 23. Almario J, Jeena G, Wunder J, Langen G, Zuccaro A, Coupland G,
Bucher M: Root-associated fungal microbiota of
4. Field KJ, Cameron DD, Leake JR, Tille S, Bidartondo MI, nonmycorrhizal Arabis alpina and its contribution to
Beerling DJ: Contrasting arbuscular mycorrhizal responses of plant phosphorus nutrition. Proc Natl Acad Sci 2017,
vascular and non-vascular plants to a simulated Palaeozoic 114:E9403-E9412.
CO2 decline. Nat Commun 2012, 3:835.
24. van der Heijden MGA, Martin FM, Selosse MA, Sanders IR:
5. Read DJ, Duckett JG, Francis R, Ligrone R, Russell A: Symbiotic Mycorrhizal ecology and evolution: the past, the present, and
fungal associations in ‘lower’ land plants. Philos Trans R Soc the future. New Phytol 2015, 205:1406-1423.
2000, 355:815-830.
25. Desirò A, Rimington WR, Jacob A, vande Pol N, Smith ME,
6. Jakobsen I, Rosendahl L: Carbon flow into soil and external Trappe JM, Bidartondo MI, Bonito GM: Multigene phylogeny of
hyphae from roots of mycorrhizal cucumber plants. New Phytol Endogonales, an early diverging lineage of fungi associated
1990, 115:77-83. with plants. IMA Fungus 2017, 8:245-257.
7. Smith SE, Read DJ: Mycorrhizal Symbiosis. edn 3. Academic 26. Bidartondo MI, Read DJ, Trappe JM, Merckx V, Ligrone R,
Press; 2010.  Duckett JG: The dawn of symbiosis between plants and fungi.
8. Jakobsen I, Abbott LK, Robso AD: External hyphae of vesicular– Biol Lett 2011, 7:574-577.
arbuscular mycorrhizal fungi associated with Trifolium First identification of Mucoromycotina symbioses in plants (i.e. liverworts,
subterraneum L. 1. Spread of hyphae and phosphorus inflow hornworts, ferns) and diverse Glomeromycotina in non-vascular plants.
into roots. New Phytol 1992, 120:371-380. 27. Rimington WR, Pressel S, Duckett JG, Bidartondo MI: Fungal
9. Leake JR, Johnson D, Donnelly DP, Muckle GE, Boddy L, Read DJ:  associations of basal vascular plants: reopening a closed
Networks of power and influence: the role of mycorrhizal book? New Phytol 2015, 205:1394-1398.
mycelium in controlling plant communities and Extensive and detailed analysis of the distribution of fungal endosym-
agroecosystem functioning. Can J Bot 2004, 82:1016-1045. bioses in lycopods and ferns showing Glomeromycotina fungi are domi-
nant, but Mucoromycotina are also present.
10. Smith SE, Smith FA: Roles of arbuscular mycorrhizas in plant
nutrition and growth: new paradigms from cellular to 28. Yamamoto K, Endo N, Degawa Y, Fukuda M, Yamada A: First
ecosystem scales. Annu Rev Plant Biol 2011, 62:227-250. detection of Endogone ectomycorrhizas in natural oak
forests. Mycorrhiza 2017, 27:295-301.
11. Hodge A, Storer K: Arbuscular mycorrhiza and nitrogen:
implications for individual plants through to ecosystems. Plant 29. Walker C: Endogone lactiflua forming ectomycorrhizas with
Soil 2015, 386:1-19. Pinus contorta. Trans Br Mycol Soc 1985, 84:353-355.

12. Luginbuehl LH, Menard GN, Kurup S, Van Erp H, 30. Blasius D, Feil W, Kottke I, Oberwinkler F: Hartig net structure
Radhakrishmam GV, Breakspear A, Oldroyd GE, Eastmond PJ: and formation in fully ensheathed ectomycorrhizas. Nord J Bot
Fatty acids in arbuscular mycorrhizal fungi are synthesised by 1986, 6:837-842.
the host plant. Science 2017. eaan0081. 31. Desiro A, Duckett JG, Pressel S, Villarreal JC, Bidartondo MI:
13. Lewis DH, Harley JL: Carbohydrate physiology of mycorrhizal  Fungal symbioses in hornworts: a chequered history. Proc
roots of beech. New Phytol 1965, 64:224-237. Royal Soc B 2013, 280:20130207.
Comprehensive analysis of Mucoromycotina and Glomeromycotina dis-
14. Jiang Y, Wang W, Xie Q, Liu N, Liu L, Wang D, Zhang X, Yang C, tribution and evolution in hornworts, showing single, dual and absent
Chen X, Tang D et al.: Plants transfer lipids to sustain symbioses.
colonization by mutualistic mycorrhizal and parasitic fungi.
Science 2017, 356:1172-1175. 32. Strullu-Derrien C, Kenrick P, Pressel S, Duckett JG, Rioult JP,
Strullu DG: Fungal associations in Horneophyton ligneri from
15. Keymer A, Pimprikar P, Wewer V, Huber C, Brands M, Bucerius S, the Rhynie Chert (c. 407 million year old) closely resemble
Delaux PM, Klingl V, von Roepenack-Lahaye E, Wang TL et al.: those in extant lower land plants: novel insights into ancestral
Lipid transfer from plants to arbuscular mycorrhizal fungi. plant–fungal symbioses. New Phytol 2014, 203:964-979.
BioRxiv 2017:143883.
33. Krings M, Taylor TN, Hass H, Kerp H, Dotzler N, Hermsen EJ: An
16. Pirozynski KA, Malloch DW: The origin of land plants: a matter of alternative mode of early land plant colonisation by putative
mycotrophism. Biosystems 1975, 6:153-164. endomycorrhizal fungi. Plant Signal Behav 2007, 2:125-126.

17. Redecker D, Kodner R, Graham LE: Glomalean fungi from the 34. Carella P, Gogleva A, Tomaselli M, Alfs C, Schornack S:
Ordovician. Science 2000, 289:1920-1921. Phytophthora palmivora establishes tissue-specific
intracellular infection structures in the earliest divergent land
18. Pressel S, Bidartondo MI, Ligrone R, Duckett JG: Fungal plant lineage. bioRxiv 2017 http://dx.doi.org/10.1101/188912.
symbioses in bryophytes: new insights in the Twenty First
Century. Phytotaxa 2014, 9:238-253. 35. Field KJ, Rimington WR, Bidartondo MI, Allison KE, Beerling DJ,
 Cameron DD, Duckett JG, Leake JR, Pressel S: Functional
19. Wang B, Yeun LH, Xue JY, Liu Y, Ané JM, Qiu YL: Presence of analysis of liverworts in dual symbiosis with Glomeromycota
three mycorrhizal genes in the common ancestor of land and Mucoromycotina fungi under a simulated Paleozoic CO2
plants suggests a key role of mycorrhizas in the colonisation decline. ISME J 2016, 10:1514-1526.
of land by plants. New Phytol 2010, 186:514-525. First direct functional comparison of Glomeromycotina and Mucoromy-
cotina symbioses in plants showing significant differences between
20. Delaux PM, Séjalon-Delmas N, Bécard G, Ané JM: Evolution of Glomeromycotina, Mucoromycotina and dual associations.
the plant–microbe symbiotic ‘toolkit’. Trends Plant Sci 2013,
18:298-304. 36. Berner RA: GEOCARBSULF: a combined model for
Phanerozoic atmospheric O2 and CO2. Geochim Cosmochim
21. Krings M, Taylor TN, Dotzler N: Fungal endophytes as a Acta 2006, 70:5653-5664.
driving force in land plant evolution. In Biocomplexity of Plant–
Fungal Interactions. Edited by Southworth D. John Wiley & Sons; 37. Qiu YL, Li L, Wang B, Chen Z, Knoop V, Groth-Malonek M,
2012:5-28. Dombrovska O, Lee J, Kent L, Rest J et al.: The deepest

www.sciencedirect.com Current Opinion in Plant Biology 2018, 44:1–6

6 Biotic interactions

divergences in land plants inferred from phylogenomic Pellaea viridis from metalliferous soils. Chemosphere 2013,
evidence. Proc Natl Acad Sci USA 2006, 103:15511-15516. 92:1267-1273.
38. Renzaglia KS, Villarreal JC, Duff RJ: New insights into 50. Orchard S, Standish RJ, Dickie IA, Renton M, Walker C, Moot D,
morphology, anatomy, and systematics of hornworts. In  Ryan MH: Fine root endophytes under scrutiny: a review of the
Bryophyte Biology. Edited by Goffinet B, Shaw AJ. Cambridge literature on arbuscule-producing fungi recently suggested to
University Press; 2009:139-172. belong to the Mucoromycotina. Mycorrhiza 2017, 27:618-638.
Comprehensive review and meta-analysis of fine root endophytes.
39. Villarreal JC, Renner SS: Hornwort pyrenoids: carbon-
concentrating mechanisms evolved and were lost at least five 51. Orchard S, Hilton S, Bending GD, Dickie IA, Standish RJ,
times during the last 100 million years. Proc Natl Acad Sci USA  Gleeson DB, Jeffery RP, Powell JR, Walker C, Bass D et al.: Fine
2009, 109:18873-18878. endophytes (Glomus tenue) are related to Mucoromycotina,
not Glomeromycota. New Phytol 2017, 213:481-486.
40. Rimington WR, Pressel S, Field KJ, Strullu-Derrien C, Duckett JG, Fine root endophytes belong in the Mucoromycotina, thus first report of
Bidartondo MI: Reappraising the origin of mycorrhizas. In arbuscules outside of the Glomeromycotina.
Molecular Mycorrhizal Symbiosis. Edited by Martin F. John Wiley
and Sons; 2016:31-32. 52. Daft MJ, Nicolson TH: Arbuscular mycorrhizas in
plants colonizing coal wastes in Scotland. New Phytol 1974,
41. Duckett JG, Ligrone R: A light and electron microscope study of 73:1129-1138.
the fungal endophytes in the sporophyte and gametophyte of
Lycopodium cernuum with observations on the gametophyte– 53. Johnson PN: Mycorrhizal Endogonaceae in a New Zealand
sporophyte junction. Can J Bot 1992, 70:58-72. forest. New Phytol 1977, 78:161-170.

42. Schmid E, Oberwinkler F: Mycorrhiza-like interaction between 54. Sigüenza C, Corkidi L, Allen E: Feedbacks of soil inoculum of
the achlorophyllous gametophyte of Lycopodium clavatum L. mycorrhizal fungi altered by N deposition on the growth of a
and its fungal endophyte studied by light and electron native shrub and an invasive annual grass. Plant Soil 2006,
microscopy. New Phytol 1993, 124:69-81. 286:153-165.
55. Sigüenza C, Crowley DE, Allen EB: Soil microorganisms of a
43. Horn K, Franke T, Unterseher M, Schnittler M, Beenken L:
native shrub and exotic grasses along a nitrogen deposition
Morphological and molecular analyses of fungal endophytes
gradient in southern California. Appl Soil Ecol 2006, 32:13-26.
of achlorophyllous gametophytes of Diphasiastrum alpinum
(Lycopodiaceae). Am J Bot 2013, 100:2158-2174. 56. Orchard S, Standish RJ, Nicol D, Gupta VVSR, Ryan MH: The
response of fine root endophyte (Glomus tenue) to
44. Pressel S, Bidartondo MI, Field KJ, Rimington WR, Duckett JG: waterlogging is dependent on host plant species and soil type.
Pteridophyte fungal associations: current knowledge and Plant Soil 2016, 403:305-315.
future perspectives. J Syst Evol 2016, 54:666-678.
57. Crush JR: Significance of endomycorrhizas in
45. Field KJ, Leake JR, Tille S, Allison KE, Rimington WR, tussock grassland in Otago, New Zealand. New Zeal J Bot
Bidartondo MI, Beerling DJ, Cameron DD: From mycoheterophy 1973, 11:645-660.
to mutualism: mycorrhizal specificity and functioning in
Ophioglossum vulgatum sporophytes. New Phytol 2015, 58. Krings M, Harper CJ, White JF, Barthel M, Heinrichs J, Taylor EL,
205:1492-1502. Taylor TN: Fungi in a Psaronius root mantle from the
Rotliegend (Asselian, Lower Permian/Cisuralian) of Thuringia,
46. Turnau K, Ronikier M, Unrug J: Role of mycorrhizal links Germany. Rev Palaeobot Palynol 2017, 239:14-30.
between plants in establishment of liverworts thalli in natural
habitats. Acta Soc Bot Pol 1999, 68:63-68. 59. Luginbuehl L, Oldroyd GED: Calcium signalling and
transcriptional regulation in arbuscular mycorrhizal
47. Turnau K, Anielska T, Jurkiewicz A: Mycothallic/mycorrhizal symbiosis. In Molecular Mycorrhizal Symbiosis. Edited by Martin
symbiosis of chlorophyllous gametophytes and sporophytes F. John Wiley and Sons; 2016:125-140.
of a fern, Pellaea viridis (Forsk.) Prantl (Pellaeaceae,
Pteridales). Mycorrhiza 2005, 15:121-128. 60. Gough C, Bécard G: Strigolactones and
 lipochitooligosachharides as molecular communication
48. Turnau K, Anielska T, Ryszka P, Gawronski S, Ostachowicz B, signals in the arbuscular mycorrhizal symbiosis. In Molecular
Jurkiewicz A: Establishment of arbuscular mycorrhizal plants Mycorrhizal Symbiosis. Edited by Martin F. John Wiley and Sons;
originating from xerothermic grasslands on heavy metal rich 2016:107-124.
industrial wastes — new solution for waste revegetation. Plant Extensive review on the roles of strigolactones and lipochitooligosac-
Soil 2008, 305:267-280. charides as early mycorrhizal signals in arbuscular mycorrhizal networks.
49. Turnau K, Przybyłowicz WJ, Ryszka P, Orłowska E, Anielska T, 61. Taylor TN, Remy W, Hass H, Kerp H: Fossil
Mesjasz-Przybyłowicz J: Mycorrhizal fungi modify element arbuscular mycorrhizae from the early Devonian. Mycologia
distribution in gametophytes and sporophytes of the fern 1995, 87:560-573.

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