The Land Flora: a Phototroph–Fungus Partnership? M-A
Total Page：16
File Type：pdf, Size：1020Kb
REVIEWS The land flora: a phototroph–fungus partnership? M-A. Selosse and F. Le Tacon iving on emerged land Numerous mutualistic associations fossils, such as the Devonian raises several problems: between phototrophs and fungi exist in Spongiophyton11 or the Siluro– water may be rare or the extant land biota. Some are Devonian nematophytes12, have L absent, implying (1) that widespread, such as lichens and been interpreted as lichen struc- mineral nutrition is more or less mycorrhizae, but some are less well tures, but this awaits further evi- impaired, (2) radiation (mainly known or restricted to special ecological dence. Less-disputed fossils from toxic UV-rays) is not filtered out conditions, such as endophytes in plants the Eocene are available13, and a and (3) strong fluctuations of tem- and algae. Recent molecular data and Permo–Triassic origin has been perature are not prevented. In fossils suggest that associations arose suggested for ascomycete spite of those adversities, Precam- repeatedly and that some of them are lichens8. Basidiomycete lichens brian land was colonized by ancient, and even ancestral in the case of are likely to have evolved more phototrophic microorganisms, land plants. Mutualism, that provides recently, such as the genus probably prokaryotes1, and multi- various adaptations to terrestrial Omphalina, in which intermedi- cellular terrestrial phototrophs constraints, may have played a crucial ates of the transition to licheniz- arose during the Silurian, about role during terrestrialization and evolution ation still exist14. Present-day 450 million years ago2. How did of land phototrophs. lichens thus probably originated phototrophs overcome land after land colonization by plants, stresses? Nowadays, the pioneer and early Paleozoic lichens should colonizers are mainly lichens – not M-A. Selosse and F. Le Tacon are in the involve a non-septate or an ances- simple phototrophs, but a mutual- Equipe de Microbiologie Forestière, INRA Nancy, tral septate fungus. An extant non- 54280 Champenoux, France. istic association of a phototroph septate fungus, Geosiphon pyri- with a fungus. At closer inspec- forme, related to the Glomales15 tion, almost all present-day photo- (the VA fungi – see below), forms trophs adapted to terrestrial bladders containing endosymbi- ecosystems form mutualistic associations with fungi otic Nostoc (Fig. 1). This association, capable of photosyn- (Box 1), which are often lost in secondarily aquatic photo- thetic carbon assimilation and N-fixation16, and living on trophs, as documented for mycorrhizal symbiosis3. The poor loamy soil, could be similar to primitive lichens. A 400 fungi involved in these associations, the ‘mycobionts’, are million year-old fossil lichen from the Rhynie Chert17, con- non-septate Zygomycotina and septate Ascomycotina and sisting of coccoid cyanobacteria and a zygomycete fungus, Basidiomycotina. Fossil record4 and molecular clock data5 supports the existence of Paleozoic non-septate lichens. (Box 2) suggest that terrestrial non-septate fungi originated Lichens involving cyanobacteria and non-septate fungi during the Cambrian, and septate fungi during the Devon- can be expected to have existed until 1000 million years ian. They thus had opportunities to interact with the terres- ago, as fungi and other main eukaryotic lineages radiated. trial flora during much of its evolution. Here, we review new However, Precambrian fossil lichens, such as Thuchomyces evidence that (1) mutualism with fungi is widespread lichenoides from South Africa, are often considered dubi- among extant phototrophs and ancient in land ecosystems ous2. The enigmatic Ediacarian fossils were recently pro- and (2) that it allowed various critical adaptations during the posed to be lichens, because of their resistance to burial evolution of land phototrophs. compaction10, but few anatomical data have been recov- ered from those compressed structures. We still know very Terrestrial algae repeatedly interacted with fungi little about possible Precambrian lichens, and phototrophs Terrestrial microscopic phototrophs, unicellular or fila- found in Precambrian paleosoils were able to live on land mentous, belong to cyanobacteria and green algae (e.g. independently of symbiosis1, as do present-day free-living Trentepohlia, Pleurococcus) and are either free-living or algae and cyanobacteria. Lichenization would thus seem more frequently associated with mutualistic fungi, to form secondary in algal and cyanobacterial evolution. Nowa- lichens6. As shown by molecular approaches7, lichen-form- days, lichenization provides these phototrophs a broader ing fungi arose many times during the evolution of both ecological niche. Earlier in their evolution, it probably Ascomycotina and Basidiomycotina. Lichens, in which the allowed them to stay and diversify on land after the rise alga is protected by the fungal stroma, tolerate a wide of multicellular plants: the latter probably outcompeted range of conditions8 under which neither vascular plants simple free-living algae. nor free-living partners could survive: they tolerate Macroscopic and pseudoparenchymatous algae – that drought, cold and heat, intense light, barren rocky is, green, red and brown algae – are not common in land eco- substrates. systems. However, such algae living in the tidal zone lead a Such conditions may well have prevailed on land before semi-terrestrial existence during low tide. Interestingly, they colonization, so that one could wonder whether lichens were form a less well-known association (the so-called ‘myco- the first the land colonizers. Fossils and molecular data indi- phycobiosis’, Box 1) with ascomycetes living intercellularly, cate that Basidiomycotina and Ascomycotina, the extant inside the algal thallus18. The best known is the brown alga mycobionts of lichens, did not arise before the Devonian2,5, Ascophyllum nodosum (Fig. 2) which is always infected by or at most the Silurian9 (Box 2). Poorly understood Paleozoic Mycosphaerella ascophylli. The association is facultative, TREE vol. 13, no. 1 January 1998 Copyright © 1998, Elsevier Science Ltd. All rights reserved. 0169-5347/98/$19.00 PII: S0169-5347(97)01230-5 15 REVIEWS Plants are ancestrally Box 1. Glossary of extant phototroph–fungi mutualisms mutualistic with Glomales Lichens are composed of a cyanobacterium or a green alga embedded in a vegetative stroma of an ascomycete or, less Land colonization by frequently, a basidiomycete6. Geosiphon pyriforme (Fig. 1) is a non-septate fungus that harbors intracellular cyanobacteria16. multicellular phototrophs Mycophycobioses are composed of an ascomycete embedded in the thallus of a multicellular alga18 (Fig. 2). involved the radiation of the ‘Plantae’ (a particular sub- 20 Mycorrhiza are composed of septate or non-septate fungi within a root, but also exploring the surrounding soil (see fig- group of green algae phylo- ure). In ectomycorrhiza, a septate fungus forms a sheath around the root (‘sheath-forming mycorrhiza’) and grows between cortical cells forming the so-called Hartig net. Endomycorrhiza involves non-septate Glomales (VA mycorrhiza) or septate genetically independent of fungi (ericoid and orchid mycorrhiza). In both cases, the fungus penetrates the cortical cells where it forms respectively terrestrial green microalgae) arbuscules or coils. Ectendomycorrhiza formed by basidiomycetes in some Ericales (e.g. Arbutus) shares features of both during the Silurian, with ecto- and endo-mycorrhizae, i.e. a sheath and intracellular coils. possible precursors during Mycorrhizome and mycothallus are composed of septate or non-septate fungi within a rhizome and a thallus (Fig. 4) of a the Ordovician2 (Box 2). land plant respectively21. These phototrophs, prob- Symptomless endophytes (often ascomycetes, such as Clavicipitaceae in grasses) live intercellularly in various plant ably derived from Charo- organs40. Some may be transmitted by seeds. The name mycophylla has been proposed for associations between leaves phyta, share an egg-protect- 42 and endophytes . ing archegonium and are divided into two main lin- Ectomycorrhizae eages: Atrachaetae (mosses, hepatics and hornworts) and Tracheophytae (vascular plants). Vascular plants, but also hepatics and hornworts, External hyphae have various mycobionts inhabiting different veg- Hartig net etative organs (Box 1). Non-septate fungi form VA endomycorrhizae mutualistic associations with Sheath about 90% of these photo- trophs. The fungus grows Arbuscule intercellularly and forms vesicles and intracellular arbuscules (Box 1). The vesicular–arbuscular (VA) associations occur in roots of Arbutoid Vesicle Spore Ectendomycorrhizae vascular plants (the so- called VA mycorrhiza)20, but also in rhizomes and gameto- phytes of ferns and their allies21 and in hepatics such as Metzgeriales and Marchantiales22 (mycorrhi- Stele zomes and mycothalli). VA fungi facilitate mineral nu- trition of the phototroph, Ericoid endomycorrhizae mainly the uptake of phos- phorus and microelements Coils whose mobility in soil is often low. They also protect Orchid endomycorrhizae the root system against soil- borne pathogens23. VA fungi belong to a small group of about 200 species of zygomycetes, the Glomales. They are strictly biotrophic, asexual, and only distantly since axenic cultures are possible, but the fungus seems to related to other zygomycetes – a feature suggesting a long protect the alga against desiccation19. The same fungus is evolutionary stasis in a stable and protected biological