The land flora: a phototroph-fungus partnership?

https://doi.org/10.1016/S0169-5347(97)01230-5Get rights and content

Abstract

Numerous mutualistic associations between phototrophs and fungi exist in the extant land biota. Some are widespread, such as lichens and mycorrhizae, but some are less well known or restricted to special ecological conditions, such as endophytes in plants and algae. Recent molecular data and fossils suggest that associations arose repeatedly and that some of them are ancient, and even ancestral in the case of land plants. Mutualism, that provides various adaptations to terrestrial constraints, may have played a crucial role during terrestrialization and evolution of land phototrophs.

Section snippets

Terrestrial algae repeatedly interacted with fungi

Terrestrial microscopic phototrophs, unicellular or filamentous, belong to cyanobacteria and green algae (e.g. Trentepohlia, Pleurococcus) and are either free-living or more frequently associated with mutualistic fungi, to form lichens[6]. As shown by molecular approaches[7], lichen-forming fungi arose many times during the evolution of both Ascomycotina and Basidiomycotina. Lichens, in which the alga is protected by the fungal stroma, tolerate a wide range of conditions[8]under which neither

Plants are ancestrally mutualistic with glomales

Land colonization by multicellular phototrophs involved the radiation of the `Plantae' (a particular subgroup of green algae phylogenetically independent of terrestrial green microalgae) during the Silurian, with possible precursors during the Ordovician[2](Appendix B). These phototrophs, probably derived from Charophyta, share an egg-protecting archegonium and are divided into two main lineages: Atrachaetae (mosses, hepatics and hornworts) and Tracheophytae (vascular plants). Vascular plants,

Plants repeatedly interacted with septate fungi

Although the majority of advanced groups, such as grasses, retained the primitive VA mycorrhiza, other plants associated with septate fungi. Numerous trees and some shrubs (Gymnosperms, Gnetales and Angiosperms) form the so-called ectomycorrhizae (EcM) with septate fungi, Ascomycotina or Basidiomycotina, that grow intercellularly in the roots (Appendix A)[20]. The oldest known fossil EcM were found on Pinus roots from the Eocene[32], demonstrating that EcM were already established at least 50

Why 1+1>2 in terrestrialization

Adaptation to terrestrial life has often arisen through symbiosis, which brought together genetic material having different and complementary characteristics. The two partners are partly `preadapted' to live on land. The mycelial habit is well adapted to three-dimensional exploration of the substrate. Some mycobionts have a huge weathering potential, that allows access to non-soluble mineral elements44a, 44b, or even saprotrophic ability, that compensates for the low availability of mineral

Acknowledgements

We thank D.G. Garbary, M. Kluge, J. Kohlmeyer and T.N. Taylor for helpful discussion, and the authors who provided illustrations. We are grateful to K.A. Pirozynski for critically reading the manuscript. M-A. Selosse is on leave from Ecole Nationale du Génie Rural, des Eaux et des Forêts.

References (51)

  • Hawksworth, D.L. (1988) Coevolution of fungi with algae and cyanobacteria in lichen symbioses, in Coevolution of Fungi...
  • M.A Sherwood-Pike et al.

    Silurian fungal remains: probable records of the class Ascomycetes

    Lethaia

    (1985)
  • G.J Retallack

    Were the Ediacarian fossils lichens?

    Paleobiology

    (1994)
  • W.E Stein et al.

    Spongiophyton from the Lower Devonian of North America reinterpreted as a lichen

    Am. J. Bot.

    (1993)
  • N.D Burgess et al.

    A new palaeozoic plant closely allied to Prototaxites Dawson

    Bot. J. Linn. Soc.

    (1988)
  • M.A Sherwood-Pike

    Pelicothallos Dilcher, an overlooked fossil lichen

    Lichenologist

    (1985)
  • F Lutzoni et al.

    Omphalina (Basidiomycota, Agaricales) as a model system for the study of coevolution in lichens

    Crypt. Bot.

    (1995)
  • H.H Gehrig et al.

    Geosiphon pyriforme, a fungus forming endocytobiosis with Nostoc (Cyanobacteria), is an ancestral member of the Glomales—evidence by SSU rRNA analysis

    Mol. Evol.

    (1996)
  • D Mollenhauer et al.

    Geosiphon pyriforme

    Endocytobiosis Cell Res.

    (1994)
  • T.N Taylor et al.

    A cyanolichen from the Lower Devonian Rhynie Chert

    Am. J. Bot.

    (1997)
  • Kohlmeyer, J. and Kohlmeyer, E. (1979) Marine Mycology: the Higher Fungi, Academic...
  • D.J Garbary et al.

    The Ascophyllum, Polysiphonia, Mycosphaerella symbiosis -V. Fungal infection protects A. nodosum from desiccation

    Bot. Mar.

    (1995)
  • Smith, S.E. and Read, D.J. (1997) Mycorrhizal Symbiosis (2nd edn), Academic...
  • B Boullard

    Considérations sur la symbiose fongique chez les Ptéridophytes

    Syllogeus

    (1979)
  • R Ligrone et al.

    Cytology and development of a mycorrhiza-like infection in the gametophyte of Conocephalum conicum (L.) Dum. (Marchantiales, Hepatophyta)

    New Phytol.

    (1989)

    • Cited by (0)

    View full text
    Copyright © 1998 Elsevier Science Ltd. All rights reserved.