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  • Review Article
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Genomic and fossil windows into the secret lives of the most ancient fungi

Abstract

Fungi have crucial roles in modern ecosystems as decomposers and pathogens, and they engage in various mutualistic associations with other organisms, especially plants. They have a lengthy geological history, and there is an emerging understanding of their impact on the evolution of Earth systems on a large scale. In this Review, we focus on the roles of fungi in the establishment and early evolution of land and freshwater ecosystems. Today, questions of evolution over deep time are informed by discoveries of new fossils and evolutionary analysis of new genomes. Inferences can be drawn from evolutionary analysis by comparing the genes and genomes of fungi with the biochemistry and development of their plant and algal hosts. We then contrast this emerging picture against evidence from the fossil record to develop a new, integrated perspective on the origin and early evolution of fungi.

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Fig. 1: Evolution of early fungi.
Fig. 2: Geological ages of fungi, host plants and pivotal events in eukaryote diversification.
Fig. 3: Early Palaeozoic fungi: landscapes, hosts and fossils.
Fig. 4: Rhynie chert sporangium.

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Acknowledgements

The authors thank V. Leshyk (http://victorleshyk.com/paleo.html) for reconstruction of the Rhynie landscape and H. Kerp (University of Münster), D. Mosquin (University of British Columbia Botanical Garden) and A. Ives (University of Wisconsin-Madison) for permission to reuse photographs. The authors thank the following agencies and grants for support: Natural Sciences and Engineering Research Council of Canada Discovery Grant RGPIN-2016-03746 (M.L.B.); Marie Curie Intra-European Fellowship for Career Development SYMBIONTS GA-2011-298735, The Palaeontological Association UK grant PA-RG20160 and Fondation ARS Cuttoli–Paul Appell–Fondation de France grant 00103178 (C.S.-D.); Agence Nationale de la Recherche (ANR) grants ANR-10-LABX-41 and ANR-17-CE20-0006-01, and the Engineering Nitrogen Symbiosis for Africa (ENSA) project supported through a grant to the University of Cambridge by the Bill & Melinda Gates Foundation (OPP1172165) and the UK Department for International Development (DFID) (P.-M.D.); NASA grant 06-EXB06-0037 (P.K.S.); and The Laboratoire d’Excellence BCDiv Museum National d’Histoire Naturelle Paris grant ANR-10-LABX-0003 (M.-A.S. and C.S.-D.).

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Glossary

Precambrian

The geological interval beginning with the origin of the Earth 4.6 billion years ago and ending 541 million years ago (Ma), encompassing the Proterozoic Eon (2,500–541 Ma).

Mycorrhizae

Soil fungi in close contact with plant roots or other organs in a mutualistic symbiosis, providing mineral nutrients to the plant, and gaining carbon energy in return.

Terrestrial

Non-marine geological environments, including freshwater as well as land.

Palaeozoic

The geological era extending from 541 to 252 million years ago, after the Precambrian.

Nucleariid amoebas

Free-living, unicellular amoeboid protists on the fungal lineage that entrap their prey with thread-like filose pseudopodia.

Holozoa

Multicellular animals (Metazoa) and their closest (less well known) unicellular relatives, including Sphaeroforma and collar flagellates.

Aphelids

Unicellular parasites counted among fungi, the amoeba-like aphelids feed by injecting themselves into an algal cell and then engulfing and ingesting its contents.

Symbiosis

A close relationship in which symbionts that are separate organisms live together. We use the term here in the historical sense of De Bary 1879; the relationship can be mutualistic, benefiting both partners, or parasitic, in which case one organism benefits at the expense of another.

Arbuscules

Symbiotic, tree-like, branched fungal filaments within a plant cell that function as sites of plant–fungus nutrient exchange in arbuscular mycorrhizae.

Biotrophy

Nutrition from other living organisms; may refer to mutualists or parasites that are not killing their host.

Thalloid

Resembling a plant-like body but lacking roots, stems and leaves.

Acritarchs

Organic-walled microfossils of biological affinity, primarily eukaryotic.

Testate amoebae

Unicellular protists, polyphyletic, with an organic, mineral or agglutinated shell (test) that partially encloses the cell.

Prostrate axes

Creeping stem-like branches of early fossil plants that can be surficial or subterranean and that do not have all of the characteristics of a root or a rhizome of living plants.

Aerial axes

Erect stem-like branches of early fossil plants that do not have all the characteristics of the stem of living plants.

Sporophore

Spore-producing structure in fungi; a mushroom is a modern example.

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Berbee, M.L., Strullu-Derrien, C., Delaux, PM. et al. Genomic and fossil windows into the secret lives of the most ancient fungi. Nat Rev Microbiol 18, 717–730 (2020). https://doi.org/10.1038/s41579-020-0426-8

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