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Large-scale genome sequencing of mycorrhizal fungi provides insights into the early evolution of symbiotic traits

Author

Listed:
  • Shingo Miyauchi

    (Université de Lorraine, Institut national de recherche pour l’agriculture, l’alimentation et l’ environnement, UMR Interactions Arbres/Microorganismes, Centre INRAE Grand Est-Nancy)

  • Enikő Kiss

    (Synthetic and Systems Biology Unit, Biological Research Centre)

  • Alan Kuo

    (US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory)

  • Elodie Drula

    (INRAE, USC1408 Architecture et Fonction des Macromolécules Biologiques)

  • Annegret Kohler

    (Université de Lorraine, Institut national de recherche pour l’agriculture, l’alimentation et l’ environnement, UMR Interactions Arbres/Microorganismes, Centre INRAE Grand Est-Nancy)

  • Marisol Sánchez-García

    (Clark University, Lasry Center for Bioscience)

  • Emmanuelle Morin

    (Université de Lorraine, Institut national de recherche pour l’agriculture, l’alimentation et l’ environnement, UMR Interactions Arbres/Microorganismes, Centre INRAE Grand Est-Nancy)

  • Bill Andreopoulos

    (US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory)

  • Kerrie W. Barry

    (US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory)

  • Gregory Bonito

    (Plant Soil and Microbial Sciences, Michigan State University)

  • Marc Buée

    (Université de Lorraine, Institut national de recherche pour l’agriculture, l’alimentation et l’ environnement, UMR Interactions Arbres/Microorganismes, Centre INRAE Grand Est-Nancy)

  • Akiko Carver

    (US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory)

  • Cindy Chen

    (US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory)

  • Nicolas Cichocki

    (Université de Lorraine, Institut national de recherche pour l’agriculture, l’alimentation et l’ environnement, UMR Interactions Arbres/Microorganismes, Centre INRAE Grand Est-Nancy)

  • Alicia Clum

    (US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory)

  • David Culley

    (Chemical & Biological Processes Development Group, Pacific Northwest National Laboratory)

  • Pedro W. Crous

    (Westerdijk Fungal Biodiversity Institute)

  • Laure Fauchery

    (Université de Lorraine, Institut national de recherche pour l’agriculture, l’alimentation et l’ environnement, UMR Interactions Arbres/Microorganismes, Centre INRAE Grand Est-Nancy)

  • Mariangela Girlanda

    (University of Torino)

  • Richard D. Hayes

    (US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory)

  • Zsófia Kéri

    (Synthetic and Systems Biology Unit, Biological Research Centre)

  • Kurt LaButti

    (US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory)

  • Anna Lipzen

    (US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory)

  • Vincent Lombard

    (INRAE, USC1408 Architecture et Fonction des Macromolécules Biologiques)

  • Jon Magnuson

    (Chemical & Biological Processes Development Group, Pacific Northwest National Laboratory)

  • François Maillard

    (Université de Lorraine, Institut national de recherche pour l’agriculture, l’alimentation et l’ environnement, UMR Interactions Arbres/Microorganismes, Centre INRAE Grand Est-Nancy)

  • Claude Murat

    (Université de Lorraine, Institut national de recherche pour l’agriculture, l’alimentation et l’ environnement, UMR Interactions Arbres/Microorganismes, Centre INRAE Grand Est-Nancy)

  • Matt Nolan

    (US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory)

  • Robin A. Ohm

    (US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory)

  • Jasmyn Pangilinan

    (US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory)

  • Maíra de Freitas Pereira

    (Université de Lorraine, Institut national de recherche pour l’agriculture, l’alimentation et l’ environnement, UMR Interactions Arbres/Microorganismes, Centre INRAE Grand Est-Nancy)

  • Silvia Perotto

    (University of Torino)

  • Martina Peter

    (Swiss Federal Institute for Forest, Snow and Landscape Research WSL)

  • Stephanie Pfister

    (Swiss Federal Institute for Forest, Snow and Landscape Research WSL)

  • Robert Riley

    (US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory)

  • Yaron Sitrit

    (The Jacob Blaustein Institutes for Desert Research, Bergman Campus, Ben-Gurion University of The Negev)

  • J. Benjamin Stielow

    (Westerdijk Fungal Biodiversity Institute)

  • Gergely Szöllősi

    (Synthetic and Systems Biology Unit, Biological Research Centre)

  • Lucia Žifčáková

    (Laboratory of Environmental Microbiology, Institute of Microbiology of the Czech Academy of Sciences)

  • Martina Štursová

    (Laboratory of Environmental Microbiology, Institute of Microbiology of the Czech Academy of Sciences)

  • Joseph W. Spatafora

    (Oregon State University)

  • Leho Tedersoo

    (University of Tartu)

  • Lu-Min Vaario

    (University of Helsinki)

  • Akiyoshi Yamada

    (Institute of Mountain Science, Faculty of Agriculture, Shinshu University, Minami-minowa, Kami-ina)

  • Mi Yan

    (US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory)

  • Pengfei Wang

    (Department of Key Laboratory, The 2nd Affiliated Hospital of Kunming Medical University)

  • Jianping Xu

    (McMaster University)

  • Tom Bruns

    (University of California – Berkeley)

  • Petr Baldrian

    (Laboratory of Environmental Microbiology, Institute of Microbiology of the Czech Academy of Sciences)

  • Rytas Vilgalys

    (Duke University)

  • Christophe Dunand

    (Laboratoire de Recherche en Sciences Végétales, Université de Toulouse, CNRS, UPS)

  • Bernard Henrissat

    (INRAE, USC1408 Architecture et Fonction des Macromolécules Biologiques
    Architecture et Fonction des Macromolécules Biologiques (AFMB), CNRS, Aix-Marseille Univ.
    King Abdulaziz University)

  • Igor V. Grigoriev

    (US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory
    University of California – Berkeley)

  • David Hibbett

    (Clark University, Lasry Center for Bioscience)

  • László G. Nagy

    (Synthetic and Systems Biology Unit, Biological Research Centre)

  • Francis M. Martin

    (Université de Lorraine, Institut national de recherche pour l’agriculture, l’alimentation et l’ environnement, UMR Interactions Arbres/Microorganismes, Centre INRAE Grand Est-Nancy
    Beijing Advanced Innovation Centre for Tree Breeding by Molecular Design (BAIC-TBMD), Institute of Microbiology, Beijing Forestry University)

Abstract

Mycorrhizal fungi are mutualists that play crucial roles in nutrient acquisition in terrestrial ecosystems. Mycorrhizal symbioses arose repeatedly across multiple lineages of Mucoromycotina, Ascomycota, and Basidiomycota. Considerable variation exists in the capacity of mycorrhizal fungi to acquire carbon from soil organic matter. Here, we present a combined analysis of 135 fungal genomes from 73 saprotrophic, endophytic and pathogenic species, and 62 mycorrhizal species, including 29 new mycorrhizal genomes. This study samples ecologically dominant fungal guilds for which there were previously no symbiotic genomes available, including ectomycorrhizal Russulales, Thelephorales and Cantharellales. Our analyses show that transitions from saprotrophy to symbiosis involve (1) widespread losses of degrading enzymes acting on lignin and cellulose, (2) co-option of genes present in saprotrophic ancestors to fulfill new symbiotic functions, (3) diversification of novel, lineage-specific symbiosis-induced genes, (4) proliferation of transposable elements and (5) divergent genetic innovations underlying the convergent origins of the ectomycorrhizal guild.

Suggested Citation

  • Shingo Miyauchi & Enikő Kiss & Alan Kuo & Elodie Drula & Annegret Kohler & Marisol Sánchez-García & Emmanuelle Morin & Bill Andreopoulos & Kerrie W. Barry & Gregory Bonito & Marc Buée & Akiko Carver &, 2020. "Large-scale genome sequencing of mycorrhizal fungi provides insights into the early evolution of symbiotic traits," Nature Communications, Nature, vol. 11(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-18795-w
    DOI: 10.1038/s41467-020-18795-w
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    Cited by:

    1. Biao-Feng Zhou & Shuai Yuan & Andrew A. Crowl & Yi-Ye Liang & Yong Shi & Xue-Yan Chen & Qing-Qing An & Ming Kang & Paul S. Manos & Baosheng Wang, 2022. "Phylogenomic analyses highlight innovation and introgression in the continental radiations of Fagaceae across the Northern Hemisphere," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    2. Fantin Mesny & Shingo Miyauchi & Thorsten Thiergart & Brigitte Pickel & Lea Atanasova & Magnus Karlsson & Bruno Hüttel & Kerrie W. Barry & Sajeet Haridas & Cindy Chen & Diane Bauer & William Andreopou, 2021. "Genetic determinants of endophytism in the Arabidopsis root mycobiome," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    3. Philipp Resl & Adina R. Bujold & Gulnara Tagirdzhanova & Peter Meidl & Sandra Freire Rallo & Mieko Kono & Samantha Fernández-Brime & Hörður Guðmundsson & Ólafur Sigmar Andrésson & Lucia Muggia & Helmu, 2022. "Large differences in carbohydrate degradation and transport potential among lichen fungal symbionts," Nature Communications, Nature, vol. 13(1), pages 1-13, December.

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