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

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, Cindy Chen, Nicolas Cichocki, Alicia Clum, David Culley, Pedro W. Crous, Laure Fauchery, Mariangela Girlanda, Richard D. Hayes, Zsófia Kéri, Kurt LaButti, Anna Lipzen, Vincent Lombard, Jon Magnuson, François Maillard, Claude Murat, Matt Nolan, Robin A. Ohm, Jasmyn Pangilinan, Maíra de Freitas Pereira, Silvia Perotto, Martina Peter, Stephanie Pfister, Robert Riley, Yaron Sitrit, J. Benjamin Stielow, Gergely Szöllősi, Lucia Žifčáková, Martina Štursová, Joseph W. Spatafora, Leho Tedersoo, Lu-Min Vaario, Akiyoshi Yamada, Mi Yan, Pengfei Wang, Jianping Xu, Tom Bruns, Petr Baldrian, Rytas Vilgalys, Christophe Dunand, Bernard Henrissat, Igor V. Grigoriev, David Hibbett, László G. Nagy and Francis M. Martin ()
Additional contact information
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
Igor V. Grigoriev: US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory
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

Nature Communications, 2020, vol. 11, issue 1, 1-17

Abstract: 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.

Date: 2020
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DOI: 10.1038/s41467-020-18795-w

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