Université de Lorraine, Institut national de recherche pour l'agriculture, l'alimentation et l' environnement, UMR Interactions Arbres/Microorganismes, Centre INRAE Grand Est-Nancy, 54280, Champenoux, France.
Synthetic and Systems Biology Unit, Biological Research Centre, 6726, Szeged, Hungary.
US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.
INRAE, USC1408 Architecture et Fonction des Macromolécules Biologiques, 13009, Marseille, France.
Biology Department, Clark University, Lasry Center for Bioscience, 950 Main Street, Worcester, MA, 01610, USA.
Plant Soil and Microbial Sciences, Michigan State University, East Lansing, MI, 48824, USA.
Chemical & Biological Processes Development Group, Pacific Northwest National Laboratory, Richland, WA, USA.
Westerdijk Fungal Biodiversity Institute, Uppsalalaan 8, 3584 CT, Utrecht, Netherlands.
Department of Life Sciences and Systems Biology, University of Torino, Viale Mattioli 25, 10125, Torino, Italy.
Swiss Federal Institute for Forest, Snow and Landscape Research WSL, Zuercherstrasse 111, 8903, Birmensdorf, Switzerland.
The Jacob Blaustein Institutes for Desert Research, Bergman Campus, Ben-Gurion University of The Negev, Beer-Sheva, Israel.
Laboratory of Environmental Microbiology, Institute of Microbiology of the Czech Academy of Sciences, Videnska 1083, 14220, Praha 4, Czech Republic.
Department Botany & Plant Pathology, Oregon State University, Corvallis, OR, USA.
Natural History Museum, University of Tartu, 14a Ravila, 50411, Tartu, Estonia.
Department of Forest Sciences, University of Helsinki, Helsinki, Finland.
Institute of Mountain Science, Faculty of Agriculture, Shinshu University, Minami-minowa, Kami-ina, Nagano, 399-4598, Japan.
Department of Key Laboratory, The 2nd Affiliated Hospital of Kunming Medical University, 374 Dian Mian Road, Kunming, 650101, Yunnan, China.
Department of Biology, McMaster University, 1280 Main St. West, Hamilton, ON, L8S 4K1, Canada.
Department of Plant and Microbial Biology, University of California - Berkeley, Berkeley, CA, USA.
Department of Biology, Duke University, Durham, NC, 27708, USA.
Laboratoire de Recherche en Sciences Végétales, Université de Toulouse, CNRS, UPS, Toulouse, France.
Architecture et Fonction des Macromolécules Biologiques (AFMB), CNRS, Aix-Marseille Univ., 13009, Marseille, France.
Department of Biological Sciences, King Abdulaziz University, Jeddah, Saudi Arabia.
Université de Lorraine, Institut national de recherche pour l'agriculture, l'alimentation et l' environnement, UMR Interactions Arbres/Microorganismes, Centre INRAE Grand Est-Nancy, 54280, Champenoux, France. francis.martin@inrae.fr.
Beijing Advanced Innovation Centre for Tree Breeding by Molecular Design (BAIC-TBMD), Institute of Microbiology, Beijing Forestry University, Tsinghua East Road Haidian District, Beijing, China. francis.martin@inrae.fr.
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.