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.

Architecture et Fonction des Macromolécules Biologiques CNRS Aix Marseille Univ 13009 Marseille France

Beijing Advanced Innovation Centre for Tree Breeding by Molecular Design Institute of Microbiology Beijing Forestry University Tsinghua East Road Haidian District Beijing China

Biology Department Clark University Lasry Center for Bioscience 950 Main Street Worcester MA 01610 USA

Chemical and Biological Processes Development Group Pacific Northwest National Laboratory Richland WA USA

Department Botany and Plant Pathology Oregon State University Corvallis OR USA

Department of Biological Sciences King Abdulaziz University Jeddah Saudi Arabia

Department of Biology Duke University Durham NC 27708 USA

Department of Biology McMaster University 1280 Main St West Hamilton ON L8S 4K1 Canada

Department of Forest Sciences University of Helsinki Helsinki Finland

Department of Key Laboratory The 2nd Affiliated Hospital of Kunming Medical University 374 Dian Mian Road Kunming 650101 Yunnan China

Department of Life Sciences and Systems Biology University of Torino Viale Mattioli 25 10125 Torino Italy

Department of Plant and Microbial Biology University of California Berkeley Berkeley CA USA

INRAE USC1408 Architecture et Fonction des Macromolécules Biologiques 13009 Marseille France

Institute of Mountain Science Faculty of Agriculture Shinshu University Minami minowa Kami ina Nagano 399 4598 Japan

Laboratoire de Recherche en Sciences Végétales Université de Toulouse CNRS UPS Toulouse France

Laboratory of Environmental Microbiology Institute of Microbiology of the Czech Academy of Sciences Videnska 1083 14220 Praha 4 Czech Republic

Natural History Museum University of Tartu 14a Ravila 50411 Tartu Estonia

Plant Soil and Microbial Sciences Michigan State University East Lansing MI 48824 USA

Swiss Federal Institute for Forest Snow and Landscape Research WSL Zuercherstrasse 111 8903 Birmensdorf Switzerland

Synthetic and Systems Biology Unit Biological Research Centre 6726 Szeged Hungary

The Jacob Blaustein Institutes for Desert Research Bergman Campus Ben Gurion University of The Negev Beer Sheva Israel

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

US Department of Energy Joint Genome Institute Lawrence Berkeley National Laboratory Berkeley CA USA

Westerdijk Fungal Biodiversity Institute Uppsalalaan 8 3584 CT Utrecht Netherlands

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