Large-scale genome sequencing of mycorrhizal fungi provides insights into the early evolution of symbiotic traits
Shingo Miyauchi, Enikö Kiss, Alan Kuo, Élodie Drula, Annegret Kohler, Marisol Sánchez‐García, Emmanuelle Morin, Bill Andreopoulos, Kerrie Barry, Gregory Bonito, Marc Buée, Akiko Carver, Cindy Chen, Nicolas Cichocki, Alicia Clum, David Culley, P.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 J. Szöllősi, Lucia Žifčáková, Martina Štursová, Joseph W. Spatafora, Leho Tedersoo, Lu‐Min Vaario, Akiyoshi Yamada, Mi Yan, Pengfei Wang, Jianping Xu, Tom Bruns, Petr Baldrián, Rytas Vilgalys, Christophe Dunand, Bernard Henrissat, Igor V. Grigoriev, David S. Hibbett, László G. Nagy, Francis Martin
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.