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

Shingo Miyauchi (1) , Enikő Kiss (2) , Alan Kuo (3) , Elodie Drula (4) , Annegret Kohler (1) , Marisol Sánchez-García (5) , Emmanuelle Morin (1) , Bill Andreopoulos (3) , Kerrie Barry (6) , Gregory Bonito (7) , Marc Buée (1) , Akiko Carver (3) , Cindy Chen (3) , Nicolas Cichocki (1) , Alicia Clum (3) , David Culley (8) , Pedro Crous (9) , Laure Fauchery (1) , Mariangela Girlanda (10) , Richard Hayes (3) , Zsófia Kéri (2) , Kurt Labutti (3) , Anna Lipzen (3) , Vincent Lombard (4) , Jon Magnuson (8) , François Maillard (1) , Claude C. Murat (1) , Matt Nolan (3) , Robin Ohm (3) , Jasmyn Pangilinan (3) , Maíra de Freitas Pereira (1) , Silvia Perotto (10) , Martina Peter (11) , Stephanie Pfister (11) , Robert Riley (3) , Yaron Sitrit (12) , J. Benjamin Stielow (9) , Gergely Szöllősi (2) , Lucia Žifčáková (13) , Martina Štursová (13) , Joseph Spatafora (14) , Leho Tedersoo (15) , Lu-Min Vaario (16) , Akiyoshi Yamada (17) , Mi Yan (3) , Pengfei Wang (18) , Jianping Xu (19) , Tom Bruns (20) , Petr Baldrian (13) , Rytas Vilgalys (21) , Christophe Dunand (22) , Bernard Henrissat (23, 4) , Igor Grigoriev (3) , David Hibbett (5) , László Nagy (2) , Francis M. Martin (1, 24)

1 IAM - Interactions Arbres-Microorganismes
2 Synthetic and Systems Biology Unit [Szeged]
3 DOE - Department of Energy / Joint Genome Institute
4 AFMB - Architecture et fonction des macromolécules biologiques
5 Clark University
6 LBNL - Lawrence Berkeley National Laboratory [Berkeley]
7 Michigan State University [East Lansing]
8 PNNL - Pacific Northwest National Laboratory
9 WI - Westerdijk Fungal Biodiversity Institute [Utrecht]
10 UNITO - Università degli studi di Torino = University of Turin
11 Swiss Federal Institute for Forest, Snow and Landscape Research WSL
12 BGU - Ben-Gurion University of the Negev
13 MBU / CAS - Institute of Microbiology of the Czech Academy of Sciences [Prague, Czech Republic]
14 OSU - Oregon State University
15 Institute of Computer Science [University of Tartu, Estonie]
16 Helsingin yliopisto = Helsingfors universitet = University of Helsinki
17 Shinshu University Hospital
18 KMU - Kunming Medical University
19 McMaster University [Hamilton, Ontario]
20 Department of Plant and Microbial Biology [Berkeley]
21 Duke University [Durham]
22 Dynamique et Evolution des Parois cellulaires végétales
23 King Abdulaziz University
24 Beijing Forestry University

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.

Domaines: Sciences de l'environnement; Sciences du Vivant [q-bio]

Shingo Miyauchi, Enikő Kiss, Alan Kuo, Elodie Drula, Annegret Kohler, et al.. Large-scale genome sequencing of mycorrhizal fungi provides insights into the early evolution of symbiotic traits. Nature Communications, 2020, 11 (1), ⟨10.1038/s41467-020-18795-w⟩. ⟨hal-03082507⟩