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

Miyauchi, Shingo; Kiss, Enikő; Kuo, Alan; Drula, Elodie; Kohler, Annegret; Sánchez-García, Marisol; Morin, Emmanuelle; Andreopoulos, Bill; Barry, Kerrie W.; Bonito, Gregory; Buée, Marc; Carver, Akiko; Chen, Cindy; Cichocki, Nicolas; Clum, Alicia; Culley, David; Crous, Pedro W.; Fauchery, Laure; Girlanda, Mariangela; Hayes, Richard D.; Kéri, Zsófia; LaButti, Kurt; Lipzen, Anna; Lombard, Vincent; Magnuson, Jon; Maillard, François; Murat, Claude; Nolan, Matt; Ohm, Robin A.; Pangilinan, Jasmyn; de Freitas Pereira, Maíra; Perotto, Silvia; Peter, Martina; Pfister, Stephanie; Riley, Robert; Sitrit, Yaron; Stielow, J. Benjamin; Szöllősi, Gergely; Žifčáková, Lucia; Štursová, Martina; Spatafora, Joseph W.; Tedersoo, Leho; Vaario, Lu-Min; Yamada, Akiyoshi; Yan, Mi; Wang, Pengfei; Xu, Jianping; Bruns, Tom; Baldrian, Petr; Vilgalys, Rytas; Dunand, Christophe; Henrissat, Bernard; Grigoriev, Igor V.; Hibbett, David; Nagy, László G.; Martin, Francis M.

doi:10.1038/s41467-020-18795-w

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

Journal Article · Mon Oct 12 00:00:00 EDT 2020 · Nature Communications

DOI:https://doi.org/10.1038/s41467-020-18795-w· OSTI ID:1713294

^[1]; Kiss, Enikő ^[2]; Kuo, Alan ^[3]; Drula, Elodie ^[4]; Kohler, Annegret ^[1]; Sánchez-García, Marisol ^[5]; Morin, Emmanuelle ^[1]; Andreopoulos, Bill ^[3]; Barry, Kerrie W. ^[3]; Bonito, Gregory ^[6]; Buée, Marc ^[1]; Carver, Akiko ^[3]; Chen, Cindy ^[3]; Cichocki, Nicolas ^[1]; Clum, Alicia ^[3]; Culley, David ^[7]; Crous, Pedro W. ^[8]; ^[1]; Girlanda, Mariangela ^[9]; ^[3] more »

Univ. of Lorraine, Champenoux (France)
Biological Research Centre, Szeged (Hungary)
USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Architecture et Fonction des Macromolecules Biologiques, Marseille (France)
Clark Univ., Worcester, MA (United States)
Michigan State Univ., East Lansing, MI (United States)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Westerdijk Fungal Biodiversity Inst., Utrecht (Netherlands)
Univ. of Torino (Italy)
Swiss Federal Inst. for Forest, Snow and Landscape Research, Birmensdorf (Switzerland)
Ben-Gurion Univ. of The Negev (Israel)
Czech Academy of Sciences, Prague (Czech Republic)
Oregon State Univ., Corvallis, OR (United States)
Univ. of Tartu (Estonia)
Univ. of Helsinki (Finland)
Shinshu Univ., Nagano (Japan)
Kunming Medical Univ., Yunnan (China)
McMaster Univ., Hamilton, ON (Canada)
Univ. of California, Berkeley, CA (United States)
Duke Univ., Durham, NC (United States)
Univ. of Toulouse (France); National Centre for Scientific Research (CNRS), Toulouse (France)
Architecture et Fonction des Macromolecules Biologiques, Marseille (France); King Abdulaziz Univ., Jeddah (Saudi Arabia)
USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States)
Univ. of Lorraine, Champenoux (France); Beijing Forestry Univ. (China)

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.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); Laboratory of Excellence ARBRE; Hungarian Academy of Sciences; National Research, Development and Innovation; European Research Council (ERC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1713294

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 11; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Additional file 3 of Disease-induced changes in plant microbiome assembly and functional adaptation Gao, Min; Xiong, Chao; Gao, Cheng figshare https://doi.org/10.6084/m9.figshare.16625387.v1	dataset	January 2021
Additional file 1 of Whole genome sequencing and analysis of Armillaria gallica Jzi34 symbiotic with Gastrodia elata Cai, Jinlong; Muhammad, Ikram; Chen, Bilian figshare https://doi.org/10.6084/m9.figshare.23084013.v1	dataset	January 2023
Additional file 1 of Evolutionary history of arbuscular mycorrhizal fungi and genomic signatures of obligate symbiosis Rosling, Anna; Eshghi Sahraei, Shadi; Kalsoom Khan, Faheema figshare https://doi.org/10.6084/m9.figshare.25929209	dataset	January 2024

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