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

Shingo Miyauchi; Enikő Kiss; Alan Kuo; Elodie Drula; Annegret Kohler; Marisol Sánchez-García; Emmanuelle Morin; Bill Andreopoulos; Kerrie W. Barry; Gregory Bonito; Marc Buée; Akiko Carver; Cindy Chen; Nicolas Cichocki; Alicia Clum; David Culley; Pedro 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 Szöllősi; Lucia Žifčáková; Martina Štursová; Joseph W. Spatafora; Leho Tedersoo; Lu-Min Vaario; Akiyoshi Yamada; Mi Yan; Pengfei Wang; Jianping Xu; Tom Bruns; Petr Baldrian; Rytas Vilgalys; Christophe Dunand; Bernard Henrissat; Igor V. Grigoriev; David Hibbett; László G. Nagy; Francis M. Martin

doi:10.1038/s41467-020-18795-w

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

Shingo Miyauchi, Enikő Kiss, Alan Kuo, Elodie Drula, Annegret Kohler, Marisol Sánchez-García, Emmanuelle Morin, Bill Andreopoulos, Kerrie W. Barry, Gregory Bonito, Marc Buée, Akiko Carver, Cindy Chen, Nicolas Cichocki, Alicia Clum, David Culley, Pedro W. Crous, Laure Fauchery, Mariangela Girlanda, Richard D. HayesZsófia 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 Szöllősi, Lucia Žifčáková, Martina Štursová, Joseph W. Spatafora, Leho Tedersoo, Lu-Min Vaario, Akiyoshi Yamada, Mi Yan, Pengfei Wang, Jianping Xu, Tom Bruns, Petr Baldrian, Rytas Vilgalys, Christophe Dunand, Bernard Henrissat, Igor V. Grigoriev, David Hibbett, László G. Nagy, Francis M. Martin

Research output: Contribution to journal/periodical › Article › Scientific › peer-review

301 Citations (Scopus)

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.

Original language	English
Journal	Nature Communications
Volume	11
Issue number	1
DOIs	https://doi.org/10.1038/s41467-020-18795-w
Publication status	Published - Oct 2020

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Miyauchi, S., Kiss, E., Kuo, A., Drula, E., Kohler, A., Sánchez-García, M., Morin, E., Andreopoulos, B., Barry, K. W., Bonito, G., Buée, M., Carver, A., Chen, C., Cichocki, N., Clum, A., Culley, D., Crous, P. W., Fauchery, L., Girlanda, M., ... Martin, F. M. (2020). Large-scale genome sequencing of mycorrhizal fungi provides insights into the early evolution of symbiotic traits. Nature Communications, 11(1). https://doi.org/10.1038/s41467-020-18795-w

@article{b8fb5515ec824ae6b40f88a201530414,

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

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.",

author = "Shingo Miyauchi and Enik{\H o} Kiss and Alan Kuo and Elodie Drula and Annegret Kohler and Marisol S{\'a}nchez-Garc{\'i}a and Emmanuelle Morin and Bill Andreopoulos and Barry, {Kerrie W.} and Gregory Bonito and Marc Bu{\'e}e and Akiko Carver and Cindy Chen and Nicolas Cichocki and Alicia Clum and David Culley and Crous, {Pedro W.} and Laure Fauchery and Mariangela Girlanda and Hayes, {Richard D.} and Zs{\'o}fia K{\'e}ri and Kurt LaButti and Anna Lipzen and Vincent Lombard and Jon Magnuson and Fran{\c c}ois Maillard and Claude Murat and Matt Nolan and Ohm, {Robin A.} and Jasmyn Pangilinan and Pereira, {Ma{\'i}ra de Freitas} and Silvia Perotto and Martina Peter and Stephanie Pfister and Robert Riley and Yaron Sitrit and Stielow, {J. Benjamin} and Gergely Sz{\"o}ll{\H o}si and Lucia {\v Z}if{\v c}{\'a}kov{\'a} and Martina {\v S}tursov{\'a} and Spatafora, {Joseph W.} and Leho Tedersoo and Lu-Min Vaario and Akiyoshi Yamada and Mi Yan and Pengfei Wang and Jianping Xu and Tom Bruns and Petr Baldrian and Rytas Vilgalys and Christophe Dunand and Bernard Henrissat and Grigoriev, {Igor V.} and David Hibbett and Nagy, {L{\'a}szl{\'o} G.} and Martin, {Francis M.}",

year = "2020",

month = oct,

doi = "10.1038/s41467-020-18795-w",

language = "English",

volume = "11",

journal = "Nature Communications",

issn = "2041-1723",

publisher = "Nature Publishing Group",

number = "1",

}

Miyauchi, S, Kiss, E, Kuo, A, Drula, E, Kohler, A, Sánchez-García, M, Morin, E, Andreopoulos, B, Barry, KW, Bonito, G, Buée, M, Carver, A, Chen, C, Cichocki, N, Clum, A, Culley, D, Crous, PW, Fauchery, L, Girlanda, M, Hayes, RD, Kéri, Z, LaButti, K, Lipzen, A, Lombard, V, Magnuson, J, Maillard, F, Murat, C, Nolan, M, Ohm, RA, Pangilinan, J, Pereira, MDF, Perotto, S, Peter, M, Pfister, S, Riley, R, Sitrit, Y, Stielow, JB, Szöllősi, G, Žifčáková, L, Štursová, M, Spatafora, JW, Tedersoo, L, Vaario, L-M, Yamada, A, Yan, M, Wang, P, Xu, J, Bruns, T, Baldrian, P, Vilgalys, R, Dunand, C, Henrissat, B, Grigoriev, IV, Hibbett, D, Nagy, LG & Martin, FM 2020, 'Large-scale genome sequencing of mycorrhizal fungi provides insights into the early evolution of symbiotic traits', Nature Communications, vol. 11, no. 1. https://doi.org/10.1038/s41467-020-18795-w

TY - JOUR

T1 - Large-scale genome sequencing of mycorrhizal fungi provides insights into the early evolution of symbiotic traits

AU - Miyauchi, Shingo

AU - Kiss, Enikő

AU - Kuo, Alan

AU - Drula, Elodie

AU - Kohler, Annegret

AU - Sánchez-García, Marisol

AU - Morin, Emmanuelle

AU - Andreopoulos, Bill

AU - Barry, Kerrie W.

AU - Bonito, Gregory

AU - Buée, Marc

AU - Carver, Akiko

AU - Chen, Cindy

AU - Cichocki, Nicolas

AU - Clum, Alicia

AU - Culley, David

AU - Crous, Pedro W.

AU - Fauchery, Laure

AU - Girlanda, Mariangela

AU - Hayes, Richard D.

AU - Kéri, Zsófia

AU - LaButti, Kurt

AU - Lipzen, Anna

AU - Lombard, Vincent

AU - Magnuson, Jon

AU - Maillard, François

AU - Murat, Claude

AU - Nolan, Matt

AU - Ohm, Robin A.

AU - Pangilinan, Jasmyn

AU - Pereira, Maíra de Freitas

AU - Perotto, Silvia

AU - Peter, Martina

AU - Pfister, Stephanie

AU - Riley, Robert

AU - Sitrit, Yaron

AU - Stielow, J. Benjamin

AU - Szöllősi, Gergely

AU - Žifčáková, Lucia

AU - Štursová, Martina

AU - Spatafora, Joseph W.

AU - Tedersoo, Leho

AU - Vaario, Lu-Min

AU - Yamada, Akiyoshi

AU - Yan, Mi

AU - Wang, Pengfei

AU - Xu, Jianping

AU - Bruns, Tom

AU - Baldrian, Petr

AU - Vilgalys, Rytas

AU - Dunand, Christophe

AU - Henrissat, Bernard

AU - Grigoriev, Igor V.

AU - Hibbett, David

AU - Nagy, László G.

AU - Martin, Francis M.

PY - 2020/10

Y1 - 2020/10

N2 - 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.

AB - 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.

U2 - 10.1038/s41467-020-18795-w

DO - 10.1038/s41467-020-18795-w

M3 - Article

SN - 2041-1723

VL - 11

JO - Nature Communications

JF - Nature Communications

IS - 1

ER -

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

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