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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.

Authors:
ORCiD logo [1];  [2];  [3];  [4];  [1];  [5];  [1];  [3];  [3];  [6];  [1];  [3];  [3];  [1];  [3];  [7];  [8]; ORCiD logo [1];  [9]; ORCiD logo [3] more »;  [2]; ORCiD logo [3];  [3];  [4]; ORCiD logo [7];  [1]; ORCiD logo [1];  [3];  [3];  [3];  [1]; ORCiD logo [9];  [10];  [10];  [3];  [11];  [8]; ORCiD logo [2];  [12];  [12];  [13];  [14];  [15];  [16];  [3];  [17]; ORCiD logo [18];  [19]; ORCiD logo [12]; ORCiD logo [20];  [21]; ORCiD logo [22]; ORCiD logo [23];  [5];  [2];  [24] « less
  1. Univ. of Lorraine, Champenoux (France)
  2. Biological Research Centre, Szeged (Hungary)
  3. USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  4. Architecture et Fonction des Macromolecules Biologiques, Marseille (France)
  5. Clark Univ., Worcester, MA (United States)
  6. Michigan State Univ., East Lansing, MI (United States)
  7. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  8. Westerdijk Fungal Biodiversity Inst., Utrecht (Netherlands)
  9. Univ. of Torino (Italy)
  10. Swiss Federal Inst. for Forest, Snow and Landscape Research, Birmensdorf (Switzerland)
  11. Ben-Gurion Univ. of The Negev (Israel)
  12. Czech Academy of Sciences, Prague (Czech Republic)
  13. Oregon State Univ., Corvallis, OR (United States)
  14. Univ. of Tartu (Estonia)
  15. Univ. of Helsinki (Finland)
  16. Shinshu Univ., Nagano (Japan)
  17. Kunming Medical Univ., Yunnan (China)
  18. McMaster Univ., Hamilton, ON (Canada)
  19. Univ. of California, Berkeley, CA (United States)
  20. Duke Univ., Durham, NC (United States)
  21. Univ. of Toulouse (France); National Centre for Scientific Research (CNRS), Toulouse (France)
  22. Architecture et Fonction des Macromolecules Biologiques, Marseille (France); King Abdulaziz Univ., Jeddah (Saudi Arabia)
  23. 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)
  24. Univ. of Lorraine, Champenoux (France); Beijing Forestry Univ. (China)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
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)
OSTI Identifier:
1713294
Grant/Contract Number:  
AC02-05CH11231; ANR11-LABX-0002-01; LP2019/13-2019; GINOP-2.3.2-15-2016-00052; 714774; GINOP-2.3.2.-15-2016-00057
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 11; Journal Issue: 1; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

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., and Martin, Francis M.. Large-scale genome sequencing of mycorrhizal fungi provides insights into the early evolution of symbiotic traits. United States: N. p., 2020. Web. https://doi.org/10.1038/s41467-020-18795-w.
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.. Large-scale genome sequencing of mycorrhizal fungi provides insights into the early evolution of symbiotic traits. United States. https://doi.org/10.1038/s41467-020-18795-w
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., and Martin, Francis M.. Mon . "Large-scale genome sequencing of mycorrhizal fungi provides insights into the early evolution of symbiotic traits". United States. https://doi.org/10.1038/s41467-020-18795-w. https://www.osti.gov/servlets/purl/1713294.
@article{osti_1713294,
title = {Large-scale genome sequencing of mycorrhizal fungi provides insights into the early evolution of symbiotic traits},
author = {Miyauchi, Shingo and Kiss, Enikő and Kuo, Alan and Drula, Elodie and Kohler, Annegret and Sánchez-García, Marisol and Morin, Emmanuelle and Andreopoulos, Bill and Barry, Kerrie W. and Bonito, Gregory and Buée, Marc and Carver, Akiko and Chen, Cindy and Cichocki, Nicolas and Clum, Alicia and Culley, David and Crous, Pedro W. and Fauchery, Laure and Girlanda, Mariangela and Hayes, Richard D. and Kéri, Zsófia and LaButti, Kurt and Lipzen, Anna and Lombard, Vincent and Magnuson, Jon and Maillard, François and Murat, Claude and Nolan, Matt and Ohm, Robin A. and Pangilinan, Jasmyn and de Freitas Pereira, Maíra and Perotto, Silvia and Peter, Martina and Pfister, Stephanie and Riley, Robert and Sitrit, Yaron and Stielow, J. Benjamin and Szöllősi, Gergely and Žifčáková, Lucia and Štursová, Martina and Spatafora, Joseph W. and Tedersoo, Leho and Vaario, Lu-Min and Yamada, Akiyoshi and Yan, Mi and Wang, Pengfei and Xu, Jianping and Bruns, Tom and Baldrian, Petr and Vilgalys, Rytas and Dunand, Christophe and Henrissat, Bernard and Grigoriev, Igor V. and Hibbett, David and Nagy, László G. and Martin, Francis M.},
abstractNote = {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.},
doi = {10.1038/s41467-020-18795-w},
journal = {Nature Communications},
number = 1,
volume = 11,
place = {United States},
year = {2020},
month = {10}
}

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Signs of sex: what we know and how we know it
journal, April 2009

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MycoCosm portal: gearing up for 1000 fungal genomes
journal, December 2013

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A phylostratigraphy approach to uncover the genomic history of major adaptations in metazoan lineages
journal, November 2007

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Out of the Palaeotropics? Historical biogeography and diversification of the cosmopolitan ectomycorrhizal mushroom family Inocybaceae
journal, April 2009


Unearthing the roots of ectomycorrhizal symbioses
journal, October 2016

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