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Title: Pezizomycetes genomes reveal the molecular basis of ectomycorrhizal truffle lifestyle

Abstract

Tuberaceae is one of the most diverse lineages of symbiotic truffle-forming fungi. To understand the molecular underpinning of the ectomycorrhizal truffle lifestyle, we compared the genomes of Piedmont white truffle (Tuber magnatum), Périgord black truffle (Tuber melanosporum), Burgundy truffle (Tuber aestivum), pig truffle (Choiromyces venosus) and desert truffle (Terfezia boudieri) to saprotrophic Pezizomycetes. Reconstructed gene duplication/loss histories along a time-calibrated phylogeny of Ascomycetes revealed that Tuberaceae-specific traits may be related to a higher gene diversification rate. Genomic features in Tuber species appear to be very similar, with high transposon content, few genes coding lignocellulose-degrading enzymes, a substantial set of lineage-specific fruiting-body-upregulated genes and high expression of genes involved in volatile organic compound metabolism. Developmental and metabolic pathways expressed in ectomycorrhizae and fruiting bodies of T. magnatum and T. melanosporum are unexpectedly very similar, owing to the fact that they diverged ~100 Ma. Volatile organic compounds from pungent truffle odours are not the products of Tuber-specific gene innovations, but rely on the differential expression of an existing gene repertoire. These genomic resources will help to address fundamental questions in the evolution of the truffle lifestyle and the ecology of fungi that have been praised as food delicacies for centuries.

Authors:
 [1];  [1];  [2];  [3]; ORCiD logo [1];  [4];  [1];  [5]; ORCiD logo [6];  [2]; ORCiD logo [7];  [8]; ORCiD logo [7];  [3];  [9];  [1];  [3];  [3];  [1];  [2] more »; ORCiD logo [10];  [1]; ORCiD logo [3];  [3];  [11];  [6];  [12]; ORCiD logo [1];  [2];  [9];  [9];  [13];  [14];  [15];  [3];  [16];  [17];  [18]; ORCiD logo [9];  [15];  [7]; ORCiD logo [16];  [19];  [20]; ORCiD logo [5]; ORCiD logo [2];  [2]; ORCiD logo [21]; ORCiD logo [22]; ORCiD logo [23] « less
  1. Institut National de la Recherche Agronomique (INRA), Champenoux (France)
  2. Institut de Génomique, Evry (France)
  3. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  4. Institut National de la Recherche Agronomique (INRA), Champenoux (France); Chinese Academy of Medical Sciences & Peking Union Medical College, Beijing (China)
  5. Hungarian Academy of Sciences, Szeged (Hungary)
  6. National Research Council – Institute for Sustainable Plant Protection, Torino (Italy)
  7. Univ. of Parma (Italy)
  8. Aix-Marseille Univ., Marseille (France)
  9. CNR-IBBR, Perugia (Italy)
  10. Univ. of L’Aquila (italy)
  11. Commissariat a l'Energie Atomique et aux Energies Alternatives (CEA-Saclay), Gif-sur-Yvette (France)
  12. Centre National de la Recherche Scientifique (CNRS), Dijon (France); Univ. Montpellier (France)
  13. Ben-Gurion Univ. of The Negev, Beer-Sheva (Israel)
  14. Goethe Univ., Frankfurt (Germany)
  15. Ruhr Univ., Bochum (Germany)
  16. Inst. of Microbiology of the CAS, Praha (Czech Republic)
  17. Centre National de la Recherche Scientifique (CNRS), Dijon (France)
  18. Univ. of Bologna (Italy)
  19. Oregon State Univ., Corvallis, OR (United States)
  20. Aix-Marseille Univ., and CNRS, Marseille (France); King Abdulaziz Univ., Jeddah (Saudi Arabia)
  21. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of California, Berkeley, CA (United States)
  22. Univ. of Torino (Italy)
  23. Institut National de la Recherche Agronomique (INRA), Champenoux (France); Beijing Forestry Univ., Beijing (China)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1546631
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Nature Ecology and Evolution
Additional Journal Information:
Journal Volume: 2; Journal Issue: 12; Journal ID: ISSN 2397-334X
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Murat, Claude, Payen, Thibaut, Noel, Benjamin, Kuo, Alan, Morin, Emmanuelle, Chen, Juan, Kohler, Annegret, Krizsán, Krisztina, Balestrini, Raffaella, Da Silva, Corinne, Montanini, Barbara, Hainaut, Mathieu, Levati, Elisabetta, Barry, Kerrie W., Belfiori, Beatrice, Cichocki, Nicolas, Clum, Alicia, Dockter, Rhyan B., Fauchery, Laure, Guy, Julie, Iotti, Mirco, Le Tacon, François, Lindquist, Erika A., Lipzen, Anna, Malagnac, Fabienne, Mello, Antonietta, Molinier, Virginie, Miyauchi, Shingo, Poulain, Julie, Riccioni, Claudia, Rubini, Andrea, Sitrit, Yaron, Splivallo, Richard, Traeger, Stefanie, Wang, Mei, Žifčáková, Lucia, Wipf, Daniel, Zambonelli, Alessandra, Paolocci, Francesco, Nowrousian, Minou, Ottonello, Simone, Baldrian, Petr, Spatafora, Joseph W., Henrissat, Bernard, Nagy, Laszlo G., Aury, Jean-Marc, Wincker, Patrick, Grigoriev, Igor V., Bonfante, Paola, and Martin, Francis M. Pezizomycetes genomes reveal the molecular basis of ectomycorrhizal truffle lifestyle. United States: N. p., 2018. Web. doi:10.1038/s41559-018-0710-4.
Murat, Claude, Payen, Thibaut, Noel, Benjamin, Kuo, Alan, Morin, Emmanuelle, Chen, Juan, Kohler, Annegret, Krizsán, Krisztina, Balestrini, Raffaella, Da Silva, Corinne, Montanini, Barbara, Hainaut, Mathieu, Levati, Elisabetta, Barry, Kerrie W., Belfiori, Beatrice, Cichocki, Nicolas, Clum, Alicia, Dockter, Rhyan B., Fauchery, Laure, Guy, Julie, Iotti, Mirco, Le Tacon, François, Lindquist, Erika A., Lipzen, Anna, Malagnac, Fabienne, Mello, Antonietta, Molinier, Virginie, Miyauchi, Shingo, Poulain, Julie, Riccioni, Claudia, Rubini, Andrea, Sitrit, Yaron, Splivallo, Richard, Traeger, Stefanie, Wang, Mei, Žifčáková, Lucia, Wipf, Daniel, Zambonelli, Alessandra, Paolocci, Francesco, Nowrousian, Minou, Ottonello, Simone, Baldrian, Petr, Spatafora, Joseph W., Henrissat, Bernard, Nagy, Laszlo G., Aury, Jean-Marc, Wincker, Patrick, Grigoriev, Igor V., Bonfante, Paola, & Martin, Francis M. Pezizomycetes genomes reveal the molecular basis of ectomycorrhizal truffle lifestyle. United States. doi:10.1038/s41559-018-0710-4.
Murat, Claude, Payen, Thibaut, Noel, Benjamin, Kuo, Alan, Morin, Emmanuelle, Chen, Juan, Kohler, Annegret, Krizsán, Krisztina, Balestrini, Raffaella, Da Silva, Corinne, Montanini, Barbara, Hainaut, Mathieu, Levati, Elisabetta, Barry, Kerrie W., Belfiori, Beatrice, Cichocki, Nicolas, Clum, Alicia, Dockter, Rhyan B., Fauchery, Laure, Guy, Julie, Iotti, Mirco, Le Tacon, François, Lindquist, Erika A., Lipzen, Anna, Malagnac, Fabienne, Mello, Antonietta, Molinier, Virginie, Miyauchi, Shingo, Poulain, Julie, Riccioni, Claudia, Rubini, Andrea, Sitrit, Yaron, Splivallo, Richard, Traeger, Stefanie, Wang, Mei, Žifčáková, Lucia, Wipf, Daniel, Zambonelli, Alessandra, Paolocci, Francesco, Nowrousian, Minou, Ottonello, Simone, Baldrian, Petr, Spatafora, Joseph W., Henrissat, Bernard, Nagy, Laszlo G., Aury, Jean-Marc, Wincker, Patrick, Grigoriev, Igor V., Bonfante, Paola, and Martin, Francis M. Mon . "Pezizomycetes genomes reveal the molecular basis of ectomycorrhizal truffle lifestyle". United States. doi:10.1038/s41559-018-0710-4. https://www.osti.gov/servlets/purl/1546631.
@article{osti_1546631,
title = {Pezizomycetes genomes reveal the molecular basis of ectomycorrhizal truffle lifestyle},
author = {Murat, Claude and Payen, Thibaut and Noel, Benjamin and Kuo, Alan and Morin, Emmanuelle and Chen, Juan and Kohler, Annegret and Krizsán, Krisztina and Balestrini, Raffaella and Da Silva, Corinne and Montanini, Barbara and Hainaut, Mathieu and Levati, Elisabetta and Barry, Kerrie W. and Belfiori, Beatrice and Cichocki, Nicolas and Clum, Alicia and Dockter, Rhyan B. and Fauchery, Laure and Guy, Julie and Iotti, Mirco and Le Tacon, François and Lindquist, Erika A. and Lipzen, Anna and Malagnac, Fabienne and Mello, Antonietta and Molinier, Virginie and Miyauchi, Shingo and Poulain, Julie and Riccioni, Claudia and Rubini, Andrea and Sitrit, Yaron and Splivallo, Richard and Traeger, Stefanie and Wang, Mei and Žifčáková, Lucia and Wipf, Daniel and Zambonelli, Alessandra and Paolocci, Francesco and Nowrousian, Minou and Ottonello, Simone and Baldrian, Petr and Spatafora, Joseph W. and Henrissat, Bernard and Nagy, Laszlo G. and Aury, Jean-Marc and Wincker, Patrick and Grigoriev, Igor V. and Bonfante, Paola and Martin, Francis M.},
abstractNote = {Tuberaceae is one of the most diverse lineages of symbiotic truffle-forming fungi. To understand the molecular underpinning of the ectomycorrhizal truffle lifestyle, we compared the genomes of Piedmont white truffle (Tuber magnatum), Périgord black truffle (Tuber melanosporum), Burgundy truffle (Tuber aestivum), pig truffle (Choiromyces venosus) and desert truffle (Terfezia boudieri) to saprotrophic Pezizomycetes. Reconstructed gene duplication/loss histories along a time-calibrated phylogeny of Ascomycetes revealed that Tuberaceae-specific traits may be related to a higher gene diversification rate. Genomic features in Tuber species appear to be very similar, with high transposon content, few genes coding lignocellulose-degrading enzymes, a substantial set of lineage-specific fruiting-body-upregulated genes and high expression of genes involved in volatile organic compound metabolism. Developmental and metabolic pathways expressed in ectomycorrhizae and fruiting bodies of T. magnatum and T. melanosporum are unexpectedly very similar, owing to the fact that they diverged ~100 Ma. Volatile organic compounds from pungent truffle odours are not the products of Tuber-specific gene innovations, but rely on the differential expression of an existing gene repertoire. These genomic resources will help to address fundamental questions in the evolution of the truffle lifestyle and the ecology of fungi that have been praised as food delicacies for centuries.},
doi = {10.1038/s41559-018-0710-4},
journal = {Nature Ecology and Evolution},
number = 12,
volume = 2,
place = {United States},
year = {2018},
month = {11}
}

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    Works referencing / citing this record:

    Orchard Conditions and Fruiting Body Characteristics Drive the Microbiome of the Black Truffle Tuber aestivum
    journal, June 2019

    • Splivallo, Richard; Vahdatzadeh, Maryam; Maciá-Vicente, Jose G.
    • Frontiers in Microbiology, Vol. 10
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