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:
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[1];
[6];
[7];
[7];
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- Institut National de la Recherche Agronomique (INRA), Champenoux (France)
- Institut de Génomique, Evry (France)
- USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
- Institut National de la Recherche Agronomique (INRA), Champenoux (France); Chinese Academy of Medical Sciences & Peking Union Medical College, Beijing (China)
- Hungarian Academy of Sciences, Szeged (Hungary)
- National Research Council – Institute for Sustainable Plant Protection, Torino (Italy)
- Univ. of Parma (Italy)
- Aix-Marseille Univ., Marseille (France)
- CNR-IBBR, Perugia (Italy)
- Univ. of L’Aquila (italy)
- Commissariat a l'Energie Atomique et aux Energies Alternatives (CEA-Saclay), Gif-sur-Yvette (France)
- Centre National de la Recherche Scientifique (CNRS), Dijon (France); Univ. Montpellier (France)
- Ben-Gurion Univ. of The Negev, Beer-Sheva (Israel)
- Goethe Univ., Frankfurt (Germany)
- Ruhr Univ., Bochum (Germany)
- Inst. of Microbiology of the CAS, Praha (Czech Republic)
- Centre National de la Recherche Scientifique (CNRS), Dijon (France)
- Univ. of Bologna (Italy)
- Oregon State Univ., Corvallis, OR (United States)
- Aix-Marseille Univ., and CNRS, Marseille (France); King Abdulaziz Univ., Jeddah (Saudi Arabia)
- USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of California, Berkeley, CA (United States)
- Univ. of Torino (Italy)
- 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. https://doi.org/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. https://doi.org/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 referenced in this record:
Rapid incorporation of carbon from ectomycorrhizal mycelial necromass into soil fungal communities
journal, June 2012
- Drigo, B.; Anderson, I. C.; Kannangara, G. S. K.
- Soil Biology and Biochemistry, Vol. 49
Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages
journal, September 2009
- Tedersoo, Leho; May, Tom W.; Smith, Matthew E.
- Mycorrhiza, Vol. 20, Issue 4
Molecular Phylogeny of Truffles (Pezizales: Terfeziaceae, Tuberaceae) Derived from Nuclear rDNA Sequence Analysis
journal, October 1999
- Percudani, Riccardo; Trevisi, Aurelio; Zambonelli, Alessandra
- Molecular Phylogenetics and Evolution, Vol. 13, Issue 1
Laser microdissection and microarray analysis of Tuber melanosporum ectomycorrhizas reveal functional heterogeneity between mantle and Hartig net compartments : Functional heterogeneity within ectomycorrhizas
journal, February 2013
- Hacquard, Stéphane; Tisserant, Emilie; Brun, Annick
- Environmental Microbiology, Vol. 15, Issue 6
Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists
journal, February 2015
- Kohler, Annegret; Kuo, Alan; Nagy, Laszlo G.
- Nature Genetics, Vol. 47, Issue 4
Certainties and uncertainties about the life cycle of the Périgord black truffle (Tuber melanosporum Vittad.)
journal, March 2016
- Le Tacon, François; Rubini, Andrea; Murat, Claude
- Annals of Forest Science, Vol. 73, Issue 1
Mycorrhizal vs saprotrophic status of fungi: the isotopic evidence
journal, June 2001
- Hobbie, Erik A.; Weber, Nancy S.; Trappe, James M.
- New Phytologist, Vol. 150, Issue 3
Truffle volatiles: from chemical ecology to aroma biosynthesis: Research review
journal, November 2010
- Splivallo, Richard; Ottonello, Simone; Mello, Antonietta
- New Phytologist, Vol. 189, Issue 3
Genomic evidence of repeat-induced point mutation (RIP) in filamentous ascomycetes
journal, March 2011
- John Clutterbuck, A.
- Fungal Genetics and Biology, Vol. 48, Issue 3
Phylogenetic relationships among ascomycetous truffles and the true and false morels inferred from 18S and 28S ribosomal DNA sequence analysis
journal, January 1997
- O'Donnell, Kerry; Cigelnik, Elizabeth; Weber, Nancy S.
- Mycologia, Vol. 89, Issue 1
Clustering of multiple transgene integrations in highly-unstable Ascobolus immersus transformants
journal, October 1994
- Rhounim, La�la; Gr�goire, Annie; Salama, Salah
- Current Genetics, Vol. 26, Issue 4
Assembly and ecological function of the root microbiome across angiosperm plant species
journal, January 2018
- Fitzpatrick, Connor R.; Copeland, Julia; Wang, Pauline W.
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 6
Truffles: much more than a prized and local fungal delicacy
journal, July 2006
- Mello, Antonietta; Murat, Claude; Bonfante, Paola
- FEMS Microbiology Letters, Vol. 260, Issue 1
High-quality draft assemblies of mammalian genomes from massively parallel sequence data
journal, December 2010
- Gnerre, S.; MacCallum, I.; Przybylski, D.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 4
The evolutionary origin of orphan genes
journal, August 2011
- Tautz, Diethard; Domazet-Lošo, Tomislav
- Nature Reviews Genetics, Vol. 12, Issue 10
Helianthemum-Terfezia relations in different growth media
journal, February 1990
- Roth-Bejerano, N.; Livne, D.; Kagan-Zur, V.
- New Phytologist, Vol. 114, Issue 2
Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis
journal, March 2010
- Martin, Francis; Kohler, Annegret; Murat, Claude
- Nature, Vol. 464, Issue 7291
BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs
journal, June 2015
- Simão, Felipe A.; Waterhouse, Robert M.; Ioannidis, Panagiotis
- Bioinformatics, Vol. 31, Issue 19
Non-exhaustive DNA methylation-mediated transposon silencing in the black truffle genome, a complex fungal genome with massive repeat element content
journal, July 2014
- Montanini, Barbara; Chen, Pao-Yang; Morselli, Marco
- Genome Biology, Vol. 15, Issue 8
Historical Biogeography and Diversification of Truffles in the Tuberaceae and Their Newly Identified Southern Hemisphere Sister Lineage
journal, January 2013
- Bonito, Gregory; Smith, Matthew E.; Nowak, Michael
- PLoS ONE, Vol. 8, Issue 1
The role of pre-symbiotic auxin signaling in ectendomycorrhiza formation between the desert truffle Terfezia boudieri and Helianthemum sessiliflorum
journal, November 2015
- Turgeman, Tidhar; Lubinsky, Olga; Roth-Bejerano, Nurit
- Mycorrhiza, Vol. 26, Issue 4
MycoCosm portal: gearing up for 1000 fungal genomes
journal, December 2013
- Grigoriev, Igor V.; Nikitin, Roman; Haridas, Sajeet
- Nucleic Acids Research, Vol. 42, Issue D1
Dating the Diversification of the Major Lineages of Ascomycota (Fungi)
journal, June 2013
- Prieto, María; Wedin, Mats
- PLoS ONE, Vol. 8, Issue 6
The Genome and Development-Dependent Transcriptomes of Pyronema confluens: A Window into Fungal Evolution
journal, September 2013
- Traeger, Stefanie; Altegoer, Florian; Freitag, Michael
- PLoS Genetics, Vol. 9, Issue 9
The Role of the Microbiome of Truffles in Aroma Formation: a Meta-Analysis Approach
journal, July 2015
- Vahdatzadeh, Maryam; Deveau, Aurélie; Splivallo, Richard
- Applied and Environmental Microbiology, Vol. 81, Issue 20
Whole genome comparative analysis of transposable elements provides new insight into mechanisms of their inactivation in fungal genomes
journal, February 2015
- Amselem, Joëlle; Lebrun, Marc-Henri; Quesneville, Hadi
- BMC Genomics, Vol. 16, Issue 1
Ectomycorrhizal ecology is imprinted in the genome of the dominant symbiotic fungus Cenococcum geophilum
journal, September 2016
- Peter, Martina; Kohler, Annegret; Ohm, Robin A.
- Nature Communications, Vol. 7, Issue 1
High quality draft sequences for prokaryotic genomes using a mix of new sequencing technologies
journal, January 2008
- Aury, Jean-Marc; Cruaud, Corinne; Barbe, Valérie
- BMC Genomics, Vol. 9, Issue 1
Latent homology and convergent regulatory evolution underlies the repeated emergence of yeasts
journal, July 2014
- Nagy, László G.; Ohm, Robin A.; Kovács, Gábor M.
- Nature Communications, Vol. 5, Issue 1
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