Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis

Francis Martin, Annegret Kohler, Claude Murat, Raffaella Balestrini, Pedro M. Coutinho, Olivier Jaillon, Barbara Montanini, Emmanuelle Morin, Benjamin Noel, Riccardo Percudani, Bettina Porcel, Andrea Rubini, Antonella Amicucci, Joelle Amselem, Véronique Anthouard, Sergio Arcioni, François Artiguenave, Jean Marc Aury, Paola Ballario, Angelo BolchiAndrea Brenna, Annick Brun, Marc Buée, Brandi Cantarel, Gérard Chevalier, Arnaud Couloux, Corinne Da Silva, France Denoeud, Sébastien Duplessis, Stefano Ghignone, Benot Hilselberger, Mirco Iotti, Benot Marçais, Antonietta Mello, Michele Miranda, Giovanni Pacioni, Hadi Quesneville, Claudia Riccioni, Roberta Ruotolo, Richard Splivallo, Vilberto Stocchi, Emilie Tisserant, Arturo Roberto Viscomi, Alessandra Zambonelli, Elisa Zampieri, Bernard Henrissat, Marc Henri Lebrun, Francesco Paolocci, Paola Bonfante, Simone Ottonello, Patrick Wincker

Research output: Contribution to journalArticle

416 Citations (Scopus)

Abstract

The Périgord black truffle (Tuber melanosporum Vittad.) and the Piedmont white truffle dominate todays truffle market. The hypogeous fruiting body of T. melanosporum is a gastronomic delicacy produced by an ectomycorrhizal symbiont endemic to calcareous soils in southern Europe. The worldwide demand for this truffle has fuelled intense efforts at cultivation. Identification of processes that condition and trigger fruit body and symbiosis formation, ultimately leading to efficient crop production, will be facilitated by a thorough analysis of truffle genomic traits. In the ectomycorrhizal Laccaria bicolor, the expansion of gene families may have acted as a symbiosis toolbox. This feature may however reflect evolution of this particular taxon and not a general trait shared by all ectomycorrhizal species. To get a better understanding of the biology and evolution of the ectomycorrhizal symbiosis, we report here the sequence of the haploid genome of T. melanosporum, which at 125 megabases is the largest and most complex fungal genome sequenced so far. This expansion results from a proliferation of transposable elements accounting for 58% of the genome. In contrast, this genome only contains 7,500 protein-coding genes with very rare multigene families. It lacks large sets of carbohydrate cleaving enzymes, but a few of them involved in degradation of plant cell walls are induced in symbiotic tissues. The latter feature and the upregulation of genes encoding for lipases and multicopper oxidases suggest that T. melanosporum degrades its host cell walls during colonization. Symbiosis induces an increased expression of carbohydrate and amino acid transporters in both L. bicolor and T. melanosporum, but the comparison of genomic traits in the two ectomycorrhizal fungi showed that genetic predispositions for symbiosisthe symbiosis toolboxevolved along different ways in ascomycetes and basidiomycetes.

Original languageEnglish (US)
Pages (from-to)1033-1038
Number of pages6
JournalNature
Volume464
Issue number7291
DOIs
StatePublished - Apr 15 2010

Fingerprint

Symbiosis
Genome
Cell Wall
Laccaria
Fungal Genome
Carbohydrates
Amino Acid Transport Systems
Basidiomycota
Ascomycota
DNA Transposable Elements
Haploidy
Plant Cells
Genetic Predisposition to Disease
Multigene Family
Lipase
Genes
Fruit
Oxidoreductases
Fungi
Up-Regulation

ASJC Scopus subject areas

  • Medicine(all)
  • General

Cite this

Martin, F., Kohler, A., Murat, C., Balestrini, R., Coutinho, P. M., Jaillon, O., ... Wincker, P. (2010). Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature, 464(7291), 1033-1038. https://doi.org/10.1038/nature08867

Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. / Martin, Francis; Kohler, Annegret; Murat, Claude; Balestrini, Raffaella; Coutinho, Pedro M.; Jaillon, Olivier; Montanini, Barbara; Morin, Emmanuelle; Noel, Benjamin; Percudani, Riccardo; Porcel, Bettina; Rubini, Andrea; Amicucci, Antonella; Amselem, Joelle; Anthouard, Véronique; Arcioni, Sergio; Artiguenave, François; Aury, Jean Marc; Ballario, Paola; Bolchi, Angelo; Brenna, Andrea; Brun, Annick; Buée, Marc; Cantarel, Brandi; Chevalier, Gérard; Couloux, Arnaud; Da Silva, Corinne; Denoeud, France; Duplessis, Sébastien; Ghignone, Stefano; Hilselberger, Benot; Iotti, Mirco; Marçais, Benot; Mello, Antonietta; Miranda, Michele; Pacioni, Giovanni; Quesneville, Hadi; Riccioni, Claudia; Ruotolo, Roberta; Splivallo, Richard; Stocchi, Vilberto; Tisserant, Emilie; Viscomi, Arturo Roberto; Zambonelli, Alessandra; Zampieri, Elisa; Henrissat, Bernard; Lebrun, Marc Henri; Paolocci, Francesco; Bonfante, Paola; Ottonello, Simone; Wincker, Patrick.

In: Nature, Vol. 464, No. 7291, 15.04.2010, p. 1033-1038.

Research output: Contribution to journalArticle

Martin, F, Kohler, A, Murat, C, Balestrini, R, Coutinho, PM, Jaillon, O, Montanini, B, Morin, E, Noel, B, Percudani, R, Porcel, B, Rubini, A, Amicucci, A, Amselem, J, Anthouard, V, Arcioni, S, Artiguenave, F, Aury, JM, Ballario, P, Bolchi, A, Brenna, A, Brun, A, Buée, M, Cantarel, B, Chevalier, G, Couloux, A, Da Silva, C, Denoeud, F, Duplessis, S, Ghignone, S, Hilselberger, B, Iotti, M, Marçais, B, Mello, A, Miranda, M, Pacioni, G, Quesneville, H, Riccioni, C, Ruotolo, R, Splivallo, R, Stocchi, V, Tisserant, E, Viscomi, AR, Zambonelli, A, Zampieri, E, Henrissat, B, Lebrun, MH, Paolocci, F, Bonfante, P, Ottonello, S & Wincker, P 2010, 'Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis', Nature, vol. 464, no. 7291, pp. 1033-1038. https://doi.org/10.1038/nature08867
Martin F, Kohler A, Murat C, Balestrini R, Coutinho PM, Jaillon O et al. Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature. 2010 Apr 15;464(7291):1033-1038. https://doi.org/10.1038/nature08867
Martin, Francis ; Kohler, Annegret ; Murat, Claude ; Balestrini, Raffaella ; Coutinho, Pedro M. ; Jaillon, Olivier ; Montanini, Barbara ; Morin, Emmanuelle ; Noel, Benjamin ; Percudani, Riccardo ; Porcel, Bettina ; Rubini, Andrea ; Amicucci, Antonella ; Amselem, Joelle ; Anthouard, Véronique ; Arcioni, Sergio ; Artiguenave, François ; Aury, Jean Marc ; Ballario, Paola ; Bolchi, Angelo ; Brenna, Andrea ; Brun, Annick ; Buée, Marc ; Cantarel, Brandi ; Chevalier, Gérard ; Couloux, Arnaud ; Da Silva, Corinne ; Denoeud, France ; Duplessis, Sébastien ; Ghignone, Stefano ; Hilselberger, Benot ; Iotti, Mirco ; Marçais, Benot ; Mello, Antonietta ; Miranda, Michele ; Pacioni, Giovanni ; Quesneville, Hadi ; Riccioni, Claudia ; Ruotolo, Roberta ; Splivallo, Richard ; Stocchi, Vilberto ; Tisserant, Emilie ; Viscomi, Arturo Roberto ; Zambonelli, Alessandra ; Zampieri, Elisa ; Henrissat, Bernard ; Lebrun, Marc Henri ; Paolocci, Francesco ; Bonfante, Paola ; Ottonello, Simone ; Wincker, Patrick. / Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. In: Nature. 2010 ; Vol. 464, No. 7291. pp. 1033-1038.
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AU - Jaillon, Olivier

AU - Montanini, Barbara

AU - Morin, Emmanuelle

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