Letter

Nature 464, 1033-1038 (15 April 2010) | doi:10.1038/nature08867; Received 20 August 2009; Accepted 28 January 2010; Published online 28 March 2010

Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis

Francis Martin1, Annegret Kohler1, Claude Murat1, Raffaella Balestrini2, Pedro M. Coutinho3, Olivier Jaillon4,5,6, Barbara Montanini7, Emmanuelle Morin1, Benjamin Noel4,5,6, Riccardo Percudani7, Bettina Porcel4,5,6, Andrea Rubini8, Antonella Amicucci9, Joelle Amselem10, Véronique Anthouard4,5,6, Sergio Arcioni8, François Artiguenave4,5,6, Jean-Marc Aury4,5,6, Paola Ballario11, Angelo Bolchi7, Andrea Brenna11, Annick Brun1, Marc Buée1, Brandi Cantarel3, Gérard Chevalier12, Arnaud Couloux4,5,6, Corinne Da Silva4,5,6, France Denoeud4,5,6, Sébastien Duplessis1, Stefano Ghignone2, Benoît Hilselberger1,10, Mirco Iotti13, Benoît Marçais1, Antonietta Mello2, Michele Miranda14, Giovanni Pacioni15, Hadi Quesneville10, Claudia Riccioni8, Roberta Ruotolo7, Richard Splivallo16, Vilberto Stocchi9, Emilie Tisserant1, Arturo Roberto Viscomi7, Alessandra Zambonelli13, Elisa Zampieri2, Bernard Henrissat3, Marc-Henri Lebrun17, Francesco Paolocci8, Paola Bonfante2, Simone Ottonello7 & Patrick Wincker4,5,6

  1. INRA, UMR 1136, INRA-Nancy Université, Interactions Arbres/Microorganismes, 54280 Champenoux, France
  2. Istituto per la Protezione delle Piante del CNR, sez. di Torino and Dipartimento di Biologia Vegetale, Università degli Studi di Torino, Viale Mattioli, 25, 10125 Torino, Italy
  3. Architecture et Fonction des Macromolécules Biologiques, UMR 6098 CNRS-Universités Aix-Marseille I & II, 13288 Marseille, France
  4. CEA, IG, Genoscope, 2 rue Gaston Crémieux CP5702, F-91057 Evry, France
  5. CNRS, UMR 8030, 2 rue Gaston Crémieux, CP5706, F-91057 Evry, France
  6. Université d’Evry, F-91057 Evry, France
  7. Dipartimento di Biochimica e Biologia Molecolare, Università degli Studi di Parma, Viale G.P. Usberti 23/A, 43100 Parma, Italy
  8. CNR-IGV Istituto di Genetica Vegetale, Unità Organizzativa di Supporto di Perugia, via Madonna Alta, 130, 06128 Perugia, Italy
  9. Dipartimento di Scienze Biomolecolari, Università degli Studi di Urbino, Via Saffi 2 - 61029 Urbino (PU), Italy
  10. INRA, Unité de Recherche Génomique Info, Route de Saint-Cyr, 78000 Versailles, France
  11. Dipartimento di Genetica e Biologia Molecolare & IBPM (CNR), Università La Sapienza, Roma, Piazzale, A. Moro 5, 00185 Roma, Italy
  12. INRA, UMR Amélioration et Santé des Plantes, INRA-Université Blaise Pascal, INRA – Clermont-Theix, 63122 Saint-Genes-Champanelle, France
  13. Dipartimento di Protezione e Valorizzazione Agroalimentare, Università degli Studi di Bologna, 40 126 Bologna, Italy
  14. Dipartimento di Biologia di Base ed Applicata,
  15. Dipartimento di Scienze Ambientali, Università degli Studi dell’Aquila, Via Vetoio Coppito 1 - 67100 L’Aquila, Italy
  16. University of Goettingen, Molecular Phytopathology and Mycotoxin Research, Grisebachstrasse 6, D-37077 Goettingen, Germany
  17. INRA, UMR BIOGER-CPP, INRA-Grignon, av Lucien Brétignières - 78850 Thiverval Grignon, France

Correspondence to: Francis Martin1 Correspondence and requests for materials should be addressed to F.M. (Email: fmartin@nancy.inra.fr).

This article is distributed under the terms of the Creative Commons Attribution-Non-Commercial-Share Alike licence (http://creativecommons.org/licenses/by-nc-sa/3.0/), which permits distribution, and reproduction in any medium, provided the original author and source are credited. This licence does not permit commercial exploitation, and derivative works must be licensed under the same or similar licence.

The Périgord black truffle (Tuber melanosporum Vittad.) and the Piedmont white truffle dominate today’s truffle market1, 2. The hypogeous fruiting body of T. melanosporum is a gastronomic delicacy produced by an ectomycorrhizal symbiont3 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’4. This feature may however reflect evolution of this particular taxon and not a general trait shared by all ectomycorrhizal species5. 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 ~125megabases 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 symbiosis—‘the symbiosis toolbox’—evolved along different ways in ascomycetes and basidiomycetes.

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