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Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis

Francis Martin 1, * Annegret Kohler 1 Claude Murat 1 Raffaella Balestrini 2 Pedro M. Coutinho 3 Olivier Jaillon 4 Barbara Montanini 5 Emmanuelle Morin 1, 6 Benjamin Noel 4 Riccardo Percudani 5 Betina Porcel 4 Andrea Rubini 7 Antonella Amicucci 8 Joelle Amselem 9 Véronique Anthouard 4, 10 Sergio Arcioni 7 François Artiguenave 4, 10 Jean-Marc Aury 4, 10 Paola Ballario 11 Angelo Bolchi 5 Andrea Brenna 12 Annick Brun 1 Marc Buée 1 Brandi Cantarel 3 Gérard Chevalier 13 Arnaud Couloux 4 Corinne da Silva 4, 10 France Denoeud 4, 10 Sébastien Duplessis 1 Stefano Ghignone 2 Benoît Hilselberger 1 Mirco Iotti 14 Benoit Marçais 1 Antonietta Mello 15 Michele Miranda 16 Giovanni Pacioni 17 Hadi Quesneville 18 Claudia Riccioni 19 Roberta Ruotolo 5 Richard Splivallo 20 Vilberto Stocchi 8 Emilie Tisserant 1 Arturo Roberto Viscomi 5 Alessandra Zambonelli 14 Elisa Zampieri 21 Bernard Henrissat 22 Marc-Henri Lebrun 23 Francesco Paolocci 24 Paola Bonfante 21 Simone Ottonello 5 Patrick Wincker 4
* Corresponding author
1 IAM - Interactions Arbres-Microorganismes
2 Istituto per la Protezione Sostenibile delle Piante (CNR-IPSP)
3 AFMB - Architecture et fonction des Macromolécules Biologiques - UMR 6098
4 GENOSCOPE - Genoscope - Centre national de séquençage [Evry]
5 Dipartimento di Biochimica e Biologia Molecolare
6 CEISAM - Chimie Et Interdisciplinarité : Synthèse, Analyse, Modélisation
7 CNR - Consiglio Nazionale delle Ricerche [Milano]
8 DISB - Dipartimento di Scienze Biomolecolari Universita di Urbino
9 INRA - Institut National de la Recherche Agronomique
10 UMR 8030 - Génomique métabolique
11 Dipartimento di Genetica e Biologia Molecolare
12 Dipartimento di Genetica e Biologia Molecolare
13 UBP - Université Blaise Pascal - Clermont-Ferrand 2
14 Università degli Studi di Bologna
15 Dipartimento di Biologia Vegetale
16 Dipartimento di Biologia di Base ed Applicata
17 UNIVAQ - Università degli Studi dell'Aquila
18 URGI - Unité de Recherche Génomique Info
19 CNR IGV
20 University of Goettingen
21 CNR - Consiglio Nazionale delle Ricerche [Torino]
22 AFMB - Architecture et fonction des macromolécules biologiques
23 BIOGER - BIOlogie et GEstion des Risques en agriculture
24 ISTM-CNR [Perugia - Milano] - Istituto di Scienze e Tecnologie Molecolari = Institute of Molecular Science and Technologies
Abstract : The Périgord black truffle ($Tuber\ melanosporum$ Vittad.) and the Piedmont white truffle dominate today's 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 $\sim$125 megabases is the largest and most complex fungal genome sequenced so far. This expansion results from a proliferation of transposable elements accounting for $\sim$58% of the genome. In contrast, this genome only contains $\sim$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
Keywords : TRUFFE NOIRE DU PERIGORD
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CEA | UNIV-LORRAINE | INC-CNRS | GENOMIQUE-METABOLIQUE | JACOB | CEA-DRF | IAM-UL | GENOSCOPE | CNRS | INRA | UNIV-EVRY | UNIV-NANTES | UNIV-AMU | ACL-SVSAE | AGROPARISTECH | PRES_CLERMONT | INRAE | A2F-UL

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Francis Martin, Annegret Kohler, Claude Murat, Raffaella Balestrini, Pedro M. Coutinho, et al.. Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature, Nature Publishing Group, 2010, 464 (7291), pp.1033-1038. ⟨10.1038/nature08867⟩. ⟨cea-00907731⟩

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