Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis

Francis Martin; Annegret Kohler; Claude Murat; Raffaella Balestrini; Pedro Coutinho; Olivier Jaillon; Barbara Montanini; Emmanuelle Morin; Benjamin Noel; Riccardo Percudani; Betina Porcel; Andrea Rubini; Antonella Amicucci; Joelle Amselem; Véronique Anthouard; Sergio Arcioni; François Artiguenave; Jean-Marc Aury; Paola Ballario; Angelo Bolchi; Andrea Brenna; Annick Brun; Marc Buée; Brandi Cantarel; Gérard Chevalier; Arnaud Couloux; Corinne da Silva; France Denoeud; Sébastien Duplessis; Stefano Ghignone; Benoît Hilselberger; Mirco Iotti; Benoit 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

doi:10.1038/nature08867

Journal articles

Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis

Francis Martin ^{1, *} Annegret Kohler ¹ Claude Murat ¹ Raffaella Balestrini ² Pedro 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 Göttingen - Georg-August-Universität Göttingen

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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Journal articles

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Life Sciences [q-bio]

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Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis

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