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Pezizomycetes genomes reveal the molecular basis of ectomycorrhizal truffle lifestyle

Claude Murat 1 Thibaut Payen 1 Benjamin Noël 2 Alan Kuo 3 Emmanuelle Morin 1 Juan Chen 4 Annegret Kohler 1 Krisztina Krizsán 5 Raffaella Balestrini 6 Corinne da Silva 2 Barbara Montanini 7 Mathieu Hainaut Elisabetta Levati 8 Kerrie Barry 9 Beatrice Belfiori 10 Nicolas Cichocki 1 Alicia Clum 11 Rhyan Dockter 11 Laure Fauchery 1 Julie Guy 12 Mirco Iotti 13 François Le Tacon 1 Erika Lindquist 9 Anna Lipzen 3 Fabienne Malagnac 14 Antonietta Mello 15 Virginie Molinier 16 Shingo Miyauchi 1 Julie Poulain 12 Claudia Riccioni 10 Andrea Rubini 10 Yaron Sitrit Richard Splivallo 17 Stefanie Traeger 18 Mei Wang 3 Daniel Wipf 19 Alessandra Zambonelli 20 Francesco Paolocci 21 Minou Nowrousian Simone Ottonello 7 Petr Baldrian 22 Joseph Spatafora 23 Bernard Henrissat 24 Laszlo Nagy 25 Jean-Marc Aury 2 Patrick Wincker 26 Igor Grigoriev 11 Paola Bonfante 27 Francis Martin 1
1 IAM - Interactions Arbres-Microorganismes
2 GENOSCOPE - Genoscope - Centre national de séquençage [Evry]
3 US Department of Energy Joint Genome Institute
4 Institute of medicinal plant development
5 Synthet & Syst Biol Unit
6 CNR, Ist Protez Piante
7 Laboratory of Functional Genomics and Protein Engineering, Biochemistry and Molecular Biology Unit, Department of Life Sciences
8 Dept Life Sci, Biochem & Mol Biol Unit, Lab Funct Genom & Prot Engn
9 Joint Genome Institute
10 Plant Genetics Institute
11 DOE - Department of Energy / Joint Genome Institute
12 UMR 8030 - Génomique métabolique
13 Dipartimento Protez & Valorizzaz Agroalimentare
14 IGM - Institut de génétique et microbiologie [Orsay]
15 Istituto per la Protezione delle Piante
16 Agroécologie [Dijon]
17 IPF – Integrative Fungal Research
18 Institut für biologie und biotechnologie der pflanzen
19 0977 Unité associée de Biologie forestière
20 UNIBO - Alma Mater Studiorum University of Bologna
21 Plant Genetics Institute
22 Institute of Microbiology of the CAS
23 Department of Botany and Plant Pathology
24 AFMB - Architecture et fonction des macromolécules biologiques
25 Department of Biochemistry and Molecular Biology
26 IG - Institut de Génomique d'Evry
27 Dipartimento di Biologia Vegetale
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.
Keywords : volatile organic compound truffle tuber (truffles)
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JOLIOT | CNRS | CEA | I2BC | UNIV-BOURGOGNE | INRA | JACOB | UNIV-AMU | UNIV-LORRAINE | IAM-UL | CEA-DRF | UNIV-EVRY | GENOMIQUE-METABOLIQUE | AGROECOLOGIE | CEA-UPSAY | GENOSCOPE | ARBRE | INRAE | ANR | A2F-UL | GS-BIOSPHERA | GS-HEALTH-DRUG-SCIENCES | AFMB

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Claude Murat, Thibaut Payen, Benjamin Noël, Alan Kuo, Emmanuelle Morin, et al.. Pezizomycetes genomes reveal the molecular basis of ectomycorrhizal truffle lifestyle. Nature Ecology & Evolution, Nature, 2018, 2 (12), pp.1956-1965. ⟨10.1038/s41559-018-0710-4⟩. ⟨hal-02094494⟩

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