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) , Matthieu 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 F. 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 S. 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 (12) , Igor Grigoriev (11) , Paola Bonfante (26) , Francis Martin (1)

1 IAM - Interactions Arbres-Microorganismes
2 LBGB - Laboratoire de Bioinformatique pour la Génomique et la Biodiversité
3 US Department of Energy Joint Genome Institute
4 IMPLAD - 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 Unité associée de biologie forestière
20 UNIBO - Alma Mater Studiorum Università di Bologna = 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 Dipartimento di Biologia Vegetale

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: truffle; tuber (truffles); volatile organic compound

Keywords: composé organique volatil; expression différentielle; champignon ectomycorhizien; truffe; champignon; tuber

Domains: Life Sciences [q-bio]

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, 2018, 2 (12), pp.1956-1965. ⟨10.1038/s41559-018-0710-4⟩. ⟨hal-02094494⟩