Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis

Abstract

The genome of the Périgord black truffle Tuber melanosporum Vittad., a gourmet delicacy that grows symbiotically on the roots of European oak, has been sequenced. This is the largest and most complex fungal genome so far sequenced. The genome is unusually gene-poor, but rich in the mobile genetic elements known as transposons. Comparison with the sequence of Laccaria bicolor, another ectomycorrhizal symbiotic fungus, reveals contrasting gene sets reflecting two different molecular toolkits that have evolved independently to fit the root symbiont lifestyle. Cultivation of the truffle is a complicated process, and most truffles are still harvested from the wild. So the analysis of genetic traits related to fruiting and symbiosis could help boost crop production and make black truffles more widely available. The genome of the black truffle - one of the most popular truffles on the market - has been sequenced. This is the first genome of a symbiotic ascomycete to be analysed. Comparison with the genome of another ectomycorrhizal symbiotic fungus indicates that a genetic predisposition to symbiosis evolved differently in ascomycetes and basidiomycetes. The study also offers insight into fungal sex and fruiting. 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 ∼125 megabases 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.