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.
Highlights
Tuberaceae is one of the most diverse lineages of symbiotic truffle-forming fungi
We present the comparative analysis of these genomes, with particular emphasis on Tuberaceaespecific sequences, symbiosis- and fruiting-body-regulated genes, and genes coding for plant cell wall degrading enzymes (PCWDEs) and volatile organic compounds (VOCs) synthesis
Shared symbiosis genes in truffle ectomycorrhizae We found that 5,229 (75%) of the 6,952 orthologous T. magnatum/ T. melanosporum genes were expressed in T. magnatum–Quercus robur and T. melanosporum–Corylus avellana ectomycorrhizae (Supplementary Fig. 12A), indicating that developmental and metabolic pathways associated with symbiosis in these truffles are very similar, despite their interaction with different host species
Summary
Clusters (Gene no. percentage) I (48/10%) II (27/6%) * III (41/8%) IV (36/7%) V (38/8%). One-third of symbiosisinduced genes are homologous to genes only present in Tuberaceae (clusters I, II and III) This large set of mycorrhiza-induced genes conserved in Tuberaceae indicates that similar ancient gene networks are involved in development and functioning of ectomycorrhizae in Tuberaceae species (for example, Supplementary Table 7). A low proportion (15%) of T. magnatum symbiosis-upregulated genes are induced in T. melanosporum–Corylus avellana ectomycorrhizae (Supplementary Fig. 12B, Supplementary Table 6)[5,20] They are involved in core metabolic pathways required for an efficient symbiosis, such as carbohydrate, oligopeptide, amino acid and lipid transporters, or root colonization (for example, GH5 endoglucanase), but most of them (62–69%) have no known function (Supplementary Tables 6 and 7). Future challenges include the experimental assessment of the catalytic properties of specific enzymes involved in VOC biosynthesis and the elucidation of the role played by fruiting-body-associated microorganisms in aroma formation
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