Pangeneric analyses reveal the divergent genome evolution and ecologies between morels and truffles in the Morchellaceae

Morels are iconic macrofungi known for their culinary value and spring emergence. Molecular phylogenetic studies have hitherto failed to elucidate the evolution of the ecological lifestyles of true and false morels, impeding their capacity to resolve longstanding debates regarding the extent of their saprotrophy and the potential for biotrophic associations with plants. In this study, we examined the evolutionary history and molecular innovations of Morchellaceae by generating high-quality genomes from species encompassing all the major clades within this family. We used conserved single-copy orthologs to infer the evolutionary history of true and false morels and related truffles. The genome size, transposable element content, and polysaccharide-degrading enzyme gene content are consistent with an ectomycorrhizal lifestyle for the Morchellaceae truffles Leucangium carthusianum and Kalapuya brunnea, whereas the other clades, including all true morels (Morchella spp.), exhibited genomic signatures of saprotrophic habits characterized by a highly conserved set of genes encoding plant biomass-related degrading enzymes. Morchellaceae species were found to be predominantly heterothallic, with either the MAT1-1 or MAT1-2 loci; however, the occurrence of colocalized mating-type idiomorphs, indicative of homothallism, was observed in M. rufobrunnea, M. peruviana, L. carthusianum, and the outgroup taxon Gyromitra esculenta. This study revealed a wealth of largely undiscovered genomic traits, including saprotrophic potential within Morchellaceae and a lack of biotrophic markers, and contributes to our understanding of the intricate evolutionary trajectories of the modes of nutrition in soil fungi.