Phylogenomic Insights into the Taxonomy, Ecology, and Mating Systems of the Lorchel Family Discinaceae (Pezizales, Ascomycota)

Abstract

Lorchels, also known as false morels (Gyromitra spp.), are iconic due to their brain-shaped mushrooms and production of gyromitrin, a deadly mycotoxin. Molecular phylogenetic studies have hitherto failed to resolve deep-branching relationships in the lorchel family, Discinaceae, hampering our ability to settle longstanding taxonomic debates and to reconstruct the evolution of toxin production. We generated 75 draft genomes from cultures and mushroom samples (some collected as early as 1960), conducted phylogenomic analyses using 1542 single-copy orthologs to infer the early evolutionary history of lorchels, and identified genomic signatures of trophic mode and mating-type loci to better understand lorchel ecology and reproductive biology. Our phylogenomic tree was supported by high gene tree concordance, facilitating genus-level taxonomic revisions in Discinaceae. We recognized a single genus, Gyromitra, encompassing 10 subgenera; two subgenera were newly erected and 22 new combinations were formalized. Paradiscinamelaleuca and Marcelleina donadinii formed their own family-level clade sister to Morchellaceae. Genome size and CAZyme content agreed with a mycorrhizal lifestyle for the sequestrate species formerly classified as Hydnotrya, whereas the other clades possessed genomic properties of a saprotrophic habit. Gyromitra species were found to be predominantly heterothallic—either MAT1-1 or MAT1-2—but a single occurrence of colocalized mating-type idiomorphs indicative of homothallism was observed in Gyromitra esculenta strain CBS101906 and requires additional confirmation follow-up study. Our genomic dataset will facilitate investigations into the gyromitrin biosynthesis genes and their evolutionary history. With additional sampling of Geomoriaceae and Helvellaceae—two closely related families with no publicly available genomes—these data will enable comprehensive studies on the independent evolution of truffloid morphology and ecological diversification in an economically important group of Pezizales fungi.

Keywords: CAZymes, comparative genomics, false morels, fungal mating-type locus, Gyromitra, taxonomic revision