Massive genome investigations reveal insights of prevalent introgression for environmental adaptation and triterpene biosynthesis in Ganoderma.

ABSTRACT

Genome introgression is one of the driving forces that can increase species and genetic diversity and facilitate the adaptive evolution of organisms and biodiversity conservation. However, the genomic introgression and its contribution to biodiversity of macrofungi are still unclear. The genus Ganoderma is a typical macrofungal group that plays crucial roles in forest ecosystem as saprophytic organisms and plant pathogens, and is also involved in human health as medicinal mushrooms. Most public Ganoderma genomes are fragmented, and reference genomes and whole-genome information of diverse germplasm resources for many Ganoderma species are lacking, thus hindering functional and evolutionary genomic investigations among Ganoderma species. In this study, we provide high-quality genomes of 10 Ganoderma species and whole-genome variants data of 224 individuals from various ecoregions, enabling us to infer the phylogeny of Ganoderma species and their historical population dynamics. Based on whole-genome variants, widespread and genome-wide introgression among Ganoderma species is revealed. Genes with significant introgression signals were related to stress response, digestive absorption, and secondary metabolite synthesis, factors that may contribute to environmental adaptation and important biocomponent metabolism. CYP512U6, an essential functional gene in the CYP450 family related to Ganoderma triterpene synthesis, was detected with significant introgression and selection signals combined with Ganoderma metabolomic analysis, indicating that both ancient gene exchange and recent domestication have contributed to the categories and content of secondary metabolites of Ganoderma. The reference genomes, whole-genome variants, and metabolite profiles could serve as abundant and valuable genetic resources for evolution, ecology, and conservation investigations of Ganoderma species and other macrofungi.