Large-scale fungal strain sequencing unravels the molecular diversity in mating loci maintained by long-term balancing selection

Abstract

Balancing selection, an evolutionary force that retains genetic diversity, has been detected in multiple genes and organisms, such as the sexual mating loci in fungi. However, to quantify the strength of balancing selection and define the mating-related genes require a large number of strains. In tetrapolar basidiomycete fungi, sexual type is determined by two unlinked loci,MATAandMATB. Genes in both loci define mating type identity, control successful mating and completion of the life cycle. These loci are usually highly diverse. Previous studies have speculated, based on culture crosses, that species of the non-model genusTrichaptum(Hymenochaetales, Basidiomycota) possess a tetrapolar mating system, with multiple alleles. Here, we sequenced a hundred and eighty strains of threeTrichaptumspecies. We characterized the chromosomal location ofMATAandMATB, the molecular structure ofMATregions and their allelic richness. The sequencing effort was sufficient to molecularly characterize multipleMATalleles segregating before the speciation event ofTrichaptumspecies. Analyses suggested that long-term balancing selection has generated trans-species polymorphisms. Mating sequences were classified in different allelic classes based on an amino acid identity (AAI) threshold supported by phylogenetics. 17,550 mating types were predicted based on the allelic classes.In vitrocrosses allowed us to support the degree of allelic divergence needed for successful mating. Even with the high amount of divergence, key amino acids in functional domains are conserved. We conclude that the genetic diversity of mating loci inTrichaptumis due to long-term balancing selection, with limited recombination and duplication activity. The large number of sequenced strains highlighted the importance of sequencing multiple individuals from different species to detect the mating-related genes, the mechanisms generating diversity and the evolutionary forces maintaining them.