Repeated loss of function at HD mating-type genes and of recombination in anther-smut fungi

Basidiomycete fungi typically have two mating-type loci controlling mating compatibility, HD and PR, residing on different chromosomes. Loss-of-function in mating compatibility has been reported at the PR genes in a few heterothallic basidiomycetes, but not for the HD genes. In Microbotryum anther-smut fungi, there have been repeated linkage events between the HD and PR loci through chromosome fusions, leading to non-recombining regions. Here, we found that two sister Microbotryum species parasitizing Dianthus plants, M. superbum and M. shykoffianum, as well as the distantly related M. scorzonerae, have their HD and PR loci on different chromosomes, but with the PR chromosome fused with a part of the ancestral HD chromosome. In addition, recombination suppression has extended stepwise, generating evolutionary strata. In all three species, the HD genes lost their function in mating compatibility, natural diploid strains being often homozygous at the HD locus. Strains could be homozygous for a disrupted HD2 gene, that was hardly expressed during mating. Mating tests confirmed that a single genetic factor controlled mating compatibility and that haploid strains with identical HD alleles could mate and produce hyphae. This study shows that a unifactorial mating-type determinism can evolve, repeatedly, from a bifactorial system, by different mechanisms.