Evolution of Mating Systems in Basidiomycetes and the Genetic Architecture Underlying Mating-Type Determination in the Yeast Leucosporidium scottii

In most fungi, sexual reproduction is bipolar; that is, two alternate sets of genes at a single mating-type (MAT) locus determine two mating types. However, in the Basidiomycota, a unique (tetrapolar) reproductive system emerged in which sexual identity is governed by two unlinked MAT loci, each of which controls independent mechanisms of self/nonself recognition. Tetrapolar-to-bipolar transitions have occurred on multiple occasions in the Basidiomycota, resulting, for example, from linkage of the two MAT loci into a single inheritable unit. Nevertheless, owing to the scarcity of molecular data regarding tetrapolar systems in the earliest-branching lineage of the Basidiomycota (subphylum Pucciniomycotina), it is presently unclear if the last common ancestor was tetrapolar or bipolar. Here, we address this question, by investigating the mating system of the Pucciniomycotina yeast Leucosporidium scottii. Using whole-genome sequencing and chromoblot analysis, we discovered that sexual reproduction is governed by two physically unlinked gene clusters: a multiallelic homeodomain (HD) locus and a pheromone/receptor (P/R) locus that is biallelic, thereby dismissing the existence of a third P/R allele as proposed earlier. Allele distribution of both MAT genes in natural populations showed that the two loci were in strong linkage disequilibrium, but independent assortment of MAT alleles was observed in the meiotic progeny of a test cross. The sexual cycle produces fertile progeny with similar proportions of the four mating types, but approximately 2/3 of the progeny was found to be nonhaploid. Our study adds to others in reinforcing tetrapolarity as the ancestral state of all basidiomycetes.