Multiple Pathways to Homothallism in Closely Related Yeast Lineages in the Basidiomycota.

Sexual reproduction in fungi relies on proteins with well-known functions encoded by the mating type () loci. In the Basidiomycota, loci are often bipartite, with the locus encoding pheromone precursors and pheromone receptors and the locus encoding heterodimerizing homeodomain transcription factors (Hd1/Hd2). The interplay between different alleles of these genes within a single species usually generates at least two compatible mating types. However, a minority of species are homothallic, reproducing sexually without an obligate need for a compatible partner. Here, we examine the organization and function of the loci of , a species in the order Cystofilobasidiales, which is unusually rich in homothallic species. We determined gene content and organization in and found that it resembles a mating type of the closely related heterothallic species To explain the homothallic sexual reproduction observed in , we examined HD protein interactions in the two species and determined gene expression both in a natural setting and upon heterologous expression in , a homothallic species belonging to a clade sister to that of We conclude that the molecular basis for homothallism in appears to be distinct from that previously established for Unlike in the latter species, homothallism in may involve constitutive activation or dispensability of the pheromone receptor and the functional replacement of the usual Hd1/Hd2 heterodimer by an Hd2 homodimer. Overall, our results suggest that homothallism evolved multiple times within the Cystofilobasidiales. Sexual reproduction is important for the biology of eukaryotes because it strongly impacts the dynamics of genetic variation. In fungi, although sexual reproduction is usually associated with the fusion between cells belonging to different individuals (heterothallism), sometimes a single individual is capable of completing the sexual cycle alone (homothallism). Homothallic species are unusually common in a fungal lineage named Cystofilobasidiales. Here, we studied the genetic bases of homothallism in one species in this lineage, , and found it to be different in several aspects from those of another homothallic species, , belonging to the genus most closely related to Our results strongly suggest that homothallism evolved independently in and , lending support to the idea that transitions between heterothallism and homothallism are not as infrequent as previously thought. Our work also helps to establish the Cystofilobasidiales as a model lineage in which to study these transitions.