Abstract
Sexual reproduction in fungi relies on proteins with well-known functions encoded at the mating type (MAT) loci. In the Basidiomycota, MAT loci are often bipartite, the P/R locus encoding pheromone precursors and pheromone receptors and the HD locus encoding heterodimerizing homeodomain transcription factors (Hd1 and Hd2). The interplay between different alleles of these genes within a single species determines a variety of sexual systems and patterns, which may result in the emergence of hundreds of compatible mating types. However, a minority of species are homothallic, reproducing sexually without the need for a compatible partner.
Here we examine the organization and function of the MAT loci of Cystofilobasidium capitatum, a species in the order Cystofilobasidiales, which is unusually rich in homothallic species. For this, we determined MAT gene content and organization in C. capitatum and found that it resembled a mating type of the closely related heterothallic species Cystofilobasidium ferigula. To explain the homothallic sexual reproduction observed in C. capitatum we examined HD -protein interactions in the two individual Cystofilobasidium species and determined C. capitatum MAT gene expression both in the natural setting and upon heterologous expression in Phaffia rhodozyma, a homothallic species belonging to a clade sister to the Cystofilobasidium. We conclude that the molecular basis for homothallism in C. capitatum appears to be distinct from that previously established for P. rhodozyma. Unlike the latter species, homothallism in C. capitatum 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 in the Cystofilobasidiales, underpinned by diverse molecular mechanisms.
Importance 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, Cystofilobasidium capitatum, and found it to be different in several aspects when compared to another homothallic species, Phaffia rhodozyma, belonging to the genus most closely related to Cystofilobasidium. Our results strongly suggest that homothallism evolved independently in Phaffia and Cystofilobasidium, 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.
Competing Interest Statement
The authors have declared no competing interest.