Identification of Mating Type Genes in the Bipolar Basidiomycetous Yeast Rhodosporidium toruloides : First Insight into the MAT Locus Structure of the Sporidiobolales

Abstract

Rhodosporidium toruloides is a heterothallic, bipolar, red yeast that belongs to the Sporidiobolales, an order within a major lineage of basidiomycetes, the Pucciniomycotina. In contrast to other basidiomycetes, considerably less is known about the nature of the mating type (MAT) loci that control sexual reproduction in this lineage. Three genes (RHA1, RHA2, and RHA3) encoding precursors of the MAT A1 pheromone (rhodotorucine A) were previously identified and formed the basis for a genome walking approach that led to the identification of additional MAT genes in complementary mating strains of R. toruloides. Two mating type-specific alleles encoding a p21-activated kinase (PAK; Ste20 homolog) were found between the RHA2 and RHA3 genes, and identification in MAT A2 strains of a gene encoding a presumptive pheromone precursor enabled prediction of the structure of rhodotorucine a. In addition, a putative pheromone receptor gene (STE3 homolog) was identified upstream of RHA1. Analyses of genomic data from two closely related species, Sporobolomyces roseus and Sporidiobolus salmonicolor, identified syntenic regions that contain homologs of all the above-mentioned genes. Notably, six novel pheromone precursor genes were uncovered, which encoded, similarly to the RHA genes, multiple tandem copies of the peptide moiety. This suggests that this structure, which is unique among fungal lipopeptide pheromones, seems to be prevalent in red yeasts. Species comparisons provided evidence for a large, multigenic MAT locus structure in the Sporidiobolales, but no putative homeodomain transcription factor genes (which are present in all basidiomycetous MAT loci characterized thus far) could be found in any of the three species in the vicinity of the MAT genes identified.Fungal mating type (MAT) loci are specialized genomic regions that determine cell type identity and coordinate the sexual cycle. Their genetic structure has been relatively sparsely sampled in broad phylogenetic terms, but results of published studies have revealed both conserved features and remarkable diversity in ascomycetes and basidiomycetes (8, 13). A common trait of fungal MAT loci is the presence of genes encoding homeodomain or other classes of transcription factors that control the expression of genes that establish cell type identity and activate sexual development. In basidiomycetes, two major types of MAT loci have so far been recognized (9). The tetrapolar mating system of the corn smut Ustilago maydis and the mushrooms Coprinopsis cinerea and Schizophyllum commune is governed by two small (Ͻ10-kb) unlinked loci: one encodes homeodomain transcription factors (HD1 and HD2 homologs), and the other encodes lipopeptide pheromones and pheromone receptors (STE3 homologs), which mediate intercellular signaling prior to cell fusion and/or sexual development after mating (9). Each locus may be multiallelic, which can result in up to thousands of compatible mating types in certain tetrapolar species. On the other hand, in the bipolar system of the human pathog...

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

“…A single receptor gene (STE3-like) and three putative pheromone precursor genes presenting the characteristic C-terminal CAAX domain typical of fungal mating pheromones (Coelho et al 2008;Kües et al 2011), localized to a 238-kb-long scaffold (numbered 28; Figure 1) in CBS 5931, as identified by BLAST searches (see Material and Methods). A subsequent inspection of this genomic region revealed the presence of other genes previously shown to be involved in mating or required for the onset of the filamentous phase in dimorphic species (viz.…”

Ancient Trans-specific Polymorphism at Pheromone Receptor Genes in Basidiomycetes

“…Analyses of homeodomain proteins of a wider range of basidiomycetes are required to assess whether trans-specific polymorphism also exists at the homeodomain protein genes of the mating type. Recent studies however suggest that the homeodomain proteins could have been recruited for the mating-type function later than the pheromone receptors in the evolution of the basidiomycetes (Coelho et al 2008), which could explain that they do not show ancient transspecific polymorphism.…”

Fungal Sex: The Basidiomycota

“…Where investigated, the pheromone precursor genes each encode tandem copies of the mature peptide moiety (39–43), and an initial step of processing of a spacer region is required to reveal C-terminal CAAX motifs for each repeat (37, 44). In species where pheromones of opposite mating types have been clearly identified (namely in R. toruloides , Sporidiobolus salmonicolor , Leucosporidium scottii and Microbotryum spp.…”