Abstract
Sexual development is a key evolutionary innovation of eukaryotes. In many species, mating involves interaction between compatible mating partners that can undergo cell and nuclear fusion and subsequent steps of development including meiosis. Mating compatibility in fungi is governed by the mating type (MAT) loci. In basidiomycetes, the ancestral state is hypothesized to be tetrapolar, with two genetically unlinked MAT loci containing homeodomain transcription factor genes (HD locus) and pheromone and pheromone receptor genes (P/R locus), respectively. Alleles at both loci must differ between mating partners for completion of sexual development. However, there are also basidiomycetes with bipolar mating systems, which can arise through genomic linkage of the HD and P/R loci. In the order Tremellales, bipolarity is found only in the pathogenic Cryptococcus species. Here, we describe the analysis of MAT loci from 24 species of the Trichosporonales, a sister order to the Tremellales. In all of the species analyzed, the MAT loci are fused and a single HD gene is present in each mating type, similar to the organization in the pathogenic Cryptococci. However, the HD and P/R allele combinations in the Trichosporonales are different from those in the pathogenic Cryptococci. This and the existence of tetrapolar species in the Tremellales suggest that fusion of the HD and P/R loci occurred independently in the Trichosporonales and pathogenic Cryptococci, supporting the hypothesis of convergent evolution towards fused MAT regions, similar to previous findings in other fungal groups. Unlike the fused MAT loci in several other basidiomycete lineages though, the gene content and gene order within the fused MAT loci are highly conserved in the Trichosporonales, and there is no apparent suppression of recombination extending from the MAT loci to adjacent chromosomal regions, suggesting different mechanisms for the evolution of physically linked MAT loci in these groups.
Highlights
Sexual reproduction is prevalent among eukaryotic organisms, but despite its rather conserved core features, many aspects of sexual development show high evolutionary flexibility [1,2,3]
We analyzed the genomes of 29 isolates that belong to 24 Trichosporonales species for the organization of the mating type (MAT) loci, and found that all of them contain fused MAT loci, i.e. the MAT loci are physically linked on the same contig, with the mating-type determining genes for the P/R locus (STE3 and the pheromone precursor genes) and the HD locus (SXI homeodomain genes) located ~55 kb apart from each other
The SXI/STE3 combinations found in the majority of Trichosporonales are different from the MAT alleles in C. neoformans, where the SXI1 gene is combined with STE3α in the MATα allele, and SXI2 is combined with STE3a in the MATa allele [24, 38]
Summary
Sexual reproduction is prevalent among eukaryotic organisms, but despite its rather conserved core features (syngamy/karyogamy and meiosis), many aspects of sexual development show high evolutionary flexibility [1,2,3]. This includes the determination of compatible mating partners that can successfully undergo mating and complete the sexual cycle. Compatibility is determined by one or more genetic loci that differ between compatible mating partners The evolution of such genes has been studied in many systems including plants, animals, algae, and fungi [1, 4,5,6]. Fungi are excellent model systems to study the evolution of genomic regions involved in mating and mating type determination
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