Convergent evolution of linked mating-type loci in basidiomycete fungi
Authors: Sun Sheng , Coelho Marco A. , Heitman Joseph , Nowrousian Minou 
Published: May 2019

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 mating type determinants, which are localized at mating type (MAT) loci. In basidiomycetes, the ancestral state is hypothesized to be tetrapolar (bifactorial), with two genetically unlinkedMATloci containing homeodomain transcription factor genes (HDlocus) and pheromone and pheromone receptor genes (P/Rlocus), respectively. Alleles at both loci must differ between mating partners for completion of sexual development. However, there are also basidiomycete species with bipolar (unifactorial) mating systems, which can arise through genomic linkage of theHDandP/Rloci. In the orderTremellales, which is comprised of mostly yeast-like species, bipolarity is found only in the human pathogenicCryptococcusspecies. Here, we describe the analysis ofMATloci from theTrichosporonales, a sister order to theTremellales. We analyzed genome sequences from 29 strains that belong to 24 species, including two new genome sequences generated in this study. Interestingly, in all of the species analyzed, theMATloci are fused and a singleHDgene is present in each mating type. This is similar to the organization in the pathogenic Cryptococci, which also have linkedMATloci and carry only oneHDgene perMATlocus instead of the usual twoHDgenes found in the vast majority of basidiomycetes. However, theHDandP/Rallele combinations in theTrichosporonalesare different from those in the pathogenicCryptococcusspecies. The differences in allele combinations compared to the bipolar Cryptococci as well as the existence of tetrapolarTremellalessister species suggest that fusion of theHDandP/Rloci and differential loss of one of the twoHDgenes perMATallele occurred independently in theTrichosporonalesand pathogenic Cryptococci. This finding supports the hypothesis of convergent evolution at the molecular level towards fused mating-type regions in fungi, similar to previous findings in other fungal groups. Unlike the fusedMATloci in several other basidiomycete lineages though, the gene content and gene order within the fusedMATloci are highly conserved in theTrichosporonales, and there is no apparent suppression of recombination extending from theMATloci to adjacent chromosomal regions, suggesting different mechanisms for the evolution of physically linkedMATloci in these groups.

Author summary

Sexual development in fungi is governed by genes located within a single mating type (MAT) locus or at two unlinkedMATloci. While the latter is thought to be the ancestral state in basidiomycetes, physical linkage of the twoMATloci has occurred multiple times during basidiomycete evolution. Here, we show that physically linkedMATloci are present in all analyzed species of the basidiomycete orderTrichosporonales. In contrast to previously studied basidiomycetes, the fusedMATloci in theTrichosporonaleshave highly conserved gene order, suggesting that this fusion might date back to the common ancestor of this lineage.