RT Journal Article
SR Electronic
T1 Convergent evolution of linked mating-type loci in basidiomycetes: an ancient fusion event that has stood the test of time
JF bioRxiv
FD Cold Spring Harbor Laboratory
SP 626911
DO 10.1101/626911
A1 Sheng Sun
A1 Marco A. Coelho
A1 Joseph Heitman
A1 Minou Nowrousian
YR 2019
UL http://biorxiv.org/content/early/2019/05/05/626911.abstract
AB Sexual development is a key evolutionary innovation of eukaryotes. In many species involves the interaction of 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 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 basidiomycete species with bipolar (unifactorial) mating systems, which can arise through genomic linkage of the HD and P/R loci. In the Tremellales, which comprise mostly yeast-like species, bipolarity is found only in the pathogenic Cryptococci, e.g. in the well-studied human pathogen Cryptococcus neoformans. Here, we describe the analysis of MAT loci from the Trichosporonales, a sister group to the Tremellales. We analyzed genome sequences from 29 strains comprising 24 species, including two new genome sequences generated in this study. Somewhat surprisingly, in all of the species analyzed, the MAT loci are fused and a single HD gene is present in each allele. This is similar to the organization in the pathogenic Cryptococci, which also have linked MAT loci and carry only one HD gene per MAT locus instead of the usual two HD genes found in the vast majority of basidiomycetes. However, almost all Trichosporonales strains analyzed carry either the combination of the HD gene SXI1 with the pheromone allele STE3a, or the combination of the SXI2 gene and STE3α allele. This is in contrast to MAT alleles in C. neoformans, where SXI1 is linked with STE3α, and SXI2 is linked with STE3a. The differences in allele combinations as well as the existence of tetrapolar Tremellales sister species to the bipolar Cryptococci suggest that the fusion of the HD and P/R loci and the loss of one HD gene per allele occurred independently in the Trichosporonales and the pathogenic Cryptococci, supporting the hypothesis of convergent evolution at the molecular level towards fused mating-type regions in fungi. A phylogenetic analysis of divergence times suggests that the MAT fusion in the Trichosporonales is the oldest fusion of MAT loci observed to date.Author summary Sexual development in fungi is governed by mating-type (MAT) genes, and the corresponding MAT loci show similarities to sex chromosomes in animals and plants. One common feature is an evolutionary trend towards combining sex-associated genes on the same chromosome, which can evolve by selection because it facilitates linkage of favorable allele combinations. Here, we show that this occurred in the Trichosporonales, a sister group to the Tremellales, similar to the expanded, fused MAT loci discovered previously in the human pathogen Cryptococcus neoformans. Our data suggest that fusion of MAT loci occurred independently in the Trichosporonales and pathogenic Cryptococci, supporting the hypothesis of convergent evolution towards fused MAT regions in fungi.