Degeneration of the non-recombining regions in the mating type chromosomes of the anther smut fungi. Mating type chromosomes of the anther smut fungi

Dimorphic mating-type chromosomes in fungi can aid in testing theoretical predictions about sex chromosome evolution. Indeed they can display similar cessation of recombination as sex chromosomes in dioecious plants and animals but without an association with male/female functions or asymmetries in copy number or sheltering. Our aim here was to assess whether degeneration has occurred in the non-recombining mating type chromosomes (a1 and a2 respectively) of the anther smut fungi (Microbotryum) in a manner analogous to sex chromosomes, where suppressed recombination and reduced effective population size limit the efficiency of natural selection. We used the a1 Microbotryum lychnidis-dioicae reference genome sequence, and we identified sequences from its large a1 and a2 mating type chromosomes after isolating them electrophoretically and sequencing them. Optical maps allowed identifying pseudoautosomal region sequences. Additionally, the genomes of twelve other Microbotryum species were sequenced. We found strong evidence of degeneration in the non-recombining regions of the mating type chromosomes, with significantly higher rates of non-synonymous mutations (dN/dS) and higher transposable element load than in pseudoautosomal regions or autosomes. A tendency for more frequent shifts from optimal to non-optimal codons was observed in most species. In addition, expression data revealed ca. 80 genes on the mating type chromosomes that were only expressed in cells of one mating type, some being completely lacking in the alternate mating types genome, suggesting mutations impairing expression and even genes deletion. The two haploid mating type chromosomes were not different in the levels of degeneration, consistent with the lack of homogametic/heterogametic asymmetry between them and contrasting X/Y or Z/W sex chromosomes. Our study thus shows that fungal mating type chromosomes are useful for a general understanding of evolution in regions of suppressed recombination and for comparison to expectations based on sex chromosomes.