Degeneration of the Nonrecombining Regions in the Mating-Type Chromosomes of the Anther-Smut Fungi

Abstract

Dimorphic mating-type chromosomes in fungi are excellent models for understanding the genomic consequences of recombination suppression. Their suppressed recombination and reduced effective population size are expected to limit the efficacy of natural selection, leading to genomic degeneration. Our aim was to identify the sequences of the mating-type chromosomes (a1 and a2) of the anther-smut fungi and to investigate degeneration in their nonrecombining regions. We used the haploid a1 Microbotryum lychnidis-dioicae reference genome sequence. The a1 and a2 mating-type chromosomes were both isolated electrophoretically and sequenced. Integration with restriction-digest optical maps identified regions of recombination and nonrecombination in the mating-type chromosomes. Genome sequence data were also obtained for 12 other Microbotryum species. We found strong evidence of degeneration across the genus in the nonrecombining regions of the mating-type chromosomes, with significantly higher rates of nonsynonymous substitution (dN/dS) than in nonmating-type chromosomes or in recombining regions of the mating-type chromosomes. The nonrecombining regions of the mating-type chromosomes also showed high transposable element content, weak gene expression, and gene losses. The levels of degeneration did not differ between the a1 and a2 mating-type chromosomes, consistent with the lack of homogametic/heterogametic asymmetry between them, and contrasting with X/Y or Z/W sex chromosomes.

Polymorphic Microsatellite Markers for the Tetrapolar Anther-Smut Fungus Microbotryum saponariae Based on Genome Sequencing

“…90% of the chromosome length. These genomic data are consistent with previous findings based on marker segregation analyses and optical maps [26–28]. This large non-recombining region explains why M .…”

Introgression maintains the genetic integrity of the mating-type determining chromosome of the fungus Neurospora tetrasperma

“…Signatures of molecular degeneration associated with recombination suppression have been reported in Neurospora and Microbotryum (Hood et al 2004;Fontanillas et al 2015). There are massive changes in architecture on the Microbotryum mating-type chromosome , a pattern also reported from one of the N. tetrasperma strains (Ellison et al 2011b), and further studies using high quality genomic data have the potential to reveal the commonality of such rearrangements and their link to recombination suppression of fungal mat chromosomes.…”

“…Recombination suppression on the chromosome carrying the mating-type locus has evolved independently in several fungal species distantly related to N. tetrasperma, including Podospora, Cryptococcus, and Microbotryum (Fraser and Heitman 2004;Grognet et al 2014;Fontanillas et al 2015) and contributes to our understanding of different aspects of eukaryote genome evolution. Signatures of molecular degeneration associated with recombination suppression have been reported in Neurospora and Microbotryum (Hood et al 2004;Fontanillas et al 2015).…”

“…Low, or suppressed, recombination leads to a reduction in effective population size (N e ) through selection at linked sites; thereby the efficacy of selection is reduced and we expect an increased mutational load (Bachtrog and Charlesworth 2002;Charlesworth and Charlesworth 2010). The link between recombination suppression and molecular degeneration has been observed in the sex-and mating-type determining genomic regions of a number of taxa across all eukaryote kingdoms (e.g., Bachtrog 2003;Hood et al 2004;Liu et al 2004;Marais et al 2008;Whittle and Johannesson 2011;Whittle et al 2011a;Fontanillas et al 2015) and is one of the main factors expected to favor either rare recombination events on sex chromosomes (Malcom et al 2014) or a high turnover of chromosomes harboring the sex-determining loci (Blaser et al 2013). …”

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

“…Previous studies addressing MAT gene content and organization in Pucciniomycotina yeasts suggested that mating type-determining regions of these species might encompass a relatively large portion of a chromosome (Coelho et al 2010;Petit et al 2012;Hood et al 2013;Fontanillas et al 2014;Whittle et al 2015). We therefore considered that defining MAT regions in L. scottii would benefit from obtaining genome sequences of two strains of compatible mating types since, unlike the rest of the genome, MAT loci should be clearly distinct in what concerns sequence divergence and gene organization.…”