Onset and stepwise extensions of recombination suppression are common in mating-type chromosomes of Microbotryum anther-smut fungi

Abstract

Sex chromosomes and mating-type chromosomes can display large genomic regions without recombination. Recombination suppression often extended stepwise with time away from the sex- or mating-type-determining genes, generating evolutionary strata of differentiation between alternative sex or mating-type chromosomes. In anther-smut fungi of the Microbotryum genus, recombination suppression evolved repeatedly, linking the two mating-type loci and extended multiple times in regions distal to the mating-type genes. Here, we obtained high-quality genome assemblies of alternative mating types for four Microbotryum fungi. We found an additional event of independent chromosomal rearrangements bringing the two mating-type loci on the same chromosome followed by recombination suppression linking them. We also found, in a new clade analysed here, that recombination suppression between the two mating-type loci occurred in several steps, with first an ancestral recombination suppression between one of the mating-type locus and its centromere; later, completion of recombination suppression up to the second mating-type locus occurred independently in three species. The estimated dates of recombination suppression between the mating-type loci ranged from 0.15 to 3.58 million years ago. In total, this makes at least nine independent events of linkage between the mating-type loci across the Microbotryum genus. Several mating-type locus linkage events occurred through the same types of chromosomal rearrangements, where similar chromosome fissions at centromeres represent convergence in the genomic changes leading to the phenotypic convergence. These findings further highlight Microbotryum fungi as excellent models to study the evolution of recombination suppression.

Tempo of Degeneration Across Independently Evolved Nonrecombining Regions

“…In the fungal genus Microbotryum , recombination suppression has evolved independently in several species, leading to mating-type chromosomes of different ages, some showing stepwise extension of recombination suppression and thereby the formation of evolutionary strata ( Branco et al 2017 , 2018 ; Carpentier et al 2019 ; Duhamel et al 2022 ). In these pathogenic anther-smut fungi, mating occurs mostly between haploid cells resulting from the same meiosis event (i.e., intratetrad mating or automixis [ Hood and Antonovics 2000 ]) and between cells bearing distinct alleles at the two mating-type loci, that is, the pheromone receptor (PR) locus (carrying pheromone and PR genes controlling gamete fusion) and the HD locus (carrying homeodomain genes whose proteins undergo dimerization to induce postmating growth).…”

“…The evolutionary strata linking HD and PR loci to each other or to centromeres were all called “black evolutionary strata”, though they corresponded to several independent events, often trapping different sets of genes. In some cases, the full recombination cessation linking the HD and PR loci occurred in several steps and the corresponding strata were distinguished as grey and black ( Duhamel et al 2022 ). Extensions of recombination suppression to nonmating-type genes were called colored evolutionary strata ( Branco et al 2017 , 2018 ).…”

Tempo of degeneration across independently evolved non-recombining regions

“…Multiple independent events of recombination suppression involving mating-type loci have been reported in anther-smut fungi (Branco, et al 2017; Branco, et al 2018; Carpentier, et al 2019; Duhamel, et al 2022). By sequencing and analysing the genomes of three additional Microbotryum species, we document three new independent events of mating-type chromosome rearrangements and fusions leading to PR-HD linkage, amounting to a total of eight such independent PR-HD linkage events in our present dataset.…”

“…In the fungal genus Microbotryum , recombination suppression has evolved independently in several species, leading to mating-type chromosomes of different ages, some showing stepwise extension of recombination suppression and thereby the formation of evolutionary strata (Branco, et al 2017; Branco, et al 2018; Carpentier, et al 2019; Duhamel, et al 2022). In these pathogenic anther-smut fungi, mating occurs mostly between haploid cells resulting from the same meiosis event ( i.e ., intra-tetrad mating or automixis (Hood and Antonovics 2000)) and between cells bearing distinct alleles at the two mating-type loci, i.e .…”

“…The evolutionary strata linking HD and PR loci to each other or to centromeres were all called “black evolutionary strata”, though they corresponded to several independent events, often trapping different sets of genes. In some cases, the full recombination cessation linking the HD and PR loci occurred in several steps and the corresponding strata were distinguished as grey and black (Duhamel, et al 2022). Extensions of recombination suppression to non-mating-type genes were called coloured evolutionary strata (Branco, et al 2017; Branco, et al 2018).…”