Lucotte Elise A, Jay Paul, Rougemont Quentin, Boyer Loreleï, Cornille Amandine, Snirc Alodie, Labat Amandine, Chahine Elizabeth, Duhamel Marine, Namias Alice, Gendelman Jacob, Ma Wen-Juan, Hayes Roxanne K, Baruri Shikhi, Ham Joseph P, Perlin Michael H, Hood Michael E, Rodríguez de la Vega Ricardo C, Giraud Tatiana
Université Paris-Saclay, CNRS, AgroParisTech, Ecologie Société Evolution, Gif sur Yvette, France.
Center for GeoGenetics, University of Copenhagen, Copenhagen, Denmark.
Nat Commun. 2025 May 28;16(1):4962. doi: 10.1038/s41467-025-60222-5.
Basidiomycete fungi typically have two mating-type loci controlling mating compatibility, HD and PR, residing on different chromosomes. Loss-of-function in mating compatibility has been reported at the PR genes in a few heterothallic basidiomycetes, but not for the HD genes. In Microbotryum anther-smut fungi, there have been repeated linkage events between the HD and PR loci through chromosome fusions, leading to non-recombining regions. Here, we found that two sister Microbotryum species parasitizing Dianthus plants, M. superbum and M. shykoffianum, as well as the distantly related M. scorzonerae, have their HD and PR loci on different chromosomes, but with the PR chromosome fused with a part of the ancestral HD chromosome. In addition, recombination suppression has extended stepwise, generating evolutionary strata. In all three species, the HD genes lost their function in mating compatibility, natural diploid strains being often homozygous at the HD locus. Strains could be homozygous for a disrupted HD2 gene, that was hardly expressed during mating. Mating tests confirmed that a single genetic factor controlled mating compatibility and that haploid strains with identical HD alleles could mate and produce hyphae. This study shows that a unifactorial mating-type determinism can evolve, repeatedly, from a bifactorial system, by different mechanisms.
担子菌纲真菌通常有两个控制交配兼容性的交配型位点，即HD和PR，位于不同的染色体上。在一些异宗配合的担子菌中，已报道PR基因在交配兼容性方面存在功能丧失，但HD基因未出现这种情况。在微孢黑粉菌中，HD和PR位点之间通过染色体融合发生了多次连锁事件，导致了非重组区域。在这里，我们发现寄生在石竹属植物上的两个微孢黑粉菌姐妹种，即华丽微孢黑粉菌和希科夫微孢黑粉菌，以及亲缘关系较远的黑根微孢黑粉菌，它们的HD和PR位点位于不同的染色体上，但PR染色体与祖先HD染色体的一部分融合。此外，重组抑制已逐步扩展，形成了进化层。在所有这三个物种中，HD基因在交配兼容性方面失去了功能，天然二倍体菌株在HD位点通常是纯合的。菌株可能对一个被破坏的HD2基因纯合，该基因在交配过程中几乎不表达。交配试验证实，单一遗传因素控制交配兼容性，具有相同HD等位基因的单倍体菌株可以交配并产生菌丝。这项研究表明，单因子交配型决定机制可以通过不同的机制，从双因子系统中反复进化而来。
