Repeated loss of function at HD mating-type genes and of recombination in anther-smut fungi

Elise A. Lucotte (), Paul Jay, Quentin Rougemont, Loreleï Boyer, Amandine Cornille, Alodie Snirc, Amandine Labat, Elizabeth Chahine, Marine Duhamel, Alice Namias, Jacob Gendelman, Wen-Juan Ma, Roxanne K. Hayes, Shikhi Baruri, Joseph P. Ham, Michael H. Perlin, Michael E. Hood, Ricardo C. Rodríguez de la Vega and Tatiana Giraud ()
Additional contact information
Elise A. Lucotte: Ecologie Société Evolution
Paul Jay: Ecologie Société Evolution
Quentin Rougemont: Ecologie Société Evolution
Loreleï Boyer: Ecologie Société Evolution
Amandine Cornille: Université Paris-Saclay, INRAE, CNRS, AgroParisTech, GQE—Le Moulon
Alodie Snirc: Ecologie Société Evolution
Amandine Labat: Ecologie Société Evolution
Elizabeth Chahine: Ecologie Société Evolution
Marine Duhamel: Ecologie Société Evolution
Alice Namias: Ecologie Société Evolution
Jacob Gendelman: Amherst College
Wen-Juan Ma: Amherst College
Roxanne K. Hayes: University of Louisville
Shikhi Baruri: University of Louisville
Joseph P. Ham: University of Louisville
Michael H. Perlin: University of Louisville
Michael E. Hood: Amherst College
Ricardo C. Rodríguez de la Vega: Ecologie Société Evolution
Tatiana Giraud: Ecologie Société Evolution

Nature Communications, 2025, vol. 16, issue 1, 1-20

Abstract: Abstract 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.

Date: 2025
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DOI: 10.1038/s41467-025-60222-5

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