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

Author

Listed:
  • Elise A. Lucotte

    (Ecologie Société Evolution)

  • Paul Jay

    (Ecologie Société Evolution
    University of Copenhagen)

  • 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
    Vrije Universiteit Brussel)

  • 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)

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.

Suggested Citation

  • 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 , 2025. "Repeated loss of function at HD mating-type genes and of recombination in anther-smut fungi," Nature Communications, Nature, vol. 16(1), pages 1-20, December.
    • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-60222-5
    DOI: 10.1038/s41467-025-60222-5
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    References listed on IDEAS

    as
    1. Alison E. Wright & Rebecca Dean & Fabian Zimmer & Judith E. Mank, 2016. "How to make a sex chromosome," Nature Communications, Nature, vol. 7(1), pages 1-8, November.
    2. Vincent Ranwez & Sébastien Harispe & Frédéric Delsuc & Emmanuel J P Douzery, 2011. "MACSE: Multiple Alignment of Coding SEquences Accounting for Frameshifts and Stop Codons," PLOS ONE, Public Library of Science, vol. 6(9), pages 1-10, September.
    3. Marine Duhamel & Michael E. Hood & Ricardo C. Rodríguez de la Vega & Tatiana Giraud, 2023. "Dynamics of transposable element accumulation in the non-recombining regions of mating-type chromosomes in anther-smut fungi," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
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