Repeated loss of function at HD mating-type genes and of recombination in anther-smut fungi
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...
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Nature Portfolio
2025-05-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-025-60222-5 |
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| author | 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 Tatiana Giraud |
| author_facet | 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 Tatiana Giraud |
| author_sort | Elise A. Lucotte |
| collection | DOAJ |
| description | 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. |
| format | Article |
| id | doaj-art-7d038cc106614b3489b671dcb75e9dff |
| institution | DOAJ |
| issn | 2041-1723 |
| language | English |
| publishDate | 2025-05-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj-art-7d038cc106614b3489b671dcb75e9dff2025-08-20T03:16:34ZengNature PortfolioNature Communications2041-17232025-05-0116112010.1038/s41467-025-60222-5Repeated loss of function at HD mating-type genes and of recombination in anther-smut fungiElise A. Lucotte0Paul Jay1Quentin Rougemont2Loreleï Boyer3Amandine Cornille4Alodie Snirc5Amandine Labat6Elizabeth Chahine7Marine Duhamel8Alice Namias9Jacob Gendelman10Wen-Juan Ma11Roxanne K. Hayes12Shikhi Baruri13Joseph P. Ham14Michael H. Perlin15Michael E. Hood16Ricardo C. Rodríguez de la Vega17Tatiana Giraud18Université Paris-Saclay, CNRS, AgroParisTech, Ecologie Société EvolutionUniversité Paris-Saclay, CNRS, AgroParisTech, Ecologie Société EvolutionUniversité Paris-Saclay, CNRS, AgroParisTech, Ecologie Société EvolutionUniversité Paris-Saclay, CNRS, AgroParisTech, Ecologie Société EvolutionUniversité Paris-Saclay, INRAE, CNRS, AgroParisTech, GQE—Le MoulonUniversité Paris-Saclay, CNRS, AgroParisTech, Ecologie Société EvolutionUniversité Paris-Saclay, CNRS, AgroParisTech, Ecologie Société EvolutionUniversité Paris-Saclay, CNRS, AgroParisTech, Ecologie Société EvolutionUniversité Paris-Saclay, CNRS, AgroParisTech, Ecologie Société EvolutionUniversité Paris-Saclay, CNRS, AgroParisTech, Ecologie Société EvolutionDepartment of Biology, Amherst CollegeDepartment of Biology, Amherst CollegeDepartment of Biology, Program on Disease Evolution, University of LouisvilleDepartment of Biology, Program on Disease Evolution, University of LouisvilleDepartment of Biology, Program on Disease Evolution, University of LouisvilleDepartment of Biology, Program on Disease Evolution, University of LouisvilleDepartment of Biology, Amherst CollegeUniversité Paris-Saclay, CNRS, AgroParisTech, Ecologie Société EvolutionUniversité Paris-Saclay, CNRS, AgroParisTech, Ecologie Société EvolutionAbstract 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.https://doi.org/10.1038/s41467-025-60222-5 |
| spellingShingle | 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 Tatiana Giraud Repeated loss of function at HD mating-type genes and of recombination in anther-smut fungi Nature Communications |
| title | Repeated loss of function at HD mating-type genes and of recombination in anther-smut fungi |
| title_full | Repeated loss of function at HD mating-type genes and of recombination in anther-smut fungi |
| title_fullStr | Repeated loss of function at HD mating-type genes and of recombination in anther-smut fungi |
| title_full_unstemmed | Repeated loss of function at HD mating-type genes and of recombination in anther-smut fungi |
| title_short | Repeated loss of function at HD mating-type genes and of recombination in anther-smut fungi |
| title_sort | repeated loss of function at hd mating type genes and of recombination in anther smut fungi |
| url | https://doi.org/10.1038/s41467-025-60222-5 |
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