Genetic structure and evolutionary diversity of mating-type (MAT) loci in Hypsizygus marmoreus
Abstract The mating compatibility in fungi is generally governed by genes located within a single or two unlinked mating type (MAT) loci. Hypsizygus marmoreus is an edible mushroom in the order Agaricales with a tetrapolar system, which contains two unlinked MAT loci-homeodomain (HD) transcription f...
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2021-12-01
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| Online Access: | https://doi.org/10.1186/s43008-021-00086-8 |
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| author | Gang Wang Yuanyuan Wang Lianfu Chen Hongbo Wang Lin Guo Xuan Zhou Meijie Dou Baiyu Wang Jingxian Lin Lei Liu Zhengchao Wang Youjin Deng Jisen Zhang |
| author_facet | Gang Wang Yuanyuan Wang Lianfu Chen Hongbo Wang Lin Guo Xuan Zhou Meijie Dou Baiyu Wang Jingxian Lin Lei Liu Zhengchao Wang Youjin Deng Jisen Zhang |
| author_sort | Gang Wang |
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| description | Abstract The mating compatibility in fungi is generally governed by genes located within a single or two unlinked mating type (MAT) loci. Hypsizygus marmoreus is an edible mushroom in the order Agaricales with a tetrapolar system, which contains two unlinked MAT loci-homeodomain (HD) transcription factor genes and pheromone/pheromone receptor genes (P/R). In this study, we analyzed the genetic structure and diversity of MAT loci in tetrapolar system of H. marmoreus through sequencing of 54 heterokaryon and 8 homokaryon strains. Although within the HD loci, the gene order was conserved, the gene contents were variable, and the HD loci haplotypes were further classified into four types. By analyzing the structure, phylogeny, and the HD transmissibility based on the progeny of these four HD mating-type loci types, we found that they were heritable and tightly linked at the HD loci. The P/R loci genes were found to comprise three pheromone receptors, three pheromones, and two pheromone receptor-like genes. Intra- and inter-specific phylogenetic analyses of pheromone receptors revealed that the STE3 genes were divided into three groups, and we thus theorize that they diverged before speciation. Comparative analysis of the MAT regions among 73 Basidiomycete species indicated that the diversity of HD and P/R loci in Agaricales and Boletales may contribute to mating compatibility. The number of HD genes were not correlated with the tetrapolar or bipolar systems. In H. marmoreus, the expression levels of these genes at HD and P/R loci of compatible strains were found higher than in those of homonuclear/homokaryotic strains, indicating that these mating genes acted as switches for mating processes. Further collinear analysis of HD loci in interspecific species found that HD loci contains conserved recombination hotspots showing major rearrangements in Coprinopsis cinerea and Schizophyllum commune, suggesting different mechanisms for evolution of physically linked MAT loci in these groups. It seems likely that gene rearrangements are common in Agaricales fungi around HD loci. Together, our study provides insights into the genomic basis of mating compatibility in H. marmoreus. |
| format | Article |
| id | doaj-art-e7f7171eaa884603827d402d40303cab |
| institution | Kabale University |
| issn | 2210-6359 |
| language | English |
| publishDate | 2021-12-01 |
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| series | IMA Fungus |
| spelling | doaj-art-e7f7171eaa884603827d402d40303cab2025-02-02T12:29:48ZengBMCIMA Fungus2210-63592021-12-0112111610.1186/s43008-021-00086-8Genetic structure and evolutionary diversity of mating-type (MAT) loci in Hypsizygus marmoreusGang Wang0Yuanyuan Wang1Lianfu Chen2Hongbo Wang3Lin Guo4Xuan Zhou5Meijie Dou6Baiyu Wang7Jingxian Lin8Lei Liu9Zhengchao Wang10Youjin Deng11Jisen Zhang12Jiangsu Key Laboratory for Bioresources of Saline Soils, Jiangsu Provincial Key Laboratory of Coastal Wetland Bioresources and Environmental Protection, Jiangsu Synthetic Innovation Center for Coastal Bio-Agriculture, Yancheng Teachers UniversityCenter for Genomics and Biotechnology, Haixia Institute of Science and Technology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, College of Life Sciences, Fujian Agriculture and Forestry UniversityCollege of Plant Sciences and Technology, Huazhong Agricultural UniversityCenter for Genomics and Biotechnology, Haixia Institute of Science and Technology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, College of Life Sciences, Fujian Agriculture and Forestry UniversityCenter for Genomics and Biotechnology, Haixia Institute of Science and Technology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, College of Life Sciences, Fujian Agriculture and Forestry UniversityCollege of Crop Science, Fujian Agriculture and Forestry UniversityCollege of Crop Science, Fujian Agriculture and Forestry UniversityCenter for Genomics and Biotechnology, Haixia Institute of Science and Technology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, College of Life Sciences, Fujian Agriculture and Forestry UniversityCollege of Crop Science, Fujian Agriculture and Forestry UniversityCenter for Genomics and Biotechnology, Haixia Institute of Science and Technology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, College of Life Sciences, Fujian Agriculture and Forestry UniversityProvincial Key Laboratory for Developmental Biology and Neurosciences, College of Life Sciences, Fujian Normal UniversityCenter for Genomics and Biotechnology, Haixia Institute of Science and Technology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, College of Life Sciences, Fujian Agriculture and Forestry UniversityCenter for Genomics and Biotechnology, Haixia Institute of Science and Technology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, College of Life Sciences, Fujian Agriculture and Forestry UniversityAbstract The mating compatibility in fungi is generally governed by genes located within a single or two unlinked mating type (MAT) loci. Hypsizygus marmoreus is an edible mushroom in the order Agaricales with a tetrapolar system, which contains two unlinked MAT loci-homeodomain (HD) transcription factor genes and pheromone/pheromone receptor genes (P/R). In this study, we analyzed the genetic structure and diversity of MAT loci in tetrapolar system of H. marmoreus through sequencing of 54 heterokaryon and 8 homokaryon strains. Although within the HD loci, the gene order was conserved, the gene contents were variable, and the HD loci haplotypes were further classified into four types. By analyzing the structure, phylogeny, and the HD transmissibility based on the progeny of these four HD mating-type loci types, we found that they were heritable and tightly linked at the HD loci. The P/R loci genes were found to comprise three pheromone receptors, three pheromones, and two pheromone receptor-like genes. Intra- and inter-specific phylogenetic analyses of pheromone receptors revealed that the STE3 genes were divided into three groups, and we thus theorize that they diverged before speciation. Comparative analysis of the MAT regions among 73 Basidiomycete species indicated that the diversity of HD and P/R loci in Agaricales and Boletales may contribute to mating compatibility. The number of HD genes were not correlated with the tetrapolar or bipolar systems. In H. marmoreus, the expression levels of these genes at HD and P/R loci of compatible strains were found higher than in those of homonuclear/homokaryotic strains, indicating that these mating genes acted as switches for mating processes. Further collinear analysis of HD loci in interspecific species found that HD loci contains conserved recombination hotspots showing major rearrangements in Coprinopsis cinerea and Schizophyllum commune, suggesting different mechanisms for evolution of physically linked MAT loci in these groups. It seems likely that gene rearrangements are common in Agaricales fungi around HD loci. Together, our study provides insights into the genomic basis of mating compatibility in H. marmoreus.https://doi.org/10.1186/s43008-021-00086-8BasidiomycotaHypsizygus marmoreusSexual reproductionMating-typeTetrapolar |
| spellingShingle | Gang Wang Yuanyuan Wang Lianfu Chen Hongbo Wang Lin Guo Xuan Zhou Meijie Dou Baiyu Wang Jingxian Lin Lei Liu Zhengchao Wang Youjin Deng Jisen Zhang Genetic structure and evolutionary diversity of mating-type (MAT) loci in Hypsizygus marmoreus IMA Fungus Basidiomycota Hypsizygus marmoreus Sexual reproduction Mating-type Tetrapolar |
| title | Genetic structure and evolutionary diversity of mating-type (MAT) loci in Hypsizygus marmoreus |
| title_full | Genetic structure and evolutionary diversity of mating-type (MAT) loci in Hypsizygus marmoreus |
| title_fullStr | Genetic structure and evolutionary diversity of mating-type (MAT) loci in Hypsizygus marmoreus |
| title_full_unstemmed | Genetic structure and evolutionary diversity of mating-type (MAT) loci in Hypsizygus marmoreus |
| title_short | Genetic structure and evolutionary diversity of mating-type (MAT) loci in Hypsizygus marmoreus |
| title_sort | genetic structure and evolutionary diversity of mating type mat loci in hypsizygus marmoreus |
| topic | Basidiomycota Hypsizygus marmoreus Sexual reproduction Mating-type Tetrapolar |
| url | https://doi.org/10.1186/s43008-021-00086-8 |
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