The histone deacetylase UvHOS2 regulates vegetative growth, conidiation, ustilaginoidin synthesis, and pathogenicity in Ustilaginoidea virens
Abstract Ustilaginoidea virens causes rice false smut, one of the most devastating rice diseases. The pathogen produces various types of mycotoxins, such as ustilaginoidins and ustiloxins, which are harmful to both human and animal health. Histone deacetylases in fungi play an important role in regu...
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| Format: | Article |
| Language: | English |
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BMC
2024-03-01
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| Series: | Phytopathology Research |
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| Online Access: | https://doi.org/10.1186/s42483-024-00230-3 |
| _version_ | 1827321568242434048 |
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| author | Zhaoyi Long Peiying Wang Qianheng Yu Bo Wang Dayong Li Cui Yang Ling Liu Guohua Duan Wenxian Sun |
| author_facet | Zhaoyi Long Peiying Wang Qianheng Yu Bo Wang Dayong Li Cui Yang Ling Liu Guohua Duan Wenxian Sun |
| author_sort | Zhaoyi Long |
| collection | DOAJ |
| description | Abstract Ustilaginoidea virens causes rice false smut, one of the most devastating rice diseases. The pathogen produces various types of mycotoxins, such as ustilaginoidins and ustiloxins, which are harmful to both human and animal health. Histone deacetylases in fungi play an important role in regulating chromatin structure and gene expression. However, there is limited knowledge about how histone deacetylases control pathogenicity and mycotoxin biosynthesis in U. virens. Here, we characterize a putative class I histone deacetylase UvHOS2 in U. virens. The UvHos2-deletion mutants exhibit retarded vegetative growth, reduced conidial production and germination, and attenuated virulence. UvHOS2 positively regulates tolerance to various environmental stresses, including cell wall, cell membrane integrity, osmotic and oxidative stresses. UvHOS2 reduces the acetylation levels of histones at multiple Lys sites, including H3K9, H3K14, H3K27, and H3K56. ChIP-PCR assays revealed that UvHOS2-mediated H3K9 deacetylation regulates the expression of ustilaginoidin biosynthesis genes. Consistently, transcriptome analysis indicates that UvHOS2 regulates the expression of the genes involved in secondary metabolism, mycelial growth, conidiogenesis, and pathogenicity, thereby controlling U. virens virulence and mycotoxin (ustilaginoidins and sorbicillinoids) biosynthesis. This study provides a theoretical reference for revealing the epigenetic regulation of pathogenicity and mycotoxin biosynthesis in plant pathogenic fungi. |
| first_indexed | 2024-04-25T01:08:24Z |
| format | Article |
| id | doaj.art-a034339b728b41e79409e9054f172d4f |
| institution | Directory Open Access Journal |
| issn | 2524-4167 |
| language | English |
| last_indexed | 2024-04-25T01:08:24Z |
| publishDate | 2024-03-01 |
| publisher | BMC |
| record_format | Article |
| series | Phytopathology Research |
| spelling | doaj.art-a034339b728b41e79409e9054f172d4f2024-03-10T12:07:09ZengBMCPhytopathology Research2524-41672024-03-016111610.1186/s42483-024-00230-3The histone deacetylase UvHOS2 regulates vegetative growth, conidiation, ustilaginoidin synthesis, and pathogenicity in Ustilaginoidea virensZhaoyi Long0Peiying Wang1Qianheng Yu2Bo Wang3Dayong Li4Cui Yang5Ling Liu6Guohua Duan7Wenxian Sun8College of Plant Protection, Jilin Provincial Key Laboratory of Green Management of Crop Pests and Diseases, Jilin Agricultural UniversityCollege of Plant Protection, Jilin Provincial Key Laboratory of Green Management of Crop Pests and Diseases, Jilin Agricultural UniversityCollege of Plant Protection, Jilin Provincial Key Laboratory of Green Management of Crop Pests and Diseases, Jilin Agricultural UniversityDepartment of Plant Pathology, Ministry of Agriculture Key Laboratory of Pest Monitoring and Green Management, College of Plant Protection, China Agricultural UniversityCollege of Plant Protection, Jilin Provincial Key Laboratory of Green Management of Crop Pests and Diseases, Jilin Agricultural UniversityCollege of Plant Protection, Jilin Provincial Key Laboratory of Green Management of Crop Pests and Diseases, Jilin Agricultural UniversityCollege of Plant Protection, Jilin Provincial Key Laboratory of Green Management of Crop Pests and Diseases, Jilin Agricultural UniversityCollege of Plant Protection, Jilin Provincial Key Laboratory of Green Management of Crop Pests and Diseases, Jilin Agricultural UniversityCollege of Plant Protection, Jilin Provincial Key Laboratory of Green Management of Crop Pests and Diseases, Jilin Agricultural UniversityAbstract Ustilaginoidea virens causes rice false smut, one of the most devastating rice diseases. The pathogen produces various types of mycotoxins, such as ustilaginoidins and ustiloxins, which are harmful to both human and animal health. Histone deacetylases in fungi play an important role in regulating chromatin structure and gene expression. However, there is limited knowledge about how histone deacetylases control pathogenicity and mycotoxin biosynthesis in U. virens. Here, we characterize a putative class I histone deacetylase UvHOS2 in U. virens. The UvHos2-deletion mutants exhibit retarded vegetative growth, reduced conidial production and germination, and attenuated virulence. UvHOS2 positively regulates tolerance to various environmental stresses, including cell wall, cell membrane integrity, osmotic and oxidative stresses. UvHOS2 reduces the acetylation levels of histones at multiple Lys sites, including H3K9, H3K14, H3K27, and H3K56. ChIP-PCR assays revealed that UvHOS2-mediated H3K9 deacetylation regulates the expression of ustilaginoidin biosynthesis genes. Consistently, transcriptome analysis indicates that UvHOS2 regulates the expression of the genes involved in secondary metabolism, mycelial growth, conidiogenesis, and pathogenicity, thereby controlling U. virens virulence and mycotoxin (ustilaginoidins and sorbicillinoids) biosynthesis. This study provides a theoretical reference for revealing the epigenetic regulation of pathogenicity and mycotoxin biosynthesis in plant pathogenic fungi.https://doi.org/10.1186/s42483-024-00230-3Ustilaginoidea virensHistone deacetylasePathogenicityUstilaginoidinsBiosynthesis |
| spellingShingle | Zhaoyi Long Peiying Wang Qianheng Yu Bo Wang Dayong Li Cui Yang Ling Liu Guohua Duan Wenxian Sun The histone deacetylase UvHOS2 regulates vegetative growth, conidiation, ustilaginoidin synthesis, and pathogenicity in Ustilaginoidea virens Phytopathology Research Ustilaginoidea virens Histone deacetylase Pathogenicity Ustilaginoidins Biosynthesis |
| title | The histone deacetylase UvHOS2 regulates vegetative growth, conidiation, ustilaginoidin synthesis, and pathogenicity in Ustilaginoidea virens |
| title_full | The histone deacetylase UvHOS2 regulates vegetative growth, conidiation, ustilaginoidin synthesis, and pathogenicity in Ustilaginoidea virens |
| title_fullStr | The histone deacetylase UvHOS2 regulates vegetative growth, conidiation, ustilaginoidin synthesis, and pathogenicity in Ustilaginoidea virens |
| title_full_unstemmed | The histone deacetylase UvHOS2 regulates vegetative growth, conidiation, ustilaginoidin synthesis, and pathogenicity in Ustilaginoidea virens |
| title_short | The histone deacetylase UvHOS2 regulates vegetative growth, conidiation, ustilaginoidin synthesis, and pathogenicity in Ustilaginoidea virens |
| title_sort | histone deacetylase uvhos2 regulates vegetative growth conidiation ustilaginoidin synthesis and pathogenicity in ustilaginoidea virens |
| topic | Ustilaginoidea virens Histone deacetylase Pathogenicity Ustilaginoidins Biosynthesis |
| url | https://doi.org/10.1186/s42483-024-00230-3 |
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