Liquid–liquid phase separation of H3K27me3 reader BP1 regulates transcriptional repression
Abstract Background Bromo-adjacent homology-plant homeodomain domain containing protein 1 (BP1) is a reader of histone post-translational modifications in fungi. BP1 recognizes trimethylation of lysine 27 in histone H3 (H3K27me3), an epigenetic hallmark of gene silencing. However, whether and how BP...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2024-03-01
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| Series: | Genome Biology |
| Online Access: | https://doi.org/10.1186/s13059-024-03209-7 |
| _version_ | 1797259242593320960 |
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| author | Guangfei Tang Haoxue Xia Yufei Huang Yuanwen Guo Yun Chen Zhonghua Ma Wende Liu |
| author_facet | Guangfei Tang Haoxue Xia Yufei Huang Yuanwen Guo Yun Chen Zhonghua Ma Wende Liu |
| author_sort | Guangfei Tang |
| collection | DOAJ |
| description | Abstract Background Bromo-adjacent homology-plant homeodomain domain containing protein 1 (BP1) is a reader of histone post-translational modifications in fungi. BP1 recognizes trimethylation of lysine 27 in histone H3 (H3K27me3), an epigenetic hallmark of gene silencing. However, whether and how BP1 participates in transcriptional repression remains poorly understood. Results We report that BP1 forms phase-separated liquid condensates to modulate its biological function in Fusarium graminearum. Deletion assays reveal that intrinsically disordered region 2 (IDR2) of BP1 mediates its liquid–liquid phase separation. The phase separation of BP1 is indispensable for its interaction with suppressor of Zeste 12, a component of polycomb repressive complex 2. Furthermore, IDR2 deletion abolishes BP1-H3K27me3 binding and alleviates the transcriptional repression of secondary metabolism-related genes, especially deoxynivalenol mycotoxin biosynthesis genes. Conclusions BP1 maintains transcriptional repression by forming liquid–liquid phase-separated condensates, expanding our understanding of the relationship between post-translational modifications and liquid–liquid phase separation. |
| first_indexed | 2024-04-24T23:06:19Z |
| format | Article |
| id | doaj.art-bdbd56dad0e3479b824c8d85154b2318 |
| institution | Directory Open Access Journal |
| issn | 1474-760X |
| language | English |
| last_indexed | 2024-04-24T23:06:19Z |
| publishDate | 2024-03-01 |
| publisher | BMC |
| record_format | Article |
| series | Genome Biology |
| spelling | doaj.art-bdbd56dad0e3479b824c8d85154b23182024-03-17T12:27:49ZengBMCGenome Biology1474-760X2024-03-0125112410.1186/s13059-024-03209-7Liquid–liquid phase separation of H3K27me3 reader BP1 regulates transcriptional repressionGuangfei Tang0Haoxue Xia1Yufei Huang2Yuanwen Guo3Yun Chen4Zhonghua Ma5Wende Liu6State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural SciencesState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural SciencesState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural SciencesState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural SciencesState Key Laboratory of Rice Biology, Key Laboratory of Molecular Biology of Crop Pathogens and Insects, Institute of Biotechnology, Zhejiang UniversityState Key Laboratory of Rice Biology, Key Laboratory of Molecular Biology of Crop Pathogens and Insects, Institute of Biotechnology, Zhejiang UniversityState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural SciencesAbstract Background Bromo-adjacent homology-plant homeodomain domain containing protein 1 (BP1) is a reader of histone post-translational modifications in fungi. BP1 recognizes trimethylation of lysine 27 in histone H3 (H3K27me3), an epigenetic hallmark of gene silencing. However, whether and how BP1 participates in transcriptional repression remains poorly understood. Results We report that BP1 forms phase-separated liquid condensates to modulate its biological function in Fusarium graminearum. Deletion assays reveal that intrinsically disordered region 2 (IDR2) of BP1 mediates its liquid–liquid phase separation. The phase separation of BP1 is indispensable for its interaction with suppressor of Zeste 12, a component of polycomb repressive complex 2. Furthermore, IDR2 deletion abolishes BP1-H3K27me3 binding and alleviates the transcriptional repression of secondary metabolism-related genes, especially deoxynivalenol mycotoxin biosynthesis genes. Conclusions BP1 maintains transcriptional repression by forming liquid–liquid phase-separated condensates, expanding our understanding of the relationship between post-translational modifications and liquid–liquid phase separation.https://doi.org/10.1186/s13059-024-03209-7 |
| spellingShingle | Guangfei Tang Haoxue Xia Yufei Huang Yuanwen Guo Yun Chen Zhonghua Ma Wende Liu Liquid–liquid phase separation of H3K27me3 reader BP1 regulates transcriptional repression Genome Biology |
| title | Liquid–liquid phase separation of H3K27me3 reader BP1 regulates transcriptional repression |
| title_full | Liquid–liquid phase separation of H3K27me3 reader BP1 regulates transcriptional repression |
| title_fullStr | Liquid–liquid phase separation of H3K27me3 reader BP1 regulates transcriptional repression |
| title_full_unstemmed | Liquid–liquid phase separation of H3K27me3 reader BP1 regulates transcriptional repression |
| title_short | Liquid–liquid phase separation of H3K27me3 reader BP1 regulates transcriptional repression |
| title_sort | liquid liquid phase separation of h3k27me3 reader bp1 regulates transcriptional repression |
| url | https://doi.org/10.1186/s13059-024-03209-7 |
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