Epigenomic and 3D genomic mapping reveals developmental dynamics and subgenomic asymmetry of transcriptional regulatory architecture in allotetraploid cotton
Abstract Although epigenetic modification has long been recognized as a vital force influencing gene regulation in plants, the dynamics of chromatin structure implicated in the intertwined transcriptional regulation of duplicated genes in polyploids have yet to be understood. Here, we document the d...
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Nature Portfolio
2024-12-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-024-55309-4 |
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| author | Xianhui Huang Yuejin Wang Sainan Zhang Liuling Pei Jiaqi You Yuexuan Long Jianying Li Xianlong Zhang Longfu Zhu Maojun Wang |
| author_facet | Xianhui Huang Yuejin Wang Sainan Zhang Liuling Pei Jiaqi You Yuexuan Long Jianying Li Xianlong Zhang Longfu Zhu Maojun Wang |
| author_sort | Xianhui Huang |
| collection | DOAJ |
| description | Abstract Although epigenetic modification has long been recognized as a vital force influencing gene regulation in plants, the dynamics of chromatin structure implicated in the intertwined transcriptional regulation of duplicated genes in polyploids have yet to be understood. Here, we document the dynamic organization of chromatin structure in two subgenomes of allotetraploid cotton (Gossypium hirsutum) by generating 3D genomic, epigenomic and transcriptomic datasets from 12 major tissues/developmental stages covering the life cycle. We systematically identify a subset of genes that are closely associated with specific tissue functions. Interestingly, these genes exhibit not only higher tissue specificity but also a more pronounced homoeologous bias. We comprehensively elucidate the intricate process of subgenomic collaboration and divergence across various tissues. A comparison among subgenomes in the 12 tissues reveals widespread differences in the reorganization of 3D genome structures, with the Dt subgenome exhibiting a higher extent of dynamic chromatin status than the At subgenome. Moreover, we construct a comprehensive atlas of putative functional genome elements and discover that 37 cis-regulatory elements (CREs) have selection signals acquired during domestication and improvement. These data and analyses are publicly available to the research community through a web portal. In summary, this study provides abundant resources and depicts the regulatory architecture of the genome, which thereby facilitates the understanding of biological processes and guides cotton breeding. |
| format | Article |
| id | doaj-art-b986cef600fc4005ae3f03d10dda8427 |
| institution | DOAJ |
| issn | 2041-1723 |
| language | English |
| publishDate | 2024-12-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj-art-b986cef600fc4005ae3f03d10dda84272025-08-20T02:39:38ZengNature PortfolioNature Communications2041-17232024-12-0115112010.1038/s41467-024-55309-4Epigenomic and 3D genomic mapping reveals developmental dynamics and subgenomic asymmetry of transcriptional regulatory architecture in allotetraploid cottonXianhui Huang0Yuejin Wang1Sainan Zhang2Liuling Pei3Jiaqi You4Yuexuan Long5Jianying Li6Xianlong Zhang7Longfu Zhu8Maojun Wang9National Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural UniversityNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural UniversityNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural UniversityNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural UniversityNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural UniversityNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural UniversityNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural UniversityNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural UniversityNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural UniversityNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural UniversityAbstract Although epigenetic modification has long been recognized as a vital force influencing gene regulation in plants, the dynamics of chromatin structure implicated in the intertwined transcriptional regulation of duplicated genes in polyploids have yet to be understood. Here, we document the dynamic organization of chromatin structure in two subgenomes of allotetraploid cotton (Gossypium hirsutum) by generating 3D genomic, epigenomic and transcriptomic datasets from 12 major tissues/developmental stages covering the life cycle. We systematically identify a subset of genes that are closely associated with specific tissue functions. Interestingly, these genes exhibit not only higher tissue specificity but also a more pronounced homoeologous bias. We comprehensively elucidate the intricate process of subgenomic collaboration and divergence across various tissues. A comparison among subgenomes in the 12 tissues reveals widespread differences in the reorganization of 3D genome structures, with the Dt subgenome exhibiting a higher extent of dynamic chromatin status than the At subgenome. Moreover, we construct a comprehensive atlas of putative functional genome elements and discover that 37 cis-regulatory elements (CREs) have selection signals acquired during domestication and improvement. These data and analyses are publicly available to the research community through a web portal. In summary, this study provides abundant resources and depicts the regulatory architecture of the genome, which thereby facilitates the understanding of biological processes and guides cotton breeding.https://doi.org/10.1038/s41467-024-55309-4 |
| spellingShingle | Xianhui Huang Yuejin Wang Sainan Zhang Liuling Pei Jiaqi You Yuexuan Long Jianying Li Xianlong Zhang Longfu Zhu Maojun Wang Epigenomic and 3D genomic mapping reveals developmental dynamics and subgenomic asymmetry of transcriptional regulatory architecture in allotetraploid cotton Nature Communications |
| title | Epigenomic and 3D genomic mapping reveals developmental dynamics and subgenomic asymmetry of transcriptional regulatory architecture in allotetraploid cotton |
| title_full | Epigenomic and 3D genomic mapping reveals developmental dynamics and subgenomic asymmetry of transcriptional regulatory architecture in allotetraploid cotton |
| title_fullStr | Epigenomic and 3D genomic mapping reveals developmental dynamics and subgenomic asymmetry of transcriptional regulatory architecture in allotetraploid cotton |
| title_full_unstemmed | Epigenomic and 3D genomic mapping reveals developmental dynamics and subgenomic asymmetry of transcriptional regulatory architecture in allotetraploid cotton |
| title_short | Epigenomic and 3D genomic mapping reveals developmental dynamics and subgenomic asymmetry of transcriptional regulatory architecture in allotetraploid cotton |
| title_sort | epigenomic and 3d genomic mapping reveals developmental dynamics and subgenomic asymmetry of transcriptional regulatory architecture in allotetraploid cotton |
| url | https://doi.org/10.1038/s41467-024-55309-4 |
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