Epigenomic and 3D genomic mapping reveals developmental dynamics and subgenomic asymmetry of transcriptional regulatory architecture in allotetraploid cotton

• Published in: Nature communications 2024-12, Vol.15 (1), p.10721-20, Article 10721
• Main Authors: Huang, Xianhui, Wang, Yuejin, Zhang, Sainan, Pei, Liuling, You, Jiaqi, Long, Yuexuan, Li, Jianying, Zhang, Xianlong, Zhu, Longfu, Wang, Maojun
• Format: Article
• Language: English
• Subjects: 45/15; 631/208/177; 631/208/742/3933; 631/449/2653; Biological activity; Breeding; Chromatin; Chromatin - genetics; Chromatin - metabolism; Chromosome Mapping; Cotton; Data acquisition; Developmental stages; Divergence; Domestication; Epigenesis, Genetic; Epigenetics; Epigenomics - methods; Functionals; Gene duplication; Gene Expression Regulation, Plant; Gene mapping; Gene regulation; Genes; Genome, Plant; Genomes; Genomics; Genomics - methods; Gossypium - genetics; Gossypium - growth & development; Gossypium - metabolism; Humanities and Social Sciences; Life cycles; multidisciplinary; Plant breeding; Polyploidy; Regulatory sequences; Science; Science (multidisciplinary); Tetraploidy; Tissues; Transcriptomics
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-024-55309-4

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. This study describes comprehensive dynamic divergence of subgenomes in allotetraploid cotton, with an focus on cis-regulatory elements and 3D genomic architecture at 12 major tissues/developmental stages throughout the life cycle.