Haplotype mapping of H3K27me3-associated chromatin interactions defines topological regulation of gene silencing in rice

• Published in: Cell reports (Cambridge) Vol. 42; no. 4; p. 112350
• Main Authors: Ouyang, Weizhi, Zhang, Xiwen, Guo, Minrong, Wang, Jing, Wang, Xiaoting, Gao, Runxin, Ma, Meng, Xiang, Xu, Luan, Shiping, Xing, Feng, Cao, Zhilin, Yan, Jiapei, Li, Guoliang, Li, Xingwang
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 25.04.2023; Elsevier
• Subjects: 3D genome; allele-specific expression; chromatin interaction; CP: Molecular biology; CP: Plants; gene silencing; haplotype; silencer; CP: Plants; silencer; haplotype; allele-specific expression; gene silencing; CP: Molecular biology; 3D genome; chromatin interaction
• ISSN: 2211-1247; 2211-1247
• DOI: 10.1016/j.celrep.2023.112350

Histone modification H3K27me3 is an important chromatin mark that plays vital roles in repressing expression of developmental genes. Here, we construct high-resolution 3D genome maps using long-read chromatin interaction analysis by paired-end tag sequencing (ChIA-PET) and characterize H3K27me3-associated chromatin interactions in an elite rice hybrid, Shanyou 63. We find that many H3K27me3-marked regions may function as silencer-like regulatory elements. The silencer-like elements can come into proximity with distal target genes via forming chromatin loops in 3D space of the nuclei, regulating gene silencing and plant traits. Natural and induced deletion of silencers upregulate expression of distal connected genes. Furthermore, we identify extensive allele-specific chromatin loops. We find that genetic variations alter allelic chromatin topology, thus modulating allelic gene imprinting in rice hybrids. In conclusion, the characterization of silencer-like regulatory elements and haplotype-resolved chromatin interaction maps provide insights into the understanding of molecular mechanisms underlying allelic gene silencing and plant trait controlling. [Display omitted] •H3K27me3 peak clusters may function as super silencer-like regulatory elements•Silencer-like regulatory elements regulate gene silencing via chromatin interactions•Deletion of silencers leads to chromatin loop disruption and gene upregulation•Allelic chromatin topology regulates allelic gene silencing in rice hybrids By haplotype mapping of H3K27me3-associated chromatin interactions in rice hybrids, Ouyang et al. show that silencer-like regulatory elements regulate distal gene silencing by forming long-range chromatin interactions and find that genetic variations between the two parental alleles alter allelic chromatin topology and allele-specific gene silencing.