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

Summary: 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 H3K2...

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Main Authors: Weizhi Ouyang, Xiwen Zhang, Minrong Guo, Jing Wang, Xiaoting Wang, Runxin Gao, Meng Ma, Xu Xiang, Shiping Luan, Feng Xing, Zhilin Cao, Jiapei Yan, Guoliang Li, Xingwang Li
Format: Article
Language:English
Published: Elsevier 2023-04-01
Series:Cell Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124723003613
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author Weizhi Ouyang
Xiwen Zhang
Minrong Guo
Jing Wang
Xiaoting Wang
Runxin Gao
Meng Ma
Xu Xiang
Shiping Luan
Feng Xing
Zhilin Cao
Jiapei Yan
Guoliang Li
Xingwang Li
author_facet Weizhi Ouyang
Xiwen Zhang
Minrong Guo
Jing Wang
Xiaoting Wang
Runxin Gao
Meng Ma
Xu Xiang
Shiping Luan
Feng Xing
Zhilin Cao
Jiapei Yan
Guoliang Li
Xingwang Li
author_sort Weizhi Ouyang
collection DOAJ
description Summary: 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.
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spelling doaj.art-db596e8e7c3346f0a12d5f44522631fa2023-04-19T04:22:34ZengElsevierCell Reports2211-12472023-04-01424112350Haplotype mapping of H3K27me3-associated chromatin interactions defines topological regulation of gene silencing in riceWeizhi Ouyang0Xiwen Zhang1Minrong Guo2Jing Wang3Xiaoting Wang4Runxin Gao5Meng Ma6Xu Xiang7Shiping Luan8Feng Xing9Zhilin Cao10Jiapei Yan11Guoliang Li12Xingwang Li13National Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan 430070, ChinaNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan 430070, ChinaNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan 430070, ChinaNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan 430070, ChinaNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan 430070, ChinaNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan 430070, ChinaNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan 430070, ChinaNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan 430070, ChinaNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan 430070, ChinaCollege of Life Science, Xinyang Normal University, Xinyang 464000, ChinaDepartment of Resources and Environment, Henan University of Engineering, Zhengzhou 451191, ChinaNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan 430070, ChinaNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan 430070, China; Shenzhen Institute of Nutrition and Health, Huazhong Agricultural University, Wuhan, China; Shenzhen Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China; Corresponding authorNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan 430070, China; Shenzhen Institute of Nutrition and Health, Huazhong Agricultural University, Wuhan, China; Shenzhen Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China; Corresponding authorSummary: 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.http://www.sciencedirect.com/science/article/pii/S2211124723003613CP: PlantsCP: Molecular biology
spellingShingle Weizhi Ouyang
Xiwen Zhang
Minrong Guo
Jing Wang
Xiaoting Wang
Runxin Gao
Meng Ma
Xu Xiang
Shiping Luan
Feng Xing
Zhilin Cao
Jiapei Yan
Guoliang Li
Xingwang Li
Haplotype mapping of H3K27me3-associated chromatin interactions defines topological regulation of gene silencing in rice
Cell Reports
CP: Plants
CP: Molecular biology
title Haplotype mapping of H3K27me3-associated chromatin interactions defines topological regulation of gene silencing in rice
title_full Haplotype mapping of H3K27me3-associated chromatin interactions defines topological regulation of gene silencing in rice
title_fullStr Haplotype mapping of H3K27me3-associated chromatin interactions defines topological regulation of gene silencing in rice
title_full_unstemmed Haplotype mapping of H3K27me3-associated chromatin interactions defines topological regulation of gene silencing in rice
title_short Haplotype mapping of H3K27me3-associated chromatin interactions defines topological regulation of gene silencing in rice
title_sort haplotype mapping of h3k27me3 associated chromatin interactions defines topological regulation of gene silencing in rice
topic CP: Plants
CP: Molecular biology
url http://www.sciencedirect.com/science/article/pii/S2211124723003613
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