Comprehensive multi‐tissue epigenome atlas in sheep: A resource for complex traits, domestication, and breeding

Abstract Comprehensive functional genome annotation is crucial to elucidate the molecular mechanisms of agronomic traits in livestock, yet systematic functional annotation of the sheep genome is lacking. Here, we generated 92 transcriptomic and epigenomic data sets from nine major tissues, along wit...

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Main Authors: Deyin Zhang, Jiangbo Cheng, Xiaolong Li, Kai Huang, Lvfeng Yuan, Yuan Zhao, Dan Xu, Yukun Zhang, Liming Zhao, Xiaobin Yang, Zongwu Ma, Quanzhong Xu, Chong Li, Xiaojuan Wang, Chen Zheng, Defu Tang, Fang Nian, Xiangpeng Yue, Wanhong Li, Huibin Tian, Xiuxiu Weng, Peng Hu, Yuanqing Feng, Peter Kalds, Zhihua Jiang, Yunxia Zhao, Xiaoxue Zhang, Fadi Li, Weimin Wang
Format: Article
Language:English
Published: Wiley 2024-12-01
Series:iMeta
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Online Access:https://doi.org/10.1002/imt2.254
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author Deyin Zhang
Jiangbo Cheng
Xiaolong Li
Kai Huang
Lvfeng Yuan
Yuan Zhao
Dan Xu
Yukun Zhang
Liming Zhao
Xiaobin Yang
Zongwu Ma
Quanzhong Xu
Chong Li
Xiaojuan Wang
Chen Zheng
Defu Tang
Fang Nian
Xiangpeng Yue
Wanhong Li
Huibin Tian
Xiuxiu Weng
Peng Hu
Yuanqing Feng
Peter Kalds
Zhihua Jiang
Yunxia Zhao
Xiaoxue Zhang
Fadi Li
Weimin Wang
author_facet Deyin Zhang
Jiangbo Cheng
Xiaolong Li
Kai Huang
Lvfeng Yuan
Yuan Zhao
Dan Xu
Yukun Zhang
Liming Zhao
Xiaobin Yang
Zongwu Ma
Quanzhong Xu
Chong Li
Xiaojuan Wang
Chen Zheng
Defu Tang
Fang Nian
Xiangpeng Yue
Wanhong Li
Huibin Tian
Xiuxiu Weng
Peng Hu
Yuanqing Feng
Peter Kalds
Zhihua Jiang
Yunxia Zhao
Xiaoxue Zhang
Fadi Li
Weimin Wang
author_sort Deyin Zhang
collection DOAJ
description Abstract Comprehensive functional genome annotation is crucial to elucidate the molecular mechanisms of agronomic traits in livestock, yet systematic functional annotation of the sheep genome is lacking. Here, we generated 92 transcriptomic and epigenomic data sets from nine major tissues, along with whole‐genome data from 2357 individuals across 29 breeds worldwide, and 4006 phenotypic data related to tail fat weight. We constructed the first multi‐tissue epigenome atlas in terms of functional elements, chromatin states, and their functions and explored the utility of the functional elements in interpreting phenotypic variation during sheep domestication and improvement. Particularly, we identified a total of 753,723 nonredundant functional elements, with over 60% being novel. We found tissue‐specific promoters and enhancers related to sensory abilities and immune response that were highly enriched in genomic regions influenced by domestication, while longissimus dorsi tissue‐specific active enhancers and tail fat tissue‐specific active promoters were highly enriched in genomic regions influenced by breeding and improvement. Notably, a variant, Chr13:51760995A>C, located in an enhancer region, was identified as a causal variant for tail fat deposition based on multi‐layered data sets. Overall, this research provides foundational resources and a successful case for future investigations of complex traits in sheep through the integration of multi‐omics data sets.
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spelling doaj-art-3f9c574f78b945c1939d7c8c406c61212025-08-20T02:39:52ZengWileyiMeta2770-596X2024-12-0136n/an/a10.1002/imt2.254Comprehensive multi‐tissue epigenome atlas in sheep: A resource for complex traits, domestication, and breedingDeyin Zhang0Jiangbo Cheng1Xiaolong Li2Kai Huang3Lvfeng Yuan4Yuan Zhao5Dan Xu6Yukun Zhang7Liming Zhao8Xiaobin Yang9Zongwu Ma10Quanzhong Xu11Chong Li12Xiaojuan Wang13Chen Zheng14Defu Tang15Fang Nian16Xiangpeng Yue17Wanhong Li18Huibin Tian19Xiuxiu Weng20Peng Hu21Yuanqing Feng22Peter Kalds23Zhihua Jiang24Yunxia Zhao25Xiaoxue Zhang26Fadi Li27Weimin Wang28State Key Laboratory of Herbage Improvement and Grassland Agro‐ecosystems; Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Afairs; Engineering Research Center of Grassland Industry, Ministry of Education; College of Pastoral Agriculture Science and Technology Lanzhou University Lanzhou ChinaState Key Laboratory of Herbage Improvement and Grassland Agro‐ecosystems; Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Afairs; Engineering Research Center of Grassland Industry, Ministry of Education; College of Pastoral Agriculture Science and Technology Lanzhou University Lanzhou ChinaState Key Laboratory of Herbage Improvement and Grassland Agro‐ecosystems; Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Afairs; Engineering Research Center of Grassland Industry, Ministry of Education; College of Pastoral Agriculture Science and Technology Lanzhou University Lanzhou ChinaState Key Laboratory of Herbage Improvement and Grassland Agro‐ecosystems; Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Afairs; Engineering Research Center of Grassland Industry, Ministry of Education; College of Pastoral Agriculture Science and Technology Lanzhou University Lanzhou ChinaLanzhou Veterinary Research Institute Chinese Academy of Agricultural Sciences (CAAS) Lanzhou ChinaState Key Laboratory of Herbage Improvement and Grassland Agro‐ecosystems; Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Afairs; Engineering Research Center of Grassland Industry, Ministry of Education; College of Pastoral Agriculture Science and Technology Lanzhou University Lanzhou ChinaCollege of Animal Science and Technology Gansu Agricultural University Lanzhou ChinaState Key Laboratory of Herbage Improvement and Grassland Agro‐ecosystems; Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Afairs; Engineering Research Center of Grassland Industry, Ministry of Education; College of Pastoral Agriculture Science and Technology Lanzhou University Lanzhou ChinaState Key Laboratory of Herbage Improvement and Grassland Agro‐ecosystems; Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Afairs; Engineering Research Center of Grassland Industry, Ministry of Education; College of Pastoral Agriculture Science and Technology Lanzhou University Lanzhou ChinaCollege of Animal Science and Technology Gansu Agricultural University Lanzhou ChinaCollege of Animal Science and Technology Gansu Agricultural University Lanzhou ChinaState Key Laboratory of Herbage Improvement and Grassland Agro‐ecosystems; Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Afairs; Engineering Research Center of Grassland Industry, Ministry of Education; College of Pastoral Agriculture Science and Technology Lanzhou University Lanzhou ChinaCollege of Animal Science and Technology Gansu Agricultural University Lanzhou ChinaCollege of Animal Science and Technology Gansu Agricultural University Lanzhou ChinaCollege of Animal Science and Technology Gansu Agricultural University Lanzhou ChinaCollege of Animal Science and Technology Gansu Agricultural University Lanzhou ChinaCollege of Science Gansu Agricultural University Lanzhou ChinaState Key Laboratory of Herbage Improvement and Grassland Agro‐ecosystems; Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Afairs; Engineering Research Center of Grassland Industry, Ministry of Education; College of Pastoral Agriculture Science and Technology Lanzhou University Lanzhou ChinaState Key Laboratory of Herbage Improvement and Grassland Agro‐ecosystems; Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Afairs; Engineering Research Center of Grassland Industry, Ministry of Education; College of Pastoral Agriculture Science and Technology Lanzhou University Lanzhou ChinaState Key Laboratory of Herbage Improvement and Grassland Agro‐ecosystems; Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Afairs; Engineering Research Center of Grassland Industry, Ministry of Education; College of Pastoral Agriculture Science and Technology Lanzhou University Lanzhou ChinaState Key Laboratory of Herbage Improvement and Grassland Agro‐ecosystems; Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Afairs; Engineering Research Center of Grassland Industry, Ministry of Education; College of Pastoral Agriculture Science and Technology Lanzhou University Lanzhou ChinaKey Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education Shanghai Ocean University Shanghai ChinaDepartment of Genetics University of Pennsylvania Philadelphia PA USAYazhouwan National Laboratory Sanya ChinaDepartment of Animal Sciences and Center for Reproductive Biology Washington State University (WSU) Pullman WA USAKey Laboratory of Agricultural Animal Genetics, Breeding, and Reproduction of the Ministry of Education Huazhong Agricultural University Wuhan ChinaCollege of Animal Science and Technology Gansu Agricultural University Lanzhou ChinaState Key Laboratory of Herbage Improvement and Grassland Agro‐ecosystems; Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Afairs; Engineering Research Center of Grassland Industry, Ministry of Education; College of Pastoral Agriculture Science and Technology Lanzhou University Lanzhou ChinaState Key Laboratory of Herbage Improvement and Grassland Agro‐ecosystems; Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Afairs; Engineering Research Center of Grassland Industry, Ministry of Education; College of Pastoral Agriculture Science and Technology Lanzhou University Lanzhou ChinaAbstract Comprehensive functional genome annotation is crucial to elucidate the molecular mechanisms of agronomic traits in livestock, yet systematic functional annotation of the sheep genome is lacking. Here, we generated 92 transcriptomic and epigenomic data sets from nine major tissues, along with whole‐genome data from 2357 individuals across 29 breeds worldwide, and 4006 phenotypic data related to tail fat weight. We constructed the first multi‐tissue epigenome atlas in terms of functional elements, chromatin states, and their functions and explored the utility of the functional elements in interpreting phenotypic variation during sheep domestication and improvement. Particularly, we identified a total of 753,723 nonredundant functional elements, with over 60% being novel. We found tissue‐specific promoters and enhancers related to sensory abilities and immune response that were highly enriched in genomic regions influenced by domestication, while longissimus dorsi tissue‐specific active enhancers and tail fat tissue‐specific active promoters were highly enriched in genomic regions influenced by breeding and improvement. Notably, a variant, Chr13:51760995A>C, located in an enhancer region, was identified as a causal variant for tail fat deposition based on multi‐layered data sets. Overall, this research provides foundational resources and a successful case for future investigations of complex traits in sheep through the integration of multi‐omics data sets.https://doi.org/10.1002/imt2.254multi‐omicsepigenomicsregulatory elementsgenome‐wide association studiesBMP2sheep
spellingShingle Deyin Zhang
Jiangbo Cheng
Xiaolong Li
Kai Huang
Lvfeng Yuan
Yuan Zhao
Dan Xu
Yukun Zhang
Liming Zhao
Xiaobin Yang
Zongwu Ma
Quanzhong Xu
Chong Li
Xiaojuan Wang
Chen Zheng
Defu Tang
Fang Nian
Xiangpeng Yue
Wanhong Li
Huibin Tian
Xiuxiu Weng
Peng Hu
Yuanqing Feng
Peter Kalds
Zhihua Jiang
Yunxia Zhao
Xiaoxue Zhang
Fadi Li
Weimin Wang
Comprehensive multi‐tissue epigenome atlas in sheep: A resource for complex traits, domestication, and breeding
iMeta
multi‐omics
epigenomics
regulatory elements
genome‐wide association studies
BMP2
sheep
title Comprehensive multi‐tissue epigenome atlas in sheep: A resource for complex traits, domestication, and breeding
title_full Comprehensive multi‐tissue epigenome atlas in sheep: A resource for complex traits, domestication, and breeding
title_fullStr Comprehensive multi‐tissue epigenome atlas in sheep: A resource for complex traits, domestication, and breeding
title_full_unstemmed Comprehensive multi‐tissue epigenome atlas in sheep: A resource for complex traits, domestication, and breeding
title_short Comprehensive multi‐tissue epigenome atlas in sheep: A resource for complex traits, domestication, and breeding
title_sort comprehensive multi tissue epigenome atlas in sheep a resource for complex traits domestication and breeding
topic multi‐omics
epigenomics
regulatory elements
genome‐wide association studies
BMP2
sheep
url https://doi.org/10.1002/imt2.254
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