Multi-omic characterization of allele-specific regulatory variation in hybrid pigs

Jianping Quan, Ming Yang, Xingwang Wang, Gengyuan Cai, Rongrong Ding, Zhanwei Zhuang, Shenping Zhou, Suxu Tan, Donglin Ruan, Jiajin Wu, Enqin Zheng, Zebin Zhang, Langqing Liu, Fanming Meng, Jie Wu, Cineng Xu, Yibin Qiu, Shiyuan Wang, Meng Lin, Shaoyun Li, Yong Ye, Fuchen Zhou, Danyang Lin, Xuehua Li, Shaoxiong Deng, Yuling Zhang, Zekai Yao, Xin Gao, Yingshan Yang, Yiyi Liu, Yuexin Zhan, Zhihong Liu, Jiaming Zhang, Fucai Ma, Jifei Yang, Qiaoer Chen, Jisheng Yang, Jian Ye, Linsong Dong, Ting Gu, Sixiu Huang, Zheng Xu, Zicong Li, Jie Yang (), Wen Huang () and Zhenfang Wu ()
Additional contact information
Jianping Quan: South China Agricultural University
Ming Yang: Zhongkai University of Agriculture and Engineering
Xingwang Wang: South China Agricultural University
Gengyuan Cai: South China Agricultural University
Rongrong Ding: South China Agricultural University
Zhanwei Zhuang: South China Agricultural University
Shenping Zhou: South China Agricultural University
Suxu Tan: Michigan State University
Donglin Ruan: South China Agricultural University
Jiajin Wu: South China Agricultural University
Enqin Zheng: South China Agricultural University
Zebin Zhang: South China Agricultural University
Langqing Liu: South China Agricultural University
Fanming Meng: South China Agricultural University
Jie Wu: South China Agricultural University
Cineng Xu: South China Agricultural University
Yibin Qiu: South China Agricultural University
Shiyuan Wang: South China Agricultural University
Meng Lin: South China Agricultural University
Shaoyun Li: South China Agricultural University
Yong Ye: South China Agricultural University
Fuchen Zhou: South China Agricultural University
Danyang Lin: South China Agricultural University
Xuehua Li: South China Agricultural University
Shaoxiong Deng: South China Agricultural University
Yuling Zhang: South China Agricultural University
Zekai Yao: South China Agricultural University
Xin Gao: Zhongkai University of Agriculture and Engineering
Yingshan Yang: South China Agricultural University
Yiyi Liu: South China Agricultural University
Yuexin Zhan: South China Agricultural University
Zhihong Liu: Zhongkai University of Agriculture and Engineering
Jiaming Zhang: South China Agricultural University
Fucai Ma: South China Agricultural University
Jifei Yang: South China Agricultural University
Qiaoer Chen: South China Agricultural University
Jisheng Yang: South China Agricultural University
Jian Ye: Ltd
Linsong Dong: Ltd
Ting Gu: South China Agricultural University
Sixiu Huang: South China Agricultural University
Zheng Xu: South China Agricultural University
Zicong Li: South China Agricultural University
Jie Yang: South China Agricultural University
Wen Huang: Michigan State University
Zhenfang Wu: South China Agricultural University

Nature Communications, 2024, vol. 15, issue 1, 1-18

Abstract: Abstract Hybrid mapping is a powerful approach to efficiently identify and characterize genes regulated through mechanisms in cis. In this study, using reciprocal crosses of the phenotypically divergent Duroc and Lulai pig breeds, we perform a comprehensive multi-omic characterization of regulatory variation across the brain, liver, muscle, and placenta through four developmental stages. We produce one of the largest multi-omic datasets in pigs to date, including 16 whole genome sequenced individuals, as well as 48 whole genome bisulfite sequencing, 168 ATAC-Seq and 168 RNA-Seq samples. We develop a read count-based method to reliably assess allele-specific methylation, chromatin accessibility, and RNA expression. We show that tissue specificity was much stronger than developmental stage specificity in all of DNA methylation, chromatin accessibility, and gene expression. We identify 573 genes showing allele specific expression, including those influenced by parent-of-origin as well as allele genotype effects. We integrate methylation, chromatin accessibility, and gene expression data to show that allele specific expression can be explained in great part by allele specific methylation and/or chromatin accessibility. This study provides a comprehensive characterization of regulatory variation across multiple tissues and developmental stages in pigs.

Date: 2024
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DOI: 10.1038/s41467-024-49923-5

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