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

Author

Listed:
  • Jianping Quan

    (South China Agricultural University
    Michigan State University
    South China Agricultural University
    Ltd)

  • Ming Yang

    (Zhongkai University of Agriculture and Engineering
    Yunfu Subcenter of Guangdong Laboratory for Lingnan Modern Agriculture)

  • Xingwang Wang

    (South China Agricultural University
    South China Agricultural University)

  • Gengyuan Cai

    (South China Agricultural University
    South China Agricultural University
    South China Agricultural University)

  • Rongrong Ding

    (South China Agricultural University
    Michigan State University
    Ltd
    Yunfu Subcenter of Guangdong Laboratory for Lingnan Modern Agriculture)

  • Zhanwei Zhuang

    (South China Agricultural University
    South China Agricultural University)

  • Shenping Zhou

    (South China Agricultural University
    South China Agricultural University)

  • Suxu Tan

    (Michigan State University)

  • Donglin Ruan

    (South China Agricultural University
    South China Agricultural University)

  • Jiajin Wu

    (South China Agricultural University
    South China Agricultural University
    South China Agricultural University)

  • Enqin Zheng

    (South China Agricultural University
    South China Agricultural University
    South China Agricultural University)

  • Zebin Zhang

    (South China Agricultural University
    South China Agricultural University
    South China Agricultural University)

  • Langqing Liu

    (South China Agricultural University
    South China Agricultural University
    South China Agricultural University)

  • Fanming Meng

    (South China Agricultural University
    Guangdong Key Laboratory of Animal Breeding and Nutrition)

  • Jie Wu

    (South China Agricultural University
    South China Agricultural University)

  • Cineng Xu

    (South China Agricultural University
    South China Agricultural University)

  • Yibin Qiu

    (South China Agricultural University
    South China Agricultural University)

  • Shiyuan Wang

    (South China Agricultural University
    South China Agricultural University)

  • Meng Lin

    (South China Agricultural University
    South China Agricultural University)

  • Shaoyun Li

    (South China Agricultural University
    South China Agricultural University)

  • Yong Ye

    (South China Agricultural University
    South China Agricultural University)

  • Fuchen Zhou

    (South China Agricultural University
    South China Agricultural University)

  • Danyang Lin

    (South China Agricultural University
    South China Agricultural University)

  • Xuehua Li

    (South China Agricultural University
    South China Agricultural University)

  • Shaoxiong Deng

    (South China Agricultural University
    South China Agricultural University)

  • Yuling Zhang

    (South China Agricultural University
    South China Agricultural University)

  • Zekai Yao

    (South China Agricultural University
    South China Agricultural University)

  • Xin Gao

    (Zhongkai University of Agriculture and Engineering)

  • Yingshan Yang

    (South China Agricultural University
    South China Agricultural University)

  • Yiyi Liu

    (South China Agricultural University
    South China Agricultural University)

  • Yuexin Zhan

    (South China Agricultural University
    South China Agricultural University)

  • Zhihong Liu

    (Zhongkai University of Agriculture and Engineering)

  • Jiaming Zhang

    (South China Agricultural University
    South China Agricultural University)

  • Fucai Ma

    (South China Agricultural University
    South China Agricultural University)

  • Jifei Yang

    (South China Agricultural University
    South China Agricultural University)

  • Qiaoer Chen

    (South China Agricultural University)

  • Jisheng Yang

    (South China Agricultural University)

  • Jian Ye

    (Ltd
    Yunfu Subcenter of Guangdong Laboratory for Lingnan Modern Agriculture)

  • Linsong Dong

    (Ltd
    Yunfu Subcenter of Guangdong Laboratory for Lingnan Modern Agriculture)

  • Ting Gu

    (South China Agricultural University
    South China Agricultural University)

  • Sixiu Huang

    (South China Agricultural University
    South China Agricultural University)

  • Zheng Xu

    (South China Agricultural University
    South China Agricultural University)

  • Zicong Li

    (South China Agricultural University
    South China Agricultural University)

  • Jie Yang

    (South China Agricultural University
    South China Agricultural University
    South China Agricultural University)

  • Wen Huang

    (Michigan State University)

  • Zhenfang Wu

    (South China Agricultural University
    Ltd
    Yunfu Subcenter of Guangdong Laboratory for Lingnan Modern Agriculture)

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.

Suggested Citation

  • 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 Men, 2024. "Multi-omic characterization of allele-specific regulatory variation in hybrid pigs," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49923-5
    DOI: 10.1038/s41467-024-49923-5
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    References listed on IDEAS

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