A pig BodyMap transcriptome reveals diverse tissue physiologies and evolutionary dynamics of transcription.

Long Jin, Qianzi Tang, Silu Hu, Zhongxu Chen, Xuming Zhou, Bo Zeng, Yuhao Wang, Mengnan He, Yan Li, Lixuan Gui, Linyuan Shen, Keren Long, Jideng Ma, Xun Wang, Zhengli Chen, Yanzhi Jiang, Guoqing Tang, Li Zhu, Fei Liu, Bo Zhang, Zhiqing Huang, Guisen Li, Diyan Li, Vadim N Gladyshev, Jingdong Yin, Yiren Gu, Xuewei Li, Mingzhou Li
Author Information
  1. Long Jin: Institute of Animal Genetics and Breeding, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, Sichuan, China. ORCID
  2. Qianzi Tang: Institute of Animal Genetics and Breeding, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, Sichuan, China. tangqianzi@sicau.edu.cn. ORCID
  3. Silu Hu: Institute of Animal Genetics and Breeding, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, Sichuan, China.
  4. Zhongxu Chen: Department of Life Science, Tcuni Inc., Chengdu, Sichuan, China.
  5. Xuming Zhou: Institute of Zoology, Chinese Academy of Sciences, Beijing, China.
  6. Bo Zeng: Institute of Animal Genetics and Breeding, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, Sichuan, China.
  7. Yuhao Wang: Institute of Animal Genetics and Breeding, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, Sichuan, China.
  8. Mengnan He: Institute of Animal Genetics and Breeding, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, Sichuan, China.
  9. Yan Li: Institute of Animal Genetics and Breeding, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, Sichuan, China.
  10. Lixuan Gui: Department of Life Science, Tcuni Inc., Chengdu, Sichuan, China.
  11. Linyuan Shen: Institute of Animal Genetics and Breeding, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, Sichuan, China.
  12. Keren Long: Institute of Animal Genetics and Breeding, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, Sichuan, China.
  13. Jideng Ma: Institute of Animal Genetics and Breeding, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, Sichuan, China.
  14. Xun Wang: Institute of Animal Genetics and Breeding, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, Sichuan, China.
  15. Zhengli Chen: Key Laboratory of Animal Disease and Human Health of Sichuan Province, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, China.
  16. Yanzhi Jiang: College of Life Science, Sichuan Agricultural University, Ya'an, Sichuan, China.
  17. Guoqing Tang: Institute of Animal Genetics and Breeding, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, Sichuan, China.
  18. Li Zhu: Institute of Animal Genetics and Breeding, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, Sichuan, China.
  19. Fei Liu: Information and Educational Technology Center, Sichuan Agricultural University, Chengdu, Sichuan, China.
  20. Bo Zhang: Ya'an Digital Economy Operation Company, Ya'an, Sichuan, China.
  21. Zhiqing Huang: Institute of Animal Nutrition, Sichuan Agricultural University, Chengdu, Sichuan, China. ORCID
  22. Guisen Li: Renal Department and Nephrology Institute, Sichuan Provincial People's Hospital, Chengdu, Sichuan, China. ORCID
  23. Diyan Li: Institute of Animal Genetics and Breeding, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, Sichuan, China. ORCID
  24. Vadim N Gladyshev: Division of Genetics, Department of Medicine, Brigham and Women's Hospital, Boston, MA, USA. ORCID
  25. Jingdong Yin: State Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing, China.
  26. Yiren Gu: Animal Breeding and Genetics Key Laboratory of Sichuan Province, Sichuan Animal Science Academy, Chengdu, Sichuan, China.
  27. Xuewei Li: Institute of Animal Genetics and Breeding, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, Sichuan, China.
  28. Mingzhou Li: Institute of Animal Genetics and Breeding, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, Sichuan, China. mingzhou.li@sicau.edu.cn. ORCID

Abstract

A comprehensive transcriptomic survey of pigs can provide a mechanistic understanding of tissue specialization processes underlying economically valuable traits and accelerate their use as a biomedical model. Here we characterize four transcript types (lncRNAs, TUCPs, miRNAs, and circRNAs) and protein-coding genes in 31 adult pig tissues and two cell lines. We uncover the transcriptomic variability among 47 skeletal muscles, and six adipose depots linked to their different origins, metabolism, cell composition, physical activity, and mitochondrial pathways. We perform comparative analysis of the transcriptomes of seven tissues from pigs and nine other vertebrates to reveal that evolutionary divergence in transcription potentially contributes to lineage-specific biology. Long-range promoter-enhancer interaction analysis in subcutaneous adipose tissues across species suggests evolutionarily stable transcription patterns likely attributable to redundant enhancers buffering gene expression patterns against perturbations, thereby conferring robustness during speciation. This study can facilitate adoption of the pig as a biomedical model for human biology and disease and uncovers the molecular bases of valuable traits.

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MeSH Term

Adipose Tissue
Alternative Splicing
Animals
Biological Evolution
Cell Line
Cell Lineage
Cell Nucleus
Enhancer Elements, Genetic
Evolution, Molecular
Gene Expression Profiling
Gene Regulatory Networks
MicroRNAs
Mitochondria
Molecular Conformation
Muscle, Skeletal
Myofibrils
Phylogeny
Promoter Regions, Genetic
RNA, Circular
RNA, Long Noncoding
RNA, Messenger
Spatial Analysis
Swine
Transcriptome

Chemicals

MicroRNAs
RNA, Circular
RNA, Long Noncoding
RNA, Messenger