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Molecular biology and evolution2019; 36(11); 2591-2603; doi: 10.1093/molbev/msz158

EPAS1 Gain-of-Function Mutation Contributes to High-Altitude Adaptation in Tibetan Horses.

Abstract: High altitude represents some of the most extreme environments worldwide. The genetic changes underlying adaptation to such environments have been recently identified in multiple animals but remain unknown in horses. Here, we sequence the complete genome of 138 domestic horses encompassing a whole altitudinal range across China to uncover the genetic basis for adaptation to high-altitude hypoxia. Our genome data set includes 65 lowland animals across ten Chinese native breeds, 61 horses living at least 3,300 m above sea level across seven locations along Qinghai-Tibetan Plateau, as well as 7 Thoroughbred and 5 Przewalski's horses added for comparison. We find that Tibetan horses do not descend from Przewalski's horses but were most likely introduced from a distinct horse lineage, following the emergence of pastoral nomadism in Northwestern China ∼3,700 years ago. We identify that the endothelial PAS domain protein 1 gene (EPAS1, also HIF2A) shows the strongest signature for positive selection in the Tibetan horse genome. Two missense mutations at this locus appear strongly associated with blood physiological parameters facilitating blood circulation as well as oxygen transportation and consumption in hypoxic conditions. Functional validation through protein mutagenesis shows that these mutations increase EPAS1 stability and its hetero dimerization affinity to ARNT (HIF1B). Our study demonstrates that missense mutations in the EPAS1 gene provided key evolutionary molecular adaptation to Tibetan horses living in high-altitude hypoxic environments. It reveals possible targets for genomic selection programs aimed at increasing hypoxia tolerance in livestock and provides a textbook example of evolutionary convergence across independent mammal lineages.
© The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.
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Publication Date: 2019-07-06 PubMed ID: 31273382PubMed Central: PMC6805228DOI: 10.1093/molbev/msz158Google Scholar: Lookup
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  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research article centers on the exploration of the genetic basis behind the high-altitude adaptation of Tibetan horses. This was done by studying the complete genome of 138 horses from various altitudes across China. They discovered that Tibetan horses likely developed from a different horse lineage, and the EPAS1 gene mutation played a key role in their successful adoption to high-altitude hypoxic environments.

Research Method

  • The researchers sequenced the complete genome of 138 domestic horses from different altitudes across China. The sample set includes lowland animals across ten breeds, horses living above 3,300 meters for seven locations along the Qinghai-Tibetan Plateau, and an additional 7 Thoroughbred and 5 Przewalski’s horses were included for comparative purposes.
  • Their objective was to uncover what genetic changes had occurred to allow these animals to adapt successfully to high altitude hypoxia environments, where oxygen levels in the air are extremely low.

Research Findings

  • The findings revealed that Tibetan horses do not descend from Przewalski’s horses, but likely originated from a different horse lineage. This hypothesis is supported by the emergence of pastoral nomadism in Northwestern China around 3,700 years ago.
  • A key discovery was that a gene known as the endothelial PAS domain protein 1 (EPAS1, also HIF2A) shows the strongest signature for positive selection in the Tibetan horse genome. This means that the mutations associated with this gene were beneficial for the horses’ survival in high altitude environments and thus, were passed down through generations.
  • Two missense mutations at the EPAS1 locus were strongly associated with physiological parameters related to blood circulation and oxygen transportation and consumption under hypoxic conditions. They found through protein mutagenesis that these mutations increased the stability of EPAS1 and its affinity to dimerize with ARNT (HIF1B), another gene.

Implications

  • This study sheds light on how missense mutations in the EPAS1 gene provided key evolutionary molecular adaptation in Tibetan horses for living in high-altitude hypoxic environments.
  • The research findings are not only important in understanding the evolution and adaptation of horses, but they also hold potential for genomic selection programs that aim to enhance hypoxia tolerance in livestock.
  • Furthermore, it is an example of evolutionary convergence across independent mammalian lineages, suggesting there may be a commonality in the genetic mechanism of high-altitude adaptation among various species.

Cite This Article

APA
Liu X, Zhang Y, Li Y, Pan J, Wang D, Chen W, Zheng Z, He X, Zhao Q, Pu Y, Guan W, Han J, Orlando L, Ma Y, Jiang L. (2019). EPAS1 Gain-of-Function Mutation Contributes to High-Altitude Adaptation in Tibetan Horses. Mol Biol Evol, 36(11), 2591-2603. https://doi.org/10.1093/molbev/msz158

Publication

Molecular biology and evolution
ISSN: 1537-1719
NlmUniqueID: 8501455
Country: United States
Language: English
Volume: 36
Issue: 11
Pages: 2591-2603

Researcher Affiliations

Liu, Xuexue
  • Laboratory of Animal (Poultry) Genetics Breeding and Reproduction, Ministry of Agriculture, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing, PR China.
  • CAAS-ILRI Joint Laboratory on Livestock and Forage Genetic Resources, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing, PR China.
Zhang, Yanli
  • Laboratory of Animal (Poultry) Genetics Breeding and Reproduction, Ministry of Agriculture, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing, PR China.
  • CAAS-ILRI Joint Laboratory on Livestock and Forage Genetic Resources, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing, PR China.
Li, Yefang
  • Laboratory of Animal (Poultry) Genetics Breeding and Reproduction, Ministry of Agriculture, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing, PR China.
  • CAAS-ILRI Joint Laboratory on Livestock and Forage Genetic Resources, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing, PR China.
Pan, Jianfei
  • Laboratory of Animal (Poultry) Genetics Breeding and Reproduction, Ministry of Agriculture, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing, PR China.
  • CAAS-ILRI Joint Laboratory on Livestock and Forage Genetic Resources, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing, PR China.
Wang, Dandan
  • Laboratory of Animal (Poultry) Genetics Breeding and Reproduction, Ministry of Agriculture, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing, PR China.
  • CAAS-ILRI Joint Laboratory on Livestock and Forage Genetic Resources, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing, PR China.
Chen, Weihuang
  • College of Animal Science and Technology, Northwest A&F University, Yangling, Shaanxi, PR China.
Zheng, Zhuqing
  • College of Animal Science and Technology, Northwest A&F University, Yangling, Shaanxi, PR China.
He, Xiaohong
  • Laboratory of Animal (Poultry) Genetics Breeding and Reproduction, Ministry of Agriculture, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing, PR China.
  • CAAS-ILRI Joint Laboratory on Livestock and Forage Genetic Resources, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing, PR China.
Zhao, Qianjun
  • Laboratory of Animal (Poultry) Genetics Breeding and Reproduction, Ministry of Agriculture, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing, PR China.
  • CAAS-ILRI Joint Laboratory on Livestock and Forage Genetic Resources, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing, PR China.
Pu, Yabin
  • Laboratory of Animal (Poultry) Genetics Breeding and Reproduction, Ministry of Agriculture, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing, PR China.
  • CAAS-ILRI Joint Laboratory on Livestock and Forage Genetic Resources, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing, PR China.
Guan, Weijun
  • Laboratory of Animal (Poultry) Genetics Breeding and Reproduction, Ministry of Agriculture, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing, PR China.
  • CAAS-ILRI Joint Laboratory on Livestock and Forage Genetic Resources, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing, PR China.
Han, Jianlin
  • CAAS-ILRI Joint Laboratory on Livestock and Forage Genetic Resources, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing, PR China.
  • International Livestock Research Institute (ILRI), Nairobi, Kenya.
Orlando, Ludovic
  • Lundbeck Foundation GeoGenetics Center, University of Copenhagen, Denmark.
  • Laboratoire d'Anthropobiologie Moléculaire et d'Imagerie de Synthèse, CNRS, UMR 5288, Université Paul Sabatier (UPS), Toulouse, France.
Ma, Yuehui
  • Laboratory of Animal (Poultry) Genetics Breeding and Reproduction, Ministry of Agriculture, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing, PR China.
  • CAAS-ILRI Joint Laboratory on Livestock and Forage Genetic Resources, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing, PR China.
Jiang, Lin
  • Laboratory of Animal (Poultry) Genetics Breeding and Reproduction, Ministry of Agriculture, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing, PR China.
  • CAAS-ILRI Joint Laboratory on Livestock and Forage Genetic Resources, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing, PR China.

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