Comparative transcriptomics of 5 high-altitude vertebrates and their low-altitude relatives.

Qianzi Tang, Yiren Gu, Xuming Zhou, Long Jin, Jiuqiang Guan, Rui Liu, Jing Li, Kereng Long, Shilin Tian, Tiandong Che, Silu Hu, Yan Liang, Xuemei Yang, Xuan Tao, Zhijun Zhong, Guosong Wang, Xiaohui Chen, Diyan Li, Jideng Ma, Xun Wang, Miaomiao Mai, An'an Jiang, Xiaolin Luo, Xuebin Lv, Vadim N Gladyshev, Xuewei Li, Mingzhou Li
Author Information
  1. Qianzi Tang: Institute of Animal Genetics and Breeding, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu 611130, China.
  2. Yiren Gu: Animal Breeding and Genetics Key Laboratory of Sichuan Province, Pig Science Institute, Sichuan Animal Science Academy, Chengdu 610066, China.
  3. Xuming Zhou: Division of Genetics, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts, 02115 USA.
  4. Long Jin: Institute of Animal Genetics and Breeding, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu 611130, China.
  5. Jiuqiang Guan: Yak Research Institute, Sichuan Academy of Grassland Science, Chengdu 610097, China.
  6. Rui Liu: Institute of Animal Genetics and Breeding, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu 611130, China.
  7. Jing Li: Institute of Animal Genetics and Breeding, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu 611130, China.
  8. Kereng Long: Institute of Animal Genetics and Breeding, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu 611130, China.
  9. Shilin Tian: Institute of Animal Genetics and Breeding, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu 611130, China.
  10. Tiandong Che: Institute of Animal Genetics and Breeding, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu 611130, China.
  11. Silu Hu: Institute of Animal Genetics and Breeding, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu 611130, China.
  12. Yan Liang: Animal Breeding and Genetics Key Laboratory of Sichuan Province, Pig Science Institute, Sichuan Animal Science Academy, Chengdu 610066, China.
  13. Xuemei Yang: Animal Breeding and Genetics Key Laboratory of Sichuan Province, Pig Science Institute, Sichuan Animal Science Academy, Chengdu 610066, China.
  14. Xuan Tao: Animal Breeding and Genetics Key Laboratory of Sichuan Province, Pig Science Institute, Sichuan Animal Science Academy, Chengdu 610066, China.
  15. Zhijun Zhong: Animal Breeding and Genetics Key Laboratory of Sichuan Province, Pig Science Institute, Sichuan Animal Science Academy, Chengdu 610066, China.
  16. Guosong Wang: Institute of Animal Genetics and Breeding, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu 611130, China.
  17. Xiaohui Chen: Animal Breeding and Genetics Key Laboratory of Sichuan Province, Pig Science Institute, Sichuan Animal Science Academy, Chengdu 610066, China.
  18. Diyan Li: Institute of Animal Genetics and Breeding, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu 611130, China.
  19. Jideng Ma: Institute of Animal Genetics and Breeding, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu 611130, China.
  20. Xun Wang: Institute of Animal Genetics and Breeding, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu 611130, China.
  21. Miaomiao Mai: Institute of Animal Genetics and Breeding, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu 611130, China.
  22. An'an Jiang: Institute of Animal Genetics and Breeding, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu 611130, China.
  23. Xiaolin Luo: Yak Research Institute, Sichuan Academy of Grassland Science, Chengdu 610097, China.
  24. Xuebin Lv: Animal Breeding and Genetics Key Laboratory of Sichuan Province, Pig Science Institute, Sichuan Animal Science Academy, Chengdu 610066, China.
  25. Vadim N Gladyshev: Division of Genetics, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts, 02115 USA.
  26. Xuewei Li: Institute of Animal Genetics and Breeding, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu 611130, China.
  27. Mingzhou Li: Institute of Animal Genetics and Breeding, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu 611130, China.

Abstract

Background: Species living at high altitude are subject to strong selective pressures due to inhospitable environments (e.g., hypoxia, low temperature, high solar radiation, and lack of biological production), making these species valuable models for comparative analyses of local adaptation. Studies that have examined high-altitude adaptation have identified a vast array of rapidly evolving genes that characterize the dramatic phenotypic changes in high-altitude animals. However, how high-altitude environment shapes gene expression programs remains largely unknown.
Findings: We generated a total of 910 Gb of high-quality RNA-seq data for 180 samples derived from 6 tissues of 5 agriculturally important high-altitude vertebrates (Tibetan chicken, Tibetan pig, Tibetan sheep, Tibetan goat, and yak) and their cross-fertile relatives living in geographically neighboring low-altitude regions. Of these, ∼75% reads could be aligned to their respective reference genomes, and on average ∼60% of annotated protein coding genes in each organism showed FPKM expression values greater than 0.5. We observed a general concordance in topological relationships between the nucleotide alignments and gene expression-based trees. Tissue and species accounted for markedly more variance than altitude based on either the expression or the alternative splicing patterns. Cross-species clustering analyses showed a tissue-dominated pattern of gene expression and a species-dominated pattern for alternative splicing. We also identified numerous differentially expressed genes that could potentially be involved in phenotypic divergence shaped by high-altitude adaptation.
Conclusions: These data serve as a valuable resource for examining the convergence and divergence of gene expression changes between species as they adapt or acclimatize to high-altitude environments.

Keywords

References

  1. Science. 2012 Dec 21;338(6114):1587-93 [PMID: 23258890]
  2. Nat Biotechnol. 2010 May;28(5):511-5 [PMID: 20436464]
  3. Nature. 2004 Dec 9;432(7018):695-716 [PMID: 15592404]
  4. Science. 2009 Apr 24;324(5926):522-8 [PMID: 19390049]
  5. Nucleic Acids Res. 2006 Jan 1;34(Database issue):D572-80 [PMID: 16381935]
  6. Genome Res. 2017 May;27(5):865-874 [PMID: 27646534]
  7. Bioinformatics. 2004 Jan 22;20(2):289-90 [PMID: 14734327]
  8. Nat Genet. 2013 Dec;45(12):1431-8 [PMID: 24162736]
  9. Bioinformatics. 2010 Mar 1;26(5):589-95 [PMID: 20080505]
  10. Science. 2012 Dec 21;338(6114):1593-9 [PMID: 23258891]
  11. Gigascience. 2017 Dec 1;6(12):1-9 [PMID: 29149296]
  12. Genome Res. 2010 Sep;20(9):1297-303 [PMID: 20644199]
  13. Science. 2014 Jun 6;344(6188):1168-1173 [PMID: 24904168]
  14. Genome Res. 2009 Feb;19(2):327-35 [PMID: 19029536]
  15. Genome Biol. 2003;4(5):P3 [PMID: 12734009]
  16. Nature. 2011 Oct 19;478(7369):343-8 [PMID: 22012392]
  17. Nat Biotechnol. 2013 Feb;31(2):135-41 [PMID: 23263233]
  18. Bioinformatics. 2009 May 1;25(9):1105-11 [PMID: 19289445]
  19. Genome Res. 2002 Jun;12(6):996-1006 [PMID: 12045153]
  20. Nature. 2012 Nov 15;491(7424):393-8 [PMID: 23151582]
  21. Science. 2015 May 8;348(6235):660-5 [PMID: 25954002]
  22. Nat Genet. 2012 Jul 01;44(8):946-9 [PMID: 22751099]

MeSH Term

Acclimatization
Alternative Splicing
Altitude
Animals
Cattle
Chickens
Gene Expression Profiling
Genome
Goats
Phylogeny
Sheep
Swine
Transcriptome
Whole Genome Sequencing