OpenLB
Open Library of Bioscience
Advanced Search
Nature genetics
08, 2016;48 (8): 947-52.

Genomic analysis of snub-nosed monkeys (Rhinopithecus) identifies genes and processes related to high-altitude adaptation.

Li Yu, Guo-Dong Wang, Jue Ruan, Yong-Bin Chen, Cui-Ping Yang, Xue Cao, Hong Wu, Yan-Hu Liu, Zheng-Lin Du, Xiao-Ping Wang, Jing Yang, Shao-Chen Cheng, Li Zhong, Lu Wang, Xuan Wang, Jing-Yang Hu, Lu Fang, Bing Bai, Kai-Le Wang, Na Yuan, Shi-Fang Wu, Bao-Guo Li, Jin-Guo Zhang, Ye-Qin Yang, Cheng-Lin Zhang, Yong-Cheng Long, Hai-Shu Li, Jing-Yuan Yang, David M Irwin, Oliver A Ryder, Ying Li, Chung-I Wu, Ya-Ping Zhang
Author Information
  1. Li Yu: State Key Laboratory for Conservation and Utilization of Bio-resource in Yunnan, Yunnan University, Kunming, China.
  2. Guo-Dong Wang: State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, China.
  3. Jue Ruan: Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing, China.
  4. Yong-Bin Chen: Key Laboratory of Animal Models and Human Disease Mechanisms of the Chinese Academy of Sciences and Yunnan Province, Kunming Institute of Zoology, Kunming, China.
  5. Cui-Ping Yang: Key Laboratory of Animal Models and Human Disease Mechanisms of the Chinese Academy of Sciences and Yunnan Province, Kunming Institute of Zoology, Kunming, China.
  6. Xue Cao: State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, China.
  7. Hong Wu: State Key Laboratory for Conservation and Utilization of Bio-resource in Yunnan, Yunnan University, Kunming, China.
  8. Yan-Hu Liu: State Key Laboratory for Conservation and Utilization of Bio-resource in Yunnan, Yunnan University, Kunming, China.
  9. Zheng-Lin Du: Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing, China.
  10. Xiao-Ping Wang: State Key Laboratory for Conservation and Utilization of Bio-resource in Yunnan, Yunnan University, Kunming, China.
  11. Jing Yang: State Key Laboratory for Conservation and Utilization of Bio-resource in Yunnan, Yunnan University, Kunming, China.
  12. Shao-Chen Cheng: State Key Laboratory for Conservation and Utilization of Bio-resource in Yunnan, Yunnan University, Kunming, China.
  13. Li Zhong: State Key Laboratory for Conservation and Utilization of Bio-resource in Yunnan, Yunnan University, Kunming, China.
  14. Lu Wang: State Key Laboratory for Conservation and Utilization of Bio-resource in Yunnan, Yunnan University, Kunming, China.
  15. Xuan Wang: State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, China.
  16. Jing-Yang Hu: State Key Laboratory for Conservation and Utilization of Bio-resource in Yunnan, Yunnan University, Kunming, China.
  17. Lu Fang: Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing, China.
  18. Bing Bai: State Key Laboratory for Conservation and Utilization of Bio-resource in Yunnan, Yunnan University, Kunming, China.
  19. Kai-Le Wang: Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing, China.
  20. Na Yuan: Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing, China.
  21. Shi-Fang Wu: State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, China.
  22. Bao-Guo Li: College of Life Sciences, Northwest University, Xi'an, China.
  23. Jin-Guo Zhang: Beijing Key Laboratory of Captive Wildlife Technologies, Beijing Zoo, Beijing, China.
  24. Ye-Qin Yang: Fanjing Mountain National Nature Reserve, Guizhou, China.
  25. Cheng-Lin Zhang: Beijing Key Laboratory of Captive Wildlife Technologies, Beijing Zoo, Beijing, China.
  26. Yong-Cheng Long: Institue of Primatology and Human Evolution, Sun Yat-Sen University, Guangzhou, China.
  27. Hai-Shu Li: Nujiang Prefecture Forestry Bureau, Yunnan, China.
  28. Jing-Yuan Yang: Shennongjia National Nature Reserve, Hubei, China.
  29. David M Irwin: Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, Ontario, Canada.
  30. Oliver A Ryder: San Diego Zoo Institute for Conservation Research, Escondido, California, USA.
  31. Ying Li: Institute of Animal Genetics and Breeding, Sichuan Agricultural University, Ya'an, China.
  32. Chung-I Wu: Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing, China.
  33. Ya-Ping Zhang: State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, China.
PMID: 27399969 DOI: 10.1038/ng.3615

Abstract

The snub-nosed monkey genus Rhinopithecus includes five closely related species distributed across altitudinal gradients from 800 to 4,500 m. Rhinopithecus bieti, Rhinopithecus roxellana, and Rhinopithecus strykeri inhabit high-altitude habitats, whereas Rhinopithecus brelichi and Rhinopithecus avunculus inhabit lowland regions. We report the de novo whole-genome sequence of R. bieti and genomic sequences for the four other species. Eight shared substitutions were found in six genes related to lung function, DNA repair, and angiogenesis in the high-altitude snub-nosed monkeys. Functional assays showed that the high-altitude variant of CDT1 (Ala537Val) renders cells more resistant to UV irradiation, and the high-altitude variants of RNASE4 (Asn89Lys and Thr128Ile) confer enhanced ability to induce endothelial tube formation in vitro. Genomic scans in the R. bieti and R. roxellana populations identified signatures of selection between and within populations at genes involved in functions relevant to high-altitude adaptation. These results provide valuable insights into the adaptation to high altitude in the snub-nosed monkeys.

References

Mol Med Rep. 2012 Sep;6(3):631-8 [PMID: 22736055]
Mol Biol Evol. 2000 Apr;17(4):540-52 [PMID: 10742046]
Proc Natl Acad Sci U S A. 2010 May 11;107(19):8666-71 [PMID: 20421465]
Am J Hum Genet. 2001 Dec;69(6):1378-84 [PMID: 11704930]
Syst Biol. 2009 Oct;58(5):468-77 [PMID: 20525601]
Nature. 2011 Jul 13;475(7357):493-6 [PMID: 21753753]
Cell. 2008 Oct 17;135(2):261-71 [PMID: 18957201]
Proc Biol Sci. 2012 Sep 7;279(1742):3491-500 [PMID: 22628470]
PLoS One. 2012;7(9):e46480 [PMID: 23029527]
Nature. 2013 Jul 25;499(7459):471-5 [PMID: 23823723]
Syst Biol. 2002 Jun;51(3):492-508 [PMID: 12079646]
Physiol Genomics. 2014 Jan 15;46(2):39-56 [PMID: 24220328]
Forensic Sci Int. 2009 Nov 20;192(1-3):53-5 [PMID: 19709828]
PLoS Genet. 2012;8(12 ):e1003110 [PMID: 23236293]
J Lipid Res. 2007 Dec;48(12):2736-50 [PMID: 17762044]
Genome Biol Evol. 2014 Aug;6(8):2122-8 [PMID: 25091388]
Mol Med Rep. 2010 Jan-Feb;3(1):127-32 [PMID: 21472211]
Genome Res. 2014 Aug;24(8):1308-15 [PMID: 24721644]
Science. 2010 Jul 2;329(5987):75-8 [PMID: 20595611]
Bioinformatics. 2001 Dec;17(12):1246-7 [PMID: 11751242]
Proc Natl Acad Sci U S A. 2002 Aug 6;99(16):10282-6 [PMID: 12142464]
Genome Biol. 2013 Apr 25;14(4):R36 [PMID: 23618408]
Ann Hum Genet. 2001 Nov;65(Pt 6):531-6 [PMID: 11851983]
Genetics. 2003 May;164(1):269-75 [PMID: 12750338]
Am J Respir Crit Care Med. 2002 Nov 15;166(10):1396-402 [PMID: 12406857]
Genome Res. 2009 Sep;19(9):1639-45 [PMID: 19541911]
Stem Cells. 2014 Feb;32(2):364-76 [PMID: 24123565]
Cancer Res. 2004 Sep 15;64(18):6556-62 [PMID: 15374968]
Cytogenet Genome Res. 2005;110(1-4):462-7 [PMID: 16093699]
Mol Cell. 2003 Nov;12 (5):1087-99 [PMID: 14636569]
J Comput Biol. 1998 Summer;5(2):197-210 [PMID: 9672828]
PLoS Genet. 2014 Jul 31;10 (7):e1004466 [PMID: 25078401]
Proc Natl Acad Sci U S A. 2007 May 15;104 Suppl 1:8655-60 [PMID: 17494744]
Protein Expr Purif. 2001 Jul;22(2):307-17 [PMID: 11437607]
Cell Signal. 2008 Sep;20(9):1671-8 [PMID: 18585004]
Nat Genet. 2014 Dec;46(12):1303-10 [PMID: 25362486]
Nat Genet. 2011 Sep 25;43(11):1082-90 [PMID: 21946350]
DNA Repair (Amst). 2011 Feb 7;10(2):119-25 [PMID: 21130713]
Nat Biotechnol. 2010 May;28(5):511-5 [PMID: 20436464]
Mol Biol Evol. 2007 Aug;24(8):1586-91 [PMID: 17483113]
Bioinformatics. 2006 May 15;22(10):1269-71 [PMID: 16543274]
BMC Genomics. 2013 Oct 17;14:711 [PMID: 24134808]
Nucleic Acids Res. 2011 May;39(10):e68 [PMID: 21398631]
Bioinformatics. 2009 Aug 15;25(16):2078-9 [PMID: 19505943]
Nucleic Acids Res. 2003 Oct 1;31(19):5654-66 [PMID: 14500829]
Nat Biotechnol. 2011 May 15;29(7):644-52 [PMID: 21572440]
J Biol Chem. 2004 Jun 25;279(26):27315-9 [PMID: 15102855]
Proc Natl Acad Sci U S A. 2005 Jul 26;102(30):10557-62 [PMID: 16000407]
Bioinformatics. 2014 Sep 1;30(17):i541-8 [PMID: 25161245]
Genome Res. 2009 Feb;19(2):327-35 [PMID: 19029536]
Bioinformatics. 2005 Sep 15;21(18):3674-6 [PMID: 16081474]
Bioinformatics. 2001 Sep;17(9):847-8 [PMID: 11590104]
Am J Physiol. 1998 May;274(5 Pt 2):H1792-9 [PMID: 9612392]
Nature. 1987 Nov 26-Dec 2;330(6146):401-4 [PMID: 3120013]
PLoS One. 2012;7(5):e37418 [PMID: 22616004]
Genome Biol. 2008 Jan 11;9(1):R7 [PMID: 18190707]
Bioinformatics. 2011 Aug 1;27(15):2156-8 [PMID: 21653522]
Nat Genet. 2012 Feb 05;44(3):328-33 [PMID: 22306652]
Nucleic Acids Res. 2011 Jul;39(Web Server issue):W29-37 [PMID: 21593126]
Nucleic Acids Res. 2004 Jul 1;32(Web Server issue):W309-12 [PMID: 15215400]
Bioinformatics. 2014 May 1;30(9):1312-3 [PMID: 24451623]
Nat Rev Genet. 2012 Oct;13(10 ):745-53 [PMID: 22965354]
EMBO J. 1998 Jan 2;17(1):159-69 [PMID: 9427750]
Proc Natl Acad Sci U S A. 2015 Nov 10;112(45):13958-63 [PMID: 26460028]
Nat Commun. 2013;4:1858 [PMID: 23673643]
Oncogene. 2013 Sep 12;32(37):4387-96 [PMID: 23085754]
J Biol Chem. 2004 Apr 16;279(16):16128-35 [PMID: 14764593]
Mol Biol Evol. 2015 Aug;32(8):2085-96 [PMID: 25862140]
Nucleic Acids Res. 1998 Feb 15;26(4):1107-15 [PMID: 9461475]
Proc Biol Sci. 2013 Feb 06;280(1756):20122758 [PMID: 23390104]
Nat Genet. 2015 Mar;47(3):217-25 [PMID: 25621459]
Biol Direct. 2014 Oct 14;9(1):20 [PMID: 25319552]
Mol Ecol. 2007 Aug;16(16):3334-49 [PMID: 17688537]
Mol Ecol. 2009 Sep;18(18):3831-46 [PMID: 19732331]
Mol Biol Evol. 1997 May;14(5):527-36 [PMID: 9159930]
Angiogenesis. 2013 Apr;16(2):387-404 [PMID: 23143660]
Proc Natl Acad Sci U S A. 2002 Jan 22;99(2):715-20 [PMID: 11805326]
Cell. 2007 Apr 6;129(1):111-22 [PMID: 17418790]
Pharmacogenet Genomics. 2008 Jun;18(6):525-33 [PMID: 18496132]
Bioinformatics. 2009 Jul 15;25(14):1754-60 [PMID: 19451168]
PLoS Genet. 2010 Sep 09;6(9):e1001116 [PMID: 20838600]
Genome Res. 2009 Sep;19(9):1655-64 [PMID: 19648217]
BMC Bioinformatics. 2005 Feb 15;6:31 [PMID: 15713233]
Am J Primatol. 2011 Jan;73(1):96-107 [PMID: 20981682]
Science. 2008 Jun 20;320(5883):1632-5 [PMID: 18566285]
PLoS Genet. 2007 Mar 30;3(3):e45 [PMID: 17397259]
Nature. 2005 Sep 15;437(7057):376-80 [PMID: 16056220]
Bioinformatics. 2004 Nov 1;20(16):2878-9 [PMID: 15145805]
Hum Mol Genet. 2001 Feb 1;10(3):189-94 [PMID: 11159936]
Wilderness Environ Med. 2008 Spring;19(1):22-9 [PMID: 18333655]
Genome Res. 2010 Feb;20(2):265-72 [PMID: 20019144]

MeSH Term

Adaptation, Physiological
Amino Acid Sequence
Animals
Colobinae
Genetic Markers
Genome
Genomics
Phylogeny
Sequence Homology, Amino Acid

Chemicals

Genetic Markers
Journal Article Research Support, Non-U.S. Gov't

Word Cloud

Similar Articles

Cited By