Asian-Australasian Journal of Animal Sciences

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
권호 표지
DOI QR코드

DOI QR Code

Y-Single Nucleotide Polymorphisms Diversity in Chinese Indigenous Horse

  • Han, Haoyuan (College of Animal Science and Technology, Northwest A&F University) ;
  • Zhang, Qin (College of Life Sciences, Northwest A&F University) ;
  • Gao, Kexin (College of Animal Science and Technology, Northwest A&F University) ;
  • Yue, Xiangpeng (College of Animal Science and Technology, Northwest A&F University) ;
  • Zhang, Tao (Shaanxi University of Technology) ;
  • Dang, Ruihua (College of Animal Science and Technology, Northwest A&F University) ;
  • Lan, Xianyong (College of Animal Science and Technology, Northwest A&F University) ;
  • Chen, Hong (College of Animal Science and Technology, Northwest A&F University) ;
  • Lei, Chuzhao (College of Animal Science and Technology, Northwest A&F University)
  • Received : 2014.10.08
  • Accepted : 2015.03.04
  • Published : 2015.08.01
Download PDF
⟨ Previous Next ⟩

Abstract

In contrast to high genetic diversity of mitochondrial DNA (mtDNA), equine Y chromosome shows extremely low variability, implying limited patrilines in the domesticated horse. In this study, we applied direct sequencing and restriction fragment length polymorphism (RFLP) methods to investigate the polymorphisms of 33 Y chromosome specific loci in 304 Chinese indigenous horses from 13 breeds. Consequently, two Y-single nucleotide polymorphisms (SNPs) (Y-45701/997 and Y-50869) and one Y-indel (Y-45288) were identified. Of those, the Y-50869 (T>A) revealed the highest variation frequency (24.67%), whereas it was only 3.29% and 1.97% in Y-45288 (T/-) and Y-45701/997 (G>T) locus, respectively. These three mutations accounted for 27.96% of the total samples and identified five Y-SNP haplotypes, demonstrating genetic diversity of Y chromosome in Chinese horses. In addition, all the five YSNP haplotypes were shared by different breeds. Among 13 horse breeds analyzed, Balikun horse displayed the highest nucleotide diversity (${\pi}=5.6{\times}10^{-4}$) and haplotype diversity (h = 0.527), while Ningqiang horse showed the lowest nucleotide diversity (${\pi}=0.00000$) and haplotype diversity (h = 0.000). The results also revealed that Chinese horses had a different polymorphic pattern of Y chromosome from European and American horses. In conclusion, Chinese horses revealed genetic diversity of Y chromosome, however more efforts should be made to better understand the domestication and paternal origin of Chinese indigenous horses.

Keywords

References

  1. Agulnik, A. I., C. E. Bishop, J. L. Lerner, S. I. Agulnik, and V. V. Solovyev. 1997. Analysis of mutation rates in the SMCY/SMCX genes shows that mammalian evolution is male driven. Mamm. Genome 8:134-138. https://doi.org/10.1007/s003359900372
  2. Brandariz-Fontes, C., J. A. Leonard, J. L. Vega-Pla, N. Backstrom, G. Lindgren, S. Lippold, and C. Rico. 2013. Y-chromosome analysis in retuertas horses. PloS One 8(5):e64985.
  3. Cai, D., Z. Tang, L. Han, C. F. Speller, D. Y. Yang, X. Ma, J. Cao, H. Zhu, and H. Zhou. 2009. Ancient DNA provides new insights into the origin of the Chinese domestic horse. J. Archaeol. Sci. 36:835-842. https://doi.org/10.1016/j.jas.2008.11.006
  4. Cieslak, M., M. Pruvost, N. Benecke, M. Hofreiter, A. Morales, M. Reissmann, and A. Ludwig. 2010. Origin and history of mitochondrial DNA lineages in domestic horses. PLoS One 5(12):e15311. https://doi.org/10.1371/journal.pone.0015311
  5. Deng, T. 2000. Phylogenetic relationship of the Chinese miniature pony to Equus przewalskii (Perissodacatyla, Equidae). Acta Veterinaria et Zootechnica Sinica 31:28-33 (in Chinese).
  6. Diamond, J. 2002. Evolution, consequences and future of plant and animal domestication. Nature 418:700-707. https://doi.org/10.1038/nature01019
  7. Excoffier, L., G. Laval, and S. Schneider. 2005. Arlequin (version 3.0): An integrated software package for population genetics data analysis. Evol. Bioinform. Online 1:47-50.
  8. Goto, H., O. A. Ryder, A. R. Fisher, B. Schultz, S. L. K. Pond, A. Nekrutenko, and K. D. Makova. 2011. A massively parallel sequencing approach uncovers ancient origins and high genetic variability of endangered Przewalski's horses. Genome Biol. Evol. 3:1096-1106. https://doi.org/10.1093/gbe/evr067
  9. Guo, S., P. Savolainen, J. Su, Q. Zhang, D. Qi, J. Zhou, Y. Zhong, X. Zhao, and J. Liu. 2006. Origin of mitochondrial DNA diversity of domestic yaks. BMC Evol. Biol. 6:73. https://doi.org/10.1186/1471-2148-6-73
  10. Gupta, A. K. 2004. Origin of agriculture and domestication of plants and animals linked to early Holocene climate amelioration. Curr. Sci. 87:54-59.
  11. Hellborg, L. and H. Ellegren. 2003. Y chromosome conserved anchored tagged sequences (YCATS) for the analysis of mammalian male-specific DNA. Mol. Ecol. 12:283-291.
  12. Ishida, N., T. Oyunsuren, S. Mashima, H. Mukoyama, and N. Saitou. 1995. Mitochondrial DNA sequences of various species of the genus Equus with special reference to the phylogenetic relationship between Przewalskii's wild horse and domestic horse. J. Mol. Evol. 41:180-188.
  13. Larson, G., K. Dobney, U. Albarella, M. Fang, E. Matisoo-Smith, J. Robins, S. Lowden, H. Finlayson, T. Brand, and E. Willerslev. 2005. Worldwide phylogeography of wild boar reveals multiple centers of pig domestication. Science 307(5715): 1618-1621. https://doi.org/10.1126/science.1106927
  14. Larson, G., R. Liu, X. Zhao, J. Yuan, D. Fuller, L. Barton, K. Dobney, Q. Fan, Z. Gu, X. H. Liu, Y. Luo, P. Lv, L. Andersson, and N. Li. 2010. Patterns of East Asian pig domestication, migration, and turnover revealed by modern and ancient DNA. Proc. Natl. Acad. Sci. USA. 107:7686-7691. https://doi.org/10.1073/pnas.0912264107
  15. Lau, A. N., L. Peng, H. Goto, L. Chemnick, O. A. Ryder, and K. D. Makova. 2009. Horse domestication and conservation genetics of Przewalski's horse inferred from sex chromosomal and autosomal sequences. Mol. Biol. Evol. 26:199-208. https://doi.org/10.1093/molbev/msn239
  16. Lei, C. Z., R. Su, M. A. Bower, C. J. Edwards, X. B. Wang, S. Weining, L. Liu, W. M. Xie, F. Li, R. Y. Liu, Y. S. Zhang, C. M. Zhang, and H. Chen. 2009. Multiple maternal origins of native modern and ancient horse populations in China. Anim. Genet. 40:933-944. https://doi.org/10.1111/j.1365-2052.2009.01950.x
  17. Lei, C. Z., W. Zhang, H. Chen, F. Lu, R. Y. Liu, X. Y. Yang, H. C. Zhang, Z. G. Liu, L. B. Yao, Z. F. Lu, and Z. L. Zhao. 2007. Independent maternal origin of Chinese swamp buffalo (Bubalus bubalis). Anim. Genet. 38:97-102. https://doi.org/10.1111/j.1365-2052.2007.01567.x
  18. Librado, P. and J. Rozas. 2009. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451-1452. https://doi.org/10.1093/bioinformatics/btp187
  19. Lindgren, G., N. Backstrom, J. Swinburne, L. Hellborg, A. Einarsson, K. Sandberg, G. Cothran, C. Vila, M. Binns, and H. Ellegren. 2004. Limited number of patrilines in horse domestication. Nat. Genet. 36:335-336. https://doi.org/10.1038/ng1326
  20. Ling, Y., Y. Ma, W. Guan, Y. Cheng, Y. Wang, J. Han, D. Jin, L. Mang, and H. Mahmut. 2010. Identification of Y chromosome genetic variations in Chinese indigenous horse breeds. J. Hered. 101:639-643. https://doi.org/10.1093/jhered/esq047
  21. Ling, Y. H., Y. H. Ma, W. J. Guan, Y. J. Cheng, Y. P. Wang, J. L. Han, L. Mang, Q. J. Zhao, X. H. He, Y. B. Pu, and B. L. Fu. 2011. Evaluation of the genetic diversity and population structure of Chinese indigenous horse breeds using 27 microsatellite markers. Anim. Genet. 42:56-65. https://doi.org/10.1111/j.1365-2052.2010.02067.x
  22. Liu, Y. P., G. S. Wu, Y. G. Yao, Y. W. Miao, G. Luikart, M. Baig, A. Beja-Pereira, Z. L. Ding, M. G. Palanichamy, and Y. P. Zhang. 2006. Multiple maternal origins of chickens: out of the Asian jungles. Mol. Phylogenet. Evol. 38:12-19. https://doi.org/10.1016/j.ympev.2005.09.014
  23. Ludwig, A., M. Pruvost, M. Reissmann, N. Benecke, G. A. Brockmann, P. Castanos, M. Cieslak, S. Lippold, L. Llorente, A. S. Malaspinas, M. Slatkin, and M. Hofreiter. 2009. Coat color variation at the beginning of horse domestication. Science 324(5926):485-485. https://doi.org/10.1126/science.1172750
  24. McGahern, A., M. A. M. Bower, C. J. Edwards, P. O. Brophy, G. Sulimova, I. Zakharov, M. Vizuete-Forster, M. Levine, S. Li, D. E. MacHugh, and E. W. Hill. 2006. Evidence for biogeographic patterning of mitochondrial DNA sequences in Eastern horse populations. Anim. Genet. 37:494-497. https://doi.org/10.1111/j.1365-2052.2006.01495.x
  25. Nei, M. 1972. Genetic distance between populations. Am. Nat. 106:283-292. https://doi.org/10.1086/282771
  26. Oakenfull, E. A. and O. A. Ryder. 1998. Mitochondrial control region and 12S rRNA variation in Przewalski's horse (Equus przewalskii). Anim. Genet. 29:456-459. https://doi.org/10.1046/j.1365-2052.1998.296380.x
  27. Oakenfull, E. A., H. N. Lim, and O. A. Ryder. 2000. A survey of equid mitochondrial DNA: Implications for the evolution, genetic diversity and conservation of Equus. Conserv. Genet. 1:341-355. https://doi.org/10.1023/A:1011559200897
  28. Outram, A. K., N. A. Stear, R. Bendrey, S. Olsen, A. Kasparov, V. Zaibert, N. Thorpe, and R. P. Evershed. 2009. The earliest horse harnessing and milking. Science 323(5919):1332-1335. https://doi.org/10.1126/science.1168594
  29. Raudsepp, T., A. Santani, B. Wallner, S. R. Kata, C. Ren, H. B. Zhang, J. E. Womack, L. C. Skow, and B. P. Chowdhary. 2004. A detailed physical map of the horse Y chromosome. Proc. Natl. Acad. Sci. USA. 101:9321-9326. https://doi.org/10.1073/pnas.0403011101
  30. Paria, N., T. Raudsepp, A. J. P. Wilkerson, P. C. M. O'Brien, M. A. Ferguson-Smith, C. C. Love, C. Arnold, P. Rakestraw, W. J. Murphy, and B. P. Chowdhary. 2011. A gene catalogue of the euchromatic male-specific region of the horse Y chromosome: comparison with human and other mammals. PloS One 6(7):e21374. https://doi.org/10.1371/journal.pone.0021374
  31. Sambrook, J. and D. W. Russell. 2002. Molecular cloning: A laboratory manual. Translated by P. T. Huang. Beijing: Science Press, Beijing, China.
  32. Savolainen, P., Y. P. Zhang, J. Luo, J. Lundeberg, and T. Leitner. 2002. Genetic evidence for an East Asian origin of domestic dogs. Science 298(5598):1610-1613. https://doi.org/10.1126/science.1073906
  33. Skaletsky, H., T. Kuroda-Kawaguchi, P. J. Minx, H. S. Cordum, L. Hillier, L. G. Brown, S. Repping, T. Pyntikova, J. Ali, and T. Bieri et al. 2003. The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature 423:825-837. https://doi.org/10.1038/nature01722
  34. Tamura, K., D. Peterson, N. Peterson, G. Stecher, M. Nei, S. Kumar. 2011. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28:2731-2739. https://doi.org/10.1093/molbev/msr121
  35. Vila, C., J. A. Leonard, A. Gotherstrom, S. Marklund, K. Sandberg, K. Liden, R. K. Wayne, and H. Ellegren. 2001. Widespread origins of domestic horse lineages. Science 291(5503):474-477. https://doi.org/10.1126/science.291.5503.474
  36. Wallner, B., G. Brem, M. Muller, and R. Achmann. 2003. Fixed nucleotide differences on the Y chromosome indicate clear divergence between Equus przewalskii and Equus caballus. Anim. Genet. 34:453-456. https://doi.org/10.1046/j.0268-9146.2003.01044.x
  37. Wallner, B., F. Piumi, G. Brem, M. Muller, and R. Achmann. 2004. Isolation of Y chromosome-specific microsatellites in the horse and cross-species amplification in the genus Equus. J. Hered. 95:158-164. https://doi.org/10.1093/jhered/esh020
  38. Wallner, B., C. Vogl, P. Shukla, J. P. Burgstaller, T. Druml, and G. Brem. 2013. Identification of genetic variation on the horse Y chromosome and the tracing of male founder lineages in modern breeds. PloS One. 8(4):e60015. https://doi.org/10.1371/journal.pone.0060015
  39. Xie, C. 1987. Chinese Horse Donkey Breeds. Shanghai Science and Technology Press, Shanghai, China (in Chineses).
  40. Zhang, C. S. 2004. Wild horses, domestic horses, and center for Eastern Asia horse raising. Agric. Archaeol. 1:252-254 (in Chinese).

Cited by

  1. Genetic Diversity of Mitochondrial DNA of Chinese Black-bone Chicken vol.20, pp.3, 2018, https://doi.org/10.1590/1806-9061-2018-0739
  2. Distribution of Y chromosomal haplotypes in Japanese native horse populations vol.29, pp.2, 2018, https://doi.org/10.1294/jes.29.39
  3. Y-chromosome polymorphisms of the domestic Bactrian camel in China vol.97, pp.1, 2018, https://doi.org/10.1007/s12041-017-0852-1
  4. Eight Y chromosome genes show copy number variations in horses vol.61, pp.3, 2015, https://doi.org/10.5194/aab-61-263-2018
  5. Origin and Diffusion of Equus caballus from the Archaeological and Genetic Perspectives vol.33, pp.2, 2020, https://doi.org/10.11637/aba.2020.33.2.57
  6. Ancient Patrilineal Lines and Relatively High ECAY Diversity Preserved in Indigenous Horses Revealed With Novel Y-Chromosome Markers vol.11, pp.None, 2015, https://doi.org/10.3389/fgene.2020.00467