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Journal of Applied Genetics

, Volume 57, Issue 4, pp 519–525 | Cite as

Distribution of coat-color-associated alleles in the domestic horse population and Przewalski’s horse

  • Monika Reissmann
  • Lutfi Musa
  • Sonia Zakizadeh
  • Arne Ludwig
Animal Genetics • Original Paper

Abstract

Considering the hidden mode of inheritance of some coat-color-associated alleles, we investigated the presence/absence of coat-color-associated alleles in 1093 domestic horses of 55 breeds and 20 specimens of Przewalski’s horse. For coat-color genotyping, allele specific PCR, pyrosequencing and Li-Cor analyses were conducted on 12 coat-color-associated alleles of five genes. Our data provide deep insight into the distribution of coat-color-associated alleles within breeds. We found that the alleles for the basic colorations (bay, black, and chestnut) are widely distributed and occur in nearly all breeds. Alleles leading to dilutions or patterns are rare in domestic breeds and were not found in Przewalski’s horse. Higher frequencies of these alleles are only found in breeds that are selected for their expressed phenotypes (e.g., Kinsky horse, Lewitzer, Tinker). Nevertheless, our study produced strong evidence that molecular testing of the coat color is necessary for well-defined phenotyping to avoid unexpected colorations of offspring that can result in legal action.

Keywords

ASIP Kit MC1R Pmel17 SLC45A2 

Notes

Acknowledgments

The authors thank Christiane Slawik (Würzburg, Germany), Tobias Knoll (Zenting, Germany), Sergey Knyasev (Novosibirsk, Russia), and Marina Politova (Moscow, Russia) for allocation of hair material and the many horse breeders who supported this study. This study was supported by the Deutsche Forschungsgemeinschaft (LU 852/7-4).

Compliance with ethical standards

Competing interests

The authors declare they have no competing interests.

References

  1. Achilli A, Olivieri A, Soares P, Lancioni H, Hooshiar KB, Perego UA, Nergadze SG, Carossa V, Santagostino M, Capomaccio S, Felicetti M, Al-Achkar W, Penedo MC, Verini-Supplizi A, Houshmand M, Woodward SR, Semino O, Silvestrelli M, Giulotto E, Pereira L, Bandelt HJ, Torroni A (2012) Mitochondrial genomes from modern horses reveal the major haplogroups that underwent domestication. Proc Natl Acad Sci U S A 109:2449–2454CrossRefPubMedPubMedCentralGoogle Scholar
  2. Andersson LS, Juras R, Ramsey DT, Eason-Butler J, Ewart S, Cothran G, Lindgren G (2008) Equine multiple congenital ocular anomalies maps to a 4.9 megabase interval on horse chromosome 6. BMC Genet 9:88CrossRefPubMedPubMedCentralGoogle Scholar
  3. Andersson LS, Axelsson J, Dubielzig RR, Lindgren G, Ekesten B (2011a) Multiple congenital ocular anomalies in Icelandic horses. BMC Vet Res 7:21CrossRefPubMedPubMedCentralGoogle Scholar
  4. Andersson LS, Lyberg K, Cothran G, Ramsey DT, Juras R, Mikko S, Ekesten B, Ewart S, Lindgren G (2011b) Targeted analysis of four breeds narrows equine multiple congenital ocular anomalies locus to 208 kilobases. Mamm Genome 22:353–360CrossRefPubMedPubMedCentralGoogle Scholar
  5. Andersson LS, Wilbe M, Viluma A, Cothran G, Ekesten B, Ewart S, Lindgren G (2013) Equine multiple congenital ocular anomalies and silver coat colour result from the pleiotropic effects of mutant PMEL. PLoS One 8, e75639CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bai DY, Yang LH, Unerhu U, Zhao YP, Zhao QN, Hasigaowa H, Dugarjaviin M (2011) Effects of Kit gene on coat depigmentation in white horses. Yi Chuan 33:1171–1178CrossRefPubMedGoogle Scholar
  7. Bellone RR (2010) Pleiotropic effects of pigmentation genes in horses. Anim Genet 41(Suppl 2):100–110CrossRefPubMedGoogle Scholar
  8. Bellone RR, Holl H, Setaluri V, Devi S, Maddodi N, Archer S, Sandmeyer L, Ludwig A, Foerster D, Pruvost M, Reissmann M, Bortfeldt R, Adelson DL, Lim SL, Nelson J, Haase B, Engensteiner M, Leeb T, Forsyth G, Mienaltowski MJ, Mahadevan P, Hofreiter M, Paijmans JLA, Gonzalez-Fortes G, Grahn B, Brooks SA (2013) Evidence for a retroviral insertion in TRPM1 as the cause of congenital stationary night blindness and leopard complex spotting in the horse. Plos One 8(10):e78280Google Scholar
  9. Brooks SA, Bailey E (2005) Exon skipping in the KIT gene causes a Sabino spotting pattern in horses. Mamm Genome 16:893–902CrossRefPubMedGoogle Scholar
  10. Campana MG, Whitten CM, Edwards CJ, Stock F, Murphy AM, Binns MM, Barker GW, Bower MA (2010) Accurate determination of phenotypic information from historic thoroughbred horses by single base extension. PLoS One 5, e15172CrossRefPubMedPubMedCentralGoogle Scholar
  11. Cieslak M, Pruvost M, Benecke N, Hofreiter M, Morales A, Reissmann M, Ludwig A (2010) Origin and history of mitochondrial DNA lineages in domestic horses. PLoS One 5:e15311CrossRefPubMedPubMedCentralGoogle Scholar
  12. Cieslak M, Reissmann M, Hofreiter M, Ludwig A (2011) Colours of domestication. Biol Rev Camb Philos Soc 86:885–899CrossRefPubMedGoogle Scholar
  13. Der Sarkissian C, Ermini L, Schubert M, Yang MA, Librado P, Fumagalli M, Jonsson H, Bar-Gal GK, Albrechtsen A, Vieira FG, Petersen B, Ginolhac A, Seguin-Orlando A, Magnussen K, Fages A, Gamba C, Lorente-Galdos B, Polani S, Steiner C, Neuditschko M, Jagannathan V, Feh C, Greenblatt CL, Ludwig A, Abramson NI, Zimmermann W, Schafberg R, Tikhonov A, Sicheritz-Ponten T, Willerslev E, Marques-Bonet T, Ryder OA, McCue M, Rieder S, Leeb T, Slatkin M, Orlando L (2015) Evolutionary genomics and conservation of the endangered Przewalski’s horse. Curr Biol 25:2577–2583CrossRefGoogle Scholar
  14. Dobberthien M. (2010) The “creme gene” in the Trakehner population (I). Der Trakehner 1:38–43Google Scholar
  15. Dobberthien M. (2010) The “creme gene” in the Trakehner population (II). Der Trakehner 1:20–4Google Scholar
  16. Geurts R (1977) Hair colour in the horse. Sporting Book Centre, Inc., CanaanGoogle Scholar
  17. Haase B, Brooks SA, Schlumbaum A, Azor PJ, Bailey E, Alaeddine F, Mevissen M, Burger D, Poncet PA, Rieder S, Leeb T (2007) Allelic heterogeneity at the equine KIT locus in dominant white (W) horses. PLoS Genet 3:e195CrossRefPubMedPubMedCentralGoogle Scholar
  18. Haase B, Brooks SA, Tozaki T, Burger D, Poncet PA, Rieder S, Hasegawa T, Penedo C, Leeb T (2009) Seven novel KIT mutations in horses with white coat colour phenotypes. Anim Genet 40:623–629CrossRefPubMedGoogle Scholar
  19. Haase B, Rieder S, Tozaki T, Hasegawa T, Penedo MC, Jude R, Leeb T (2011) Five novel KIT mutations in horses with white coat colour phenotypes. Anim Genet 42:337–339CrossRefPubMedGoogle Scholar
  20. Haase B, Jagannathan V, Rieder S, Leeb T (2015) A novel KIT variant in an Icelandic horse with white-spotted coat colour. Anim Genet 46(4):466CrossRefPubMedGoogle Scholar
  21. Hauswirth R, Haase B, Blatter M, Brooks SA, Burger D, Drogemuller C, Gerber V, Henke D, Janda J, Jude R, Magdesian KG, Matthews JM, Poncet PA, Svansson V, Tozaki T, Wilkinson-White L, Penedo MC, Rieder S, Leeb T (2012) Mutations in MITF and PAX3 cause “splashed white” and other white spotting phenotypes in horses. PLoS Genet 8, e1002653CrossRefPubMedPubMedCentralGoogle Scholar
  22. Hauswirth R, Jude R, Haase B, Bellone RR, Archer S, Holl H, Brooks SA, Tozaki T, Penedo MC, Rieder S, Leeb T (2013) Novel variants in the KIT and PAX3 genes in horses with white-spotted coat colour phenotypes. Anim Genet 44:763–765CrossRefPubMedGoogle Scholar
  23. Jansen T, Forster P, Levine MA, Oelke H, Hurles M, Renfrew C, Weber J, Olek K (2002) Mitochondrial DNA and the origins of the domestic horse. Proc Natl Acad Sci U S A 99:10905–10910CrossRefPubMedPubMedCentralGoogle Scholar
  24. Kakoi H, Tozaki T, Nagata S, Gawahara H, Kijima-Suda I (2009) Development of a method for simultaneously genotyping multiple horse coat colour loci and genetic investigation of basic colour variation in Thoroughbred and Misaki horses in Japan. J Anim Breed Genet 126:425–431CrossRefPubMedGoogle Scholar
  25. Kavar T, Ceh E, Dovc P (2012) A simplified PCR-based method for detection of gray coat color allele in horse. Mol Cell Probes 26:256–258CrossRefPubMedGoogle Scholar
  26. Komaromy AM, Rowlan JS, La Croix NC, Mangan BG (2011) Equine multiple congenital ocular anomalies (MCOA) syndrome in PMEL17 (silver) mutant ponies: five cases. Vet Ophthalmol 14:313–320CrossRefPubMedPubMedCentralGoogle Scholar
  27. Lindgren G, Backstrom N, Swinburne J, Hellborg L, Einarsson A, Sandberg K, Cothran G, Vila C, Binns M, Ellegren H (2004) Limited number of patrilines in horse domestication. Nat Genet 36:335–336CrossRefPubMedGoogle Scholar
  28. Ling Y, Ma Y, Guan W, Cheng Y, Wang Y, Han J, Jin D, Mang L, Mahmut H (2010) Identification of Y chromosome genetic variations in Chinese indigenous horse breeds. J Hered 101:639–643CrossRefPubMedGoogle Scholar
  29. Lippold S, Knapp M, Kuznetsova T, Leonard JA, Benecke N, Ludwig A, Rasmussen M, Cooper A, Weinstock J, Willerslev E, Shapiro B, Hofreiter M (2011) Discovery of lost diversity of paternal horse lineages using ancient DNA. Nat Commun 2:450CrossRefPubMedGoogle Scholar
  30. Ludwig A, Pruvost M, Reissmann M, Benecke N, Brockmann GA, Castanos P, Cieslak M, Lippold S, Llorente L, Malaspinas AS, Slatkin M, Hofreiter M (2009) Coat color variation at the beginning of horse domestication. Science 324:485CrossRefPubMedGoogle Scholar
  31. Marklund L, Johansson MM, Hoyheim B, Davies W, Fredholm M, Juneja RK, Mariani P, Coppieters W, Ellegren H, Andersson L (1996) A comprehensive linkage map of the pig based on a wild pig-Large White intercross. Anim Genet 27:255–269CrossRefPubMedGoogle Scholar
  32. Mohr E, Volf J (1984) Das Urwildpferd. A. Ziemsen, WittenbergGoogle Scholar
  33. Nissen J (1997) Encyclopedia of horse breeds. Franckh-Kosmos, StuttgartGoogle Scholar
  34. Pruvost M, Bellone R, Benecke N, Sandoval-Castellanos E, Cieslak M, Kuznetsova T, Morales-Muñiz A, O'Connor T, Reissmann M, Hofreiter M, Ludwig A (2011) Genotypes of predomestic horses match phenotypes painted in Paleolithic works of cave art. Proceedings of the National Academy of Sciences USA 108: 18626–18630Google Scholar
  35. Pruvost M, Reissmann M, Benecke N, Ludwig A (2012) From genes to phenotypes - evaluation of two methods for the SNP analysis in archaeological remains: pyrosequencing and competitive allele specific PCR (KASPar). Ann Anat 194:74–81CrossRefPubMedGoogle Scholar
  36. Reissmann M, Ludwig A (2013) Pleiotropic effects of coat colour-associated mutations in humans, mice and other mammals. Semin Cell Dev Biol 24:576–586CrossRefPubMedGoogle Scholar
  37. Reissmann M., Wagner H.J., Gulyáz L. & Schuster S. (2002) The allele ea - a rare mutation in the MC1R gene in horse (EQUUS CABALLUS). In: XXVIII International Conference on animal Genetics, p. 129. International Society for Animal Genetics, GöttingenGoogle Scholar
  38. Rieder S (2009) Molecular tests for coat colours in horses. J Anim Breed Genet 126:415–424CrossRefPubMedGoogle Scholar
  39. Rieder S, Taourit S, Mariat D, Langlois B, Guerin G (2001) Mutations in the agouti (ASIP), the extension (MC1R), and the brown (TYRP1) loci and their association to coat color phenotypes in horses (Equus caballus). Mamm Genome 12:450–455CrossRefPubMedGoogle Scholar
  40. Schlie A (1967) The Hanoverian Horse. BLV Bayerischer Landwirtschaftsverlag GmbH. München Basel, WienGoogle Scholar
  41. Vogel H (1948) Horse breeding. Parey, BerlinGoogle Scholar
  42. Wagner HJ, Reissmann M (2000) New polymorphism detected in the horse MC1R gene. Anim Genet 31:289–290CrossRefPubMedGoogle Scholar
  43. Wallner B, Vogl C, Shukla P, Burgstaller JP, Druml T, Brem G (2013) Identification of genetic variation on the horse y chromosome and the tracing of male founder lineages in modern breeds. PLoS One 8:e60015CrossRefPubMedPubMedCentralGoogle Scholar
  44. Warmuth V, Eriksson A, Bower MA, Barker G, Barrett E, Hanks BK, Li S, Lomitashvili D, Ochir-Goryaeva M, Sizonov GV, Soyonov V, Manica A (2012) Reconstructing the origin and spread of horse domestication in the Eurasian steppe. Proc Natl Acad Sci U S A 109:8202–8206CrossRefPubMedPubMedCentralGoogle Scholar
  45. Wrangel GCG (1908) The breeds of the horse. Schickhardt & Ebner (Konrad Wittwer), StuttgartGoogle Scholar
  46. Wrangel GCG (1928) The book from the horse. Schickhardt & Ebner (Konrad Wittwer), StuttgartGoogle Scholar

Copyright information

© Institute of Plant Genetics, Polish Academy of Sciences, Poznan 2016

Authors and Affiliations

  • Monika Reissmann
    • 1
  • Lutfi Musa
    • 2
  • Sonia Zakizadeh
    • 3
  • Arne Ludwig
    • 4
  1. 1.Albrecht Daniel Thaer InstituteHumboldt University BerlinBerlinGermany
  2. 2.Department of Genetics and Animal Breeding, Faculty of Animal ProductionUniversity of KhartoumKhartoumSudan
  3. 3.Department of Animal ScienceJihad-Agricultural Higher Educational ComplexMashadIran
  4. 4.Department of Evolutionary GeneticsLeibniz Institute for Zoo and Wildlife ResearchBerlinGermany

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