vavilovВавиловский журнал генетики и селекцииVavilov Journal of Genetics and Breeding2500-3259Institute of Cytology and Genetics of Siberian Branch of the RAS10.18699/VJ18.350vavilov-1444Research ArticleМЕДИЦИНСКАЯ ГЕНЕТИКА, НЕЙРОГЕНЕТИКА, ИММУНОГЕНЕТИКА, БИОМЕДИЦИНАPOPULATION GENETICSВыявление генов, вовлеченных в контроль белой окраски головы, у восьми российских пород крупного рогатого скотаGenes related to the white face colour pattern in eight Russian cattle breedsЮдинН. С.YudinN. S.

Новосибирск

Novosibirsk

БелоноговаН. М.BelonogovaN. M.

Новосибирск

Novosibirsk

ЛаркинД. М.LarkinD. M.

Новосибирск;

Лондон

Novosibirsk;

 London

dmlarkin@gmail.comФедеральный исследовательский центр Институт цитологии и генетики Сибирского отделения Российской академии наук; Новосибирский национальный исследовательский государственный университетРоссияInstitute of Cytology and Genetics SB RAS; Novosibirsk State UniversityRussian FederationФедеральный исследовательский центр Институт цитологии и генетики Сибирского отделения Российской академии наукРоссияInstitute of Cytology and Genetics SB RASRussian FederationФедеральный исследовательский центр Институт цитологии и генетики Сибирского отделения Российской академии наук; Королевский ветеринарный колледж, Лондонский университетРоссияInstitute of Cytology and Genetics SB RAS; Royal Veterinary College, University of LondonRussian Federation201806042018222217223Copyright © Юдин Н.С., Белоногова Н.М., Ларкин Д.М., 20182018Юдин Н.С., Белоногова Н.М., Ларкин Д.М.Yudin N.S., Belonogova N.M., Larkin D.M.This work is licensed under a Creative Commons Attribution 4.0 License.https://vavilov.elpub.ru/jour/article/view/1444

Характерным признаком доместикации является нарушение пигментации, приводящее к появлению пегости, вплоть до равномерной белой окраски тела животного. Целью работы была идентификация районов генома и генов-кандидатов, связанных с частным вариантом пегости, белой окраской головы, у представителей восьми российских пород крупного рогатого скота. После фильтрации для полногеномного анализа ассоциаций был использован набор из 131709 однонуклеотидных полиморфизмов (ОНП). Ассоциативный анализ был проведен с помощью пакета EMMAX при использовании двух фенотипов: фенотип 1 – белая голова (при наличии преимущественно белого окраса) и туловище любого цвета (в том числе белого), фенотип 2 – белая голова и туловище обязательно небелого цвета. Для фенотипа 1 значимо ассоциированным оказался единственный ОНП BovineHD0500019319 на хромосоме 5. Этот же ОНП входил в состав кластера из трех значимых ОНП в районе 68803879–69365854 п.н., ассоциированного и с фенотипом 2. Внутри этого района находятся пять генов. Из них наиболее вероятным функциональным кандидатом является ген SLC41A2, в интроне которого локализован ОНП BovineHD0500019319. Ген SLC41A2 кодирует белок потенциалзависимого магниевого транспортера, который также может переносить ряд других катионов. Функция белка SLC41A2 недостаточно изучена, однако известно, что другие белки этого семейства определяют окраску как кожи человека, так и шерсти животных. Положительные сигналы ассоциации для второго фенотипа обнаружены также на хромосомах 1–4, 6–15, 18, 19, 24, 27 и 29. Выявлено 37 районов генома крупного рогатого скота, достоверно ассоциированных с белой окраской головы.

One of the major effects of domestication is change of animal coat colour to up to complete white colour of the whole body. It is possible that white colour of livestock animals had aesthetic significance for humans as well. The first step towards detection of genes and mutations controlling white colouring in animals is the genome-wide association studies. These studies, however, have not been done for the cattle breeds native to the Russian Federation. The aim of this study was therefore to identify genomic intervals and candidate genes that could be responsible for white face colouring in eight Russian cattle breeds. The data on genome-wide genotyping of 131,709 high-quality single nucleotide polymorphisms (SNPs) on 148 animas have been used in the program ­EMMAX. Association analysis has been performed using two related phenotypes: a) the white face with the rest of the body of any colour and b) white face with the rest of the body of different (non-white) colour. In the first case, the only statistically significant marker found was the SNP BovineHD0500019319 located on cattle chromosome (BTA) 5. The same SNP was the most significant within the cluster of three SNPs on BTA5: 68,803,879–69,365,854 associated also with the second phenotype. Five genes were found within this interval in the cattle genome, out of which the most likely functional candidate was SLC41A2, with the SNP BovineHD0500019319 found within its intronic sequence. SLC41A2 encodes a magnesium transporter protein. However, the function of this gene is not well established. Other members of this gene family are the key genes controlling differences in human skin and animal coat colour. Additional significant association signals with the second phenotype have been detected in BTA 1–4, 6–15, 18, 19, 24, 27, and 29. Overall, 37 genomic intervals have been detected associated with white face colouring in eight Russian native cattle breeds.

крупный рогатый скотаборигенный скотпородаокраскабелая головаполногеномный анализ ассоциацийген SLC41A2доместикацияcattlenative populationsbreedcolouringwhite facegenome-wide association studiesSLC41A2domesticationReferencesAhi E.P., Sefc K.M. A gene expression study of dorso-ventrally restricted pigment pattern in adult fins of Neolamprologus meeli, an African cichlid species. PeerJ. 2017;5:e2843. DOI 10.7717/ peerj.2843.Ahi E.P., Sefc K.M. A gene expression study of dorso-ventrally restricted pigment pattern in adult fins of Neolamprologus meeli, an African cichlid species. PeerJ. 2017;5:e2843. DOI 10.7717/ peerj.2843.Andersson L. Genetic dissection of phenotypic diversity in farm animals. Nat. Rev. Genet. 2001;2(2):130-138. DOI 10.1038/35052563.Andersson L. Genetic dissection of phenotypic diversity in farm animals. Nat. Rev. Genet. 2001;2(2):130-138. DOI 10.1038/35052563.Andersson L. Genome-wide association analysis in domestic animals: a powerful approach for genetic dissection of trait loci. Genetica. 2009;136:341-349. DOI 10.1007/s10709-008-9312-4.Andersson L. Genome-wide association analysis in domestic animals: a powerful approach for genetic dissection of trait loci. Genetica. 2009;136:341-349. DOI 10.1007/s10709-008-9312-4.Basu Mallick C., Iliescu F.M., Möls M., Hill S., Tamang R., Chaubey G., Goto R., Ho S.Y., Gallego Romero I., Crivellaro F., Hudjashov G., Rai N., Metspalu M., Mascie-Taylor C.G., Pitchappan R., Singh L., Mirazon-Lahr M., Thangaraj K., Villems R., Kivisild T. The light skin allele of SLC24A5 in South Asians and Europeans shares identity by descent. PLoS Genet. 2013;9(11):e1003912. DOI 10.1371/journal.pgen.1003912.Basu Mallick C., Iliescu F.M., Möls M., Hill S., Tamang R., Chaubey G., Goto R., Ho S.Y., Gallego Romero I., Crivellaro F., Hudjashov G., Rai N., Metspalu M., Mascie-Taylor C.G., Pitchappan R., Singh L., Mirazon-Lahr M., Thangaraj K., Villems R., Kivisild T. The light skin allele of SLC24A5 in South Asians and Europeans shares identity by descent. PLoS Genet. 2013;9(11):e1003912. DOI 10.1371/journal.pgen.1003912.Belyaev D.K. Destabilizing selection as a factor in domestication. J. Hered. 1979;70:301-308. BioGPS. SLC41A2 (solute carrier family 41 member 2). 2017. Available at http://biogps.org/#goto=genereport&id=84102.Belyaev D.K. Destabilizing selection as a factor in domestication. J. Hered. 1979;70:301-308. BioGPS. SLC41A2 (solute carrier family 41 member 2). 2017. Available at http://biogps.org/#goto=genereport&id=84102.Branicki W., Brudnik U., Draus-Barini J., Kupiec T., Wojas-Pelc A. Association of the SLC45A2 gene with physiological human hair colour variation. J. Hum. Genet. 2008;53(11-12):966-971. DOI 10.1007/s10038-008-0338-3.Branicki W., Brudnik U., Draus-Barini J., Kupiec T., Wojas-Pelc A. Association of the SLC45A2 gene with physiological human hair colour variation. J. Hum. Genet. 2008;53(11-12):966-971. DOI 10.1007/s10038-008-0338-3.Caduff M., Bauer A., Jagannathan V., Leeb T. A single base deletion in the SLC45A2 gene in a Bullmastiff with oculocutaneous albinism. Anim. Genet. 2017;48(5):619-621. DOI 10.1111/age.12582.Caduff M., Bauer A., Jagannathan V., Leeb T. A single base deletion in the SLC45A2 gene in a Bullmastiff with oculocutaneous albinism. Anim. Genet. 2017;48(5):619-621. DOI 10.1111/age.12582.Cieslak M., Reissmann M., Hofreiter M., Ludwig A. Colours of domestication. Biol. Rev. Camb. Philos. Soc. 2011;86(4):885-899. DOI 10.1111/j.1469-185X.2011.00177.x. D’Mello S.A., Finlay G.J., Baguley B.C., Askarian-Amiri M.E. Signaling pathways in melanogenesis. Int. J. Mol. Sci. 2016;17(7). pii: E1144. DOI 10.3390/ijms17071144.Cieslak M., Reissmann M., Hofreiter M., Ludwig A. Colours of domestication. Biol. Rev. Camb. Philos. Soc. 2011;86(4):885-899. DOI 10.1111/j.1469-185X.2011.00177.x. D’Mello S.A., Finlay G.J., Baguley B.C., Askarian-Amiri M.E. Signaling pathways in melanogenesis. Int. J. Mol. Sci. 2016;17(7). pii: E1144. DOI 10.3390/ijms17071144.Drögemüller C., Demmel S., Engensteiner M., Rieder S., Leeb T. A shared 336 kb haplotype associated with the belt pattern in three divergent cattle breeds. Anim. Genet. 2010;41:304-307. DOI 10.1111/ j.1365-2052.2009.01987.x.Drögemüller C., Demmel S., Engensteiner M., Rieder S., Leeb T. A shared 336 kb haplotype associated with the belt pattern in three divergent cattle breeds. Anim. Genet. 2010;41:304-307. DOI 10.1111/ j.1365-2052.2009.01987.x.Drögemüller C., Engensteiner M., Moser S., Rieder S., Leeb T. Genetic mapping of the belt pattern in Brown Swiss cattle to BTA3. Anim. Genet. 2009;40:225-229. DOI 10.1111/j.1365-2052.2008.01826.x.Drögemüller C., Engensteiner M., Moser S., Rieder S., Leeb T. Genetic mapping of the belt pattern in Brown Swiss cattle to BTA3. Anim. Genet. 2009;40:225-229. DOI 10.1111/j.1365-2052.2008.01826.x.Fan Y., Wang P., Fu W., Dong T., Qi C., Liu L., Guo G., Li C., Cui X., Zhang S., Zhang Q., Zhang Y., Sun D. Genome-wide association study for pigmentation traits in Chinese Holstein population. Anim. Genet. 2014;45(5):740-744. DOI 10.1111/age.12189.Fan Y., Wang P., Fu W., Dong T., Qi C., Liu L., Guo G., Li C., Cui X., Zhang S., Zhang Q., Zhang Y., Sun D. Genome-wide association study for pigmentation traits in Chinese Holstein population. Anim. Genet. 2014;45(5):740-744. DOI 10.1111/age.12189.Fontanesi L., Scotti E., Russo V. Analysis of SNPs in the KIT gene of cattle with different coat colour patterns and perspectives to use these markers for breed traceability and authentication of beef and dairy products. Ital. J. Anim. Sci. 2010;9:e42. DOI 10.4081/ijas.2010.e42.Fontanesi L., Scotti E., Russo V. Analysis of SNPs in the KIT gene of cattle with different coat colour patterns and perspectives to use these markers for breed traceability and authentication of beef and dairy products. Ital. J. Anim. Sci. 2010;9:e42. DOI 10.4081/ijas.2010.e42.Fontanesi L., Scotti E., Russo V. Haplotype variability in the bovine MITF gene and association with piebaldism in Holstein and Simmental cattle breeds. Anim. Genet. 2012;43:250-256. DOI 10.1111/ j.1365-2052.2011.02242.x.Fontanesi L., Scotti E., Russo V. Haplotype variability in the bovine MITF gene and association with piebaldism in Holstein and Simmental cattle breeds. Anim. Genet. 2012;43:250-256. DOI 10.1111/ j.1365-2052.2011.02242.x.Galván I., Moraleda V., Otero I., Álvarez E., Inácio Â. Genetic favouring of pheomelanin-based pigmentation limits physiological benefits of coloniality in lesser kestrels Falco naumanni. Mol. Ecol. 2017; 26(20):5594-5602. DOI 10.1111/mec.14322.Galván I., Moraleda V., Otero I., Álvarez E., Inácio Â. Genetic favouring of pheomelanin-based pigmentation limits physiological benefits of coloniality in lesser kestrels Falco naumanni. Mol. Ecol. 2017; 26(20):5594-5602. DOI 10.1111/mec.14322.Goytain A., Quamme G.A. Functional characterization of the human solute carrier, SLC41A2. Biochem. Biophys. Res. Commun. 2005; 330:701-705. DOI 10.1016/j.bbrc.2005.03.037.Goytain A., Quamme G.A. Functional characterization of the human solute carrier, SLC41A2. Biochem. Biophys. Res. Commun. 2005; 330:701-705. DOI 10.1016/j.bbrc.2005.03.037.Grosz M.D., MacNeil M.D. The ‘‘spotted’’ locus maps to bovine chromosome 6 in a Hereford-cross population. J. Hered. 1999;90:233-236.Grosz M.D., MacNeil M.D. The ‘‘spotted’’ locus maps to bovine chromosome 6 in a Hereford-cross population. J. Hered. 1999;90:233-236.Hardman J.A., Haslam I.S., Farjo N., Farjo B., Paus R. Thyroxine differentially modulates the peripheral clock: lessons from the human hair follicle. PLoS ONE. 2015;10(3):e0121878. DOI 10.1371/ journal.pone.0121878.Hardman J.A., Haslam I.S., Farjo N., Farjo B., Paus R. Thyroxine differentially modulates the peripheral clock: lessons from the human hair follicle. PLoS ONE. 2015;10(3):e0121878. DOI 10.1371/ journal.pone.0121878.Hayes B.J., Pryce J., Chamberlain A.J., Bowman P.J., Goddard M.E. Genetic architecture of complex traits and accuracy of genomic prediction: coat colour, milk-fat percentage, and type in Holstein cattle as contrasting model traits. PLoS Genet. 2010;6(9):e1001139. DOI 10.1371/journal.pgen.1001139.Hayes B.J., Pryce J., Chamberlain A.J., Bowman P.J., Goddard M.E. Genetic architecture of complex traits and accuracy of genomic prediction: coat colour, milk-fat percentage, and type in Holstein cattle as contrasting model traits. PLoS Genet. 2010;6(9):e1001139. DOI 10.1371/journal.pgen.1001139.Izagirre N., García I., Junquera C., de la Rúa C., Alonso S. A scan for signatures of positive selection in candidate loci for skin pigmentation in humans. Mol. Biol. Evol. 2006;23(9):1697-1706. DOI 10.1093/molbev/msl030.Izagirre N., García I., Junquera C., de la Rúa C., Alonso S. A scan for signatures of positive selection in candidate loci for skin pigmentation in humans. Mol. Biol. Evol. 2006;23(9):1697-1706. DOI 10.1093/molbev/msl030.Kang H.M., Sul J.H., Service S.K., Zaitlen N.A., Kong S.Y., Freimer N.B., Sabatti C., Eskin E. Variance component model to account for sample structure in genome-wide association studies. Nat. Genet. 2010;42(4):348-354. DOI 10.1038/ng.548.Kang H.M., Sul J.H., Service S.K., Zaitlen N.A., Kong S.Y., Freimer N.B., Sabatti C., Eskin E. Variance component model to account for sample structure in genome-wide association studies. Nat. Genet. 2010;42(4):348-354. DOI 10.1038/ng.548.Kent W.J., Sugnet C.W., Furey T.S., Roskin K.M., Pringle T.H., Zahler A.M., Haussler D. The human genome browser at UCSC. Genome Res. 2002;12(6):996-1006.Kent W.J., Sugnet C.W., Furey T.S., Roskin K.M., Pringle T.H., Zahler A.M., Haussler D. The human genome browser at UCSC. Genome Res. 2002;12(6):996-1006.Klungland H., Vage D.I. Molecular genetics of pigmentation in domestic animals. Curr. Genomics. 2000;1:232-242. Larkin D.M., Yudin N.S. The genomes and history of domestic animals. Molekulyarnaya genetika, mikrobiologiya i virusologiya = Molecular Genetics, Microbiology and Virology. 2016;4:123-128. (in Russian)Klungland H., Vage D.I. Molecular genetics of pigmentation in domestic animals. Curr. Genomics. 2000;1:232-242. Larkin D.M., Yudin N.S. The genomes and history of domestic animals. Molekulyarnaya genetika, mikrobiologiya i virusologiya = Molecular Genetics, Microbiology and Virology. 2016;4:123-128. (in Russian)Liu L., Harris B., Keehan M., Zhang Y. Genome scan for the degree of white spotting in dairy cattle. Anim. Genet. 2009;40:975-977. DOI 10.1111/j.1365-2052.2009.01936.x.Liu L., Harris B., Keehan M., Zhang Y. Genome scan for the degree of white spotting in dairy cattle. Anim. Genet. 2009;40:975-977. DOI 10.1111/j.1365-2052.2009.01936.x.Luo M., Mengos A.E., Mandarino L.J., Sekulic A. Association of liprin β-1 with kank proteins in melanoma. Exp. Dermatol. 2016;25(4):321323. DOI 10.1111/exd.12933.Luo M., Mengos A.E., Mandarino L.J., Sekulic A. Association of liprin β-1 with kank proteins in melanoma. Exp. Dermatol. 2016;25(4):321323. DOI 10.1111/exd.12933.Mack M., Kowalski E., Grahn R., Bras D., Penedo M.C.T., Bellone R. Two variants in SLC24A5 are associated with “tiger-eye” iris pigmentation in Puerto Rican Paso Fino horses. G3 (Bethesda). 2017; 7(8):2799-2806. DOI 10.1534/g3.117.043786.Mack M., Kowalski E., Grahn R., Bras D., Penedo M.C.T., Bellone R. Two variants in SLC24A5 are associated with “tiger-eye” iris pigmentation in Puerto Rican Paso Fino horses. G3 (Bethesda). 2017; 7(8):2799-2806. DOI 10.1534/g3.117.043786.Mitsui H., Kiecker F., Shemer A., Cannizzaro M.V., Wang C.Q.F., Gulati N., Ohmatsu H., Shah K.R., Gilleaudeau P., SullivanWhalen M., Cueto I., McNutt N.S., Suárez-Fariñas M., Krueger J.G. Discrimination of dysplastic nevi from common melanocytic nevi by cellular and molecular criteria. J. Invest. Dermatol. 2016;136(10):2030-2040. DOI 10.1016/j.jid.2015.11.035.Mitsui H., Kiecker F., Shemer A., Cannizzaro M.V., Wang C.Q.F., Gulati N., Ohmatsu H., Shah K.R., Gilleaudeau P., SullivanWhalen M., Cueto I., McNutt N.S., Suárez-Fariñas M., Krueger J.G. Discrimination of dysplastic nevi from common melanocytic nevi by cellular and molecular criteria. J. Invest. Dermatol. 2016;136(10):2030-2040. DOI 10.1016/j.jid.2015.11.035.Montoliu L., Oetting W.S., Bennett D.C. Color Genes. European Society for Pigment Cell Research. 2017. Available at http://www. espcr.org/micemut.Montoliu L., Oetting W.S., Bennett D.C. Color Genes. European Society for Pigment Cell Research. 2017. Available at http://www. espcr.org/micemut.Morice-Picard F., Lasseaux E., François S., Simon D., Rooryck C., Bieth E., Colin E., Bonneau D., Journel H., Walraedt S., Leroy B.P., Meire F., Lacombe D., Arveiler B. SLC24A5 mutations are associated with non-syndromic oculocutaneous albinism. J. Invest. Dermatol. 2014;134(2):568-571. DOI 10.1038/jid.2013.360.Morice-Picard F., Lasseaux E., François S., Simon D., Rooryck C., Bieth E., Colin E., Bonneau D., Journel H., Walraedt S., Leroy B.P., Meire F., Lacombe D., Arveiler B. SLC24A5 mutations are associated with non-syndromic oculocutaneous albinism. J. Invest. Dermatol. 2014;134(2):568-571. DOI 10.1038/jid.2013.360.Oki R., Yamada K., Nakano S., Kimoto K., Yamamoto K., Kondo H., Kubota T. A Japanese family with autosomal dominant oculocutaneous albinism type 4. Invest. Ophthalmol. Vis. Sci. 2017;58(2):1008-1016. DOI 10.1167/iovs.16-20612.Oki R., Yamada K., Nakano S., Kimoto K., Yamamoto K., Kondo H., Kubota T. A Japanese family with autosomal dominant oculocutaneous albinism type 4. Invest. Ophthalmol. Vis. Sci. 2017;58(2):1008-1016. DOI 10.1167/iovs.16-20612.Olson T.A. The genetic basis for piebald patterns in cattle. J. Hered. 1981;72:113-116.Olson T.A. The genetic basis for piebald patterns in cattle. J. Hered. 1981;72:113-116.Olson T.A. Genetics of color variation. The Genetics of Cattle. Ed. R. Fries, A. Ruvinsky. Wallingford, 1999;33-53.Olson T.A. Genetics of color variation. The Genetics of Cattle. Ed. R. Fries, A. Ruvinsky. Wallingford, 1999;33-53.Pausch H., Wang X., Jung S., Krogmeier D., Edel C., Emmerling R., Götz K.U., Fries R. Identification of QTL for UV-protective eye area pigmentation in cattle by progeny phenotyping and genome-wide association analysis. PLoS ONE. 2012;7:e36346. DOI 10.1371/ journal.pone.0036346.Pausch H., Wang X., Jung S., Krogmeier D., Edel C., Emmerling R., Götz K.U., Fries R. Identification of QTL for UV-protective eye area pigmentation in cattle by progeny phenotyping and genome-wide association analysis. PLoS ONE. 2012;7:e36346. DOI 10.1371/ journal.pone.0036346.Prasolova L.A., Trut L.N. Effect of the “Starˮ gene on the rate of melanoblast migration in silver fox (Vulpes vulpes) embryos. Doklady RAN = Proceedings of the Russian Academy of Sciences. 1993;329: 787-789. (in Russian)Prasolova L.A., Trut L.N. Effect of the “Starˮ gene on the rate of melanoblast migration in silver fox (Vulpes vulpes) embryos. Doklady RAN = Proceedings of the Russian Academy of Sciences. 1993;329: 787-789. (in Russian)Purcell S., Neale B., Todd-Brown K., Thomas L., Ferreira M.A., Bender D., Maller J., Sklar P., de Bakker P.I., Daly M.J., Sham P.C. PLINK: a tool set for whole-genome association and populationbased linkage analyses. Am. J. Hum. Genet. 2007;81(3):559-575. DOI 10.1086/519795.Purcell S., Neale B., Todd-Brown K., Thomas L., Ferreira M.A., Bender D., Maller J., Sklar P., de Bakker P.I., Daly M.J., Sham P.C. PLINK: a tool set for whole-genome association and populationbased linkage analyses. Am. J. Hum. Genet. 2007;81(3):559-575. DOI 10.1086/519795.Raven L.A., Cocks B.G., Hayes B.J. Multibreed genome wide association can improve precision of mapping causative variants underlying milk production in dairy cattle. BMC Genomics. 2014;15:62. DOI 10.1186/1471-2164-15-62.Raven L.A., Cocks B.G., Hayes B.J. Multibreed genome wide association can improve precision of mapping causative variants underlying milk production in dairy cattle. BMC Genomics. 2014;15:62. DOI 10.1186/1471-2164-15-62.Reissmann M., Ludwig A. Pleiotropic effects of coat colour-associated mutations in humans, mice and other mammals. Semin. Cell Dev. Biol. 2013;24(6-7):576-586. DOI 10.1016/j.semcdb.2013.03.014.Reissmann M., Ludwig A. Pleiotropic effects of coat colour-associated mutations in humans, mice and other mammals. Semin. Cell Dev. Biol. 2013;24(6-7):576-586. DOI 10.1016/j.semcdb.2013.03.014.Rizvi T.A., Huang Y., Sidani A., Atit R., Largaespada D.A., Boissy R.E., Ratner N. A novel cytokine pathway suppresses glial cell melanogenesis after injury to adult nerve. J. Neurosci. 2002;22(22):9831-9840.Rizvi T.A., Huang Y., Sidani A., Atit R., Largaespada D.A., Boissy R.E., Ratner N. A novel cytokine pathway suppresses glial cell melanogenesis after injury to adult nerve. J. Neurosci. 2002;22(22):9831-9840.Rosengren Pielberg G., Golovko A., Sundström E., Curik I., Lennartsson J., Seltenhammer M.H., Druml T., Binns M., Fitzsimmons C., Lindgren G., Sandberg K., Baumung R., Vetterlein M., Strömberg S., Grabherr M., Wade C., Lindblad-Toh K., Pontén F., Heldin C.H., Sölkner J., Andersson L. A cis-acting regulatory mutation causes premature hair graying and susceptibility to melanoma in the horse. Nat. Genet. 2008;40:1004-1009. DOI 10.1038/ng.185.Rosengren Pielberg G., Golovko A., Sundström E., Curik I., Lennartsson J., Seltenhammer M.H., Druml T., Binns M., Fitzsimmons C., Lindgren G., Sandberg K., Baumung R., Vetterlein M., Strömberg S., Grabherr M., Wade C., Lindblad-Toh K., Pontén F., Heldin C.H., Sölkner J., Andersson L. A cis-acting regulatory mutation causes premature hair graying and susceptibility to melanoma in the horse. Nat. Genet. 2008;40:1004-1009. DOI 10.1038/ng.185.Rouillier K. Selected Biological Works. Moscow: USSR Academy of Sciences Publ., 1954. (in Russian) Rowan S., Chen C.M., Young T.L., Fisher D.E., Cepko C.L. Transdifferentiation of the retina into pigmented cells in ocular retardation mice defines a new function of the homeodomain gene Chx10. Development. 2004;131(20):5139-5152. DOI 10.1242/ dev.01300.Rouillier K. Selected Biological Works. Moscow: USSR Academy of Sciences Publ., 1954. (in Russian) Rowan S., Chen C.M., Young T.L., Fisher D.E., Cepko C.L. Transdifferentiation of the retina into pigmented cells in ocular retardation mice defines a new function of the homeodomain gene Chx10. Development. 2004;131(20):5139-5152. DOI 10.1242/ dev.01300.Sambrook J., Russell D.W. The Condensed Protocols from Molecular Cloning: a Laboratory Manual. N. Y.: Cold Spring Harbor Laboratory Press, 2006. Schmutz S.M. Genetics of Coat Color in Cattle. Bovine Genomics. Ed. J. Womack. Oxford, 2012;20-33.Sambrook J., Russell D.W. The Condensed Protocols from Molecular Cloning: a Laboratory Manual. N. Y.: Cold Spring Harbor Laboratory Press, 2006. Schmutz S.M. Genetics of Coat Color in Cattle. Bovine Genomics. Ed. J. Womack. Oxford, 2012;20-33.Schmutz S.M., Berryere T.G. Genes affecting coat colour and pattern in domestic dogs: a review. Anim. Genet. 2007;38:539-549. Sharma S., Wagh S., Govindarajan R. Melanosomal proteins – role in melanin polymerization. Pigment Cell Res. 2002;15(2):127-133. DOI 10.1034/j.1600-0749.2002.1o076.x.Schmutz S.M., Berryere T.G. Genes affecting coat colour and pattern in domestic dogs: a review. Anim. Genet. 2007;38:539-549. Sharma S., Wagh S., Govindarajan R. Melanosomal proteins – role in melanin polymerization. Pigment Cell Res. 2002;15(2):127-133. DOI 10.1034/j.1600-0749.2002.1o076.x.Seitz J.J., Schmutz S.M., Thue T.D., Buchanan F.C. A missense mutation in the bovine MGF gene is associated with the roan phenotype in Belgian Blue and Shorthorn cattle. Mamm. Genome. 1999;10: 710-712.Seitz J.J., Schmutz S.M., Thue T.D., Buchanan F.C. A missense mutation in the bovine MGF gene is associated with the roan phenotype in Belgian Blue and Shorthorn cattle. Mamm. Genome. 1999;10: 710-712.Seo K., Mohanty T.R., Choi T., Hwang I. Biology of epidermal and hair pigmentation in cattle: a mini-review. Vet. Dermatol. 2007;18(6): 392-400. DOI 10.1111/j.1365-3164.2007.00634.x.Seo K., Mohanty T.R., Choi T., Hwang I. Biology of epidermal and hair pigmentation in cattle: a mini-review. Vet. Dermatol. 2007;18(6): 392-400. DOI 10.1111/j.1365-3164.2007.00634.x.Storey J.D. A direct approach to false discovery rates. J. R. Stat. Soc. Ser. B. 2002;64:479-498. DOI 10.1111/1467-9868.00346.Storey J.D. A direct approach to false discovery rates. J. R. Stat. Soc. Ser. B. 2002;64:479-498. DOI 10.1111/1467-9868.00346.Sugumaran M., Barek H. Critical analysis of the melanogenic pathway in insects and higher animals. Int. J. Mol. Sci. 2016;17(10):1753. DOI 10.3390/ijms17101753.Sugumaran M., Barek H. Critical analysis of the melanogenic pathway in insects and higher animals. Int. J. Mol. Sci. 2016;17(10):1753. DOI 10.3390/ijms17101753.Taye M., Kim J., Yoon S.H., Lee W., Hanotte O., Dessie T., Kemp S., Mwai O.A., Caetano-Anolles K., Cho S., Oh S.J., Lee H.K., Kim H. Whole genome scan reveals the genetic signature of African Ankole cattle breed and potential for higher quality beef. BMC Genet. 2017;18(1):11. DOI 10.1186/s12863-016-0467-1.Taye M., Kim J., Yoon S.H., Lee W., Hanotte O., Dessie T., Kemp S., Mwai O.A., Caetano-Anolles K., Cho S., Oh S.J., Lee H.K., Kim H. Whole genome scan reveals the genetic signature of African Ankole cattle breed and potential for higher quality beef. BMC Genet. 2017;18(1):11. DOI 10.1186/s12863-016-0467-1.Trapesov O.V. Domestication as the earliest intellectual achievement of mankind. Vavilovskii Zhurnal Genetiki i Selektsii = Vavilov Journal of Genetics and Breeding. 2013;17(4/2):872-883. (in Russian)Trapesov O.V. Domestication as the earliest intellectual achievement of mankind. Vavilovskii Zhurnal Genetiki i Selektsii = Vavilov Journal of Genetics and Breeding. 2013;17(4/2):872-883. (in Russian)Trut L.N. Domestication of animals as the historical process and as the experiment. Informatsionnyy vestnik VOGiS = The Herald of Vavilov Society for Geneticists and Breeders. 2007;11(2):273-289. (in Russian)Trut L.N. Domestication of animals as the historical process and as the experiment. Informatsionnyy vestnik VOGiS = The Herald of Vavilov Society for Geneticists and Breeders. 2007;11(2):273-289. (in Russian)Tsetskhladze Z.R., Canfield V.A., Ang K.C., Wentzel S.M., Reid K.P., Berg A.S., Johnson S.L., Kawakami K., Cheng K.C. Functional assessment of human coding mutations affecting skin pigmentation using zebrafish. PloS ONE. 2012;7(10):e47398. DOI 10.1371/ journal.pone.0047398.Tsetskhladze Z.R., Canfield V.A., Ang K.C., Wentzel S.M., Reid K.P., Berg A.S., Johnson S.L., Kawakami K., Cheng K.C. Functional assessment of human coding mutations affecting skin pigmentation using zebrafish. PloS ONE. 2012;7(10):e47398. DOI 10.1371/ journal.pone.0047398.Wabakken T., Rian E., Kveine M., Aasheim H.C. The human solute carrier SLC41A1 belongs to a novel eukaryotic subfamily with homology to prokaryotic MgtE Mg2+ transporters. Biochem. Biophys. Res. Commun. 2003;306(3):718-724.Wabakken T., Rian E., Kveine M., Aasheim H.C. The human solute carrier SLC41A1 belongs to a novel eukaryotic subfamily with homology to prokaryotic MgtE Mg2+ transporters. Biochem. Biophys. Res. Commun. 2003;306(3):718-724.Wang H., Xue L., Li Y., Zhao B., Chen T., Liu Y., Chang L., Wang J. Distribution and expression of SLC45A2 in the skin of sheep with different coat colors. Folia Histochem. Cytobiol. 2016;54(3):143150. DOI 10.5603/FHC.a2016.0015.Wang H., Xue L., Li Y., Zhao B., Chen T., Liu Y., Chang L., Wang J. Distribution and expression of SLC45A2 in the skin of sheep with different coat colors. Folia Histochem. Cytobiol. 2016;54(3):143150. DOI 10.5603/FHC.a2016.0015.Wilkins A.S., Wrangham R.W., Fitch W.T. The “domestication syndrome” in mammals: a unified explanation based on neural crest cell behavior and genetics. Genetics. 2014;197(3):795-808. DOI 10.1534/genetics.114.165423.Wilkins A.S., Wrangham R.W., Fitch W.T. The “domestication syndrome” in mammals: a unified explanation based on neural crest cell behavior and genetics. Genetics. 2014;197(3):795-808. DOI 10.1534/genetics.114.165423.Yudichev Yu.F., Degtyarev V.V., Khonin G.A. Anatomiya zhivotnykh. Tom 1 [Animal Anatomy. Vol. 1]. Orenburg: OGAU Publ., 2013. (in Russian)Yudichev Yu.F., Degtyarev V.V., Khonin G.A. Anatomiya zhivotnykh. Tom 1 [Animal Anatomy. Vol. 1]. Orenburg: OGAU Publ., 2013. (in Russian)Yurchenko A., Yudin N., Aitnazarov R., Plyusnina A., Brukhin V., Soloshenko V., Lhasaranov B., Popov R., Paronyan I.A., Plemyashov K.V., Larkin D.M. Genome-wide genotyping uncovers genetic profiles and history of the Russian cattle breeds. Heredity. 2018; 120(2):125-137. DOI 10.1038/s41437-017-0024-3.Yurchenko A., Yudin N., Aitnazarov R., Plyusnina A., Brukhin V., Soloshenko V., Lhasaranov B., Popov R., Paronyan I.A., Plemyashov K.V., Larkin D.M. Genome-wide genotyping uncovers genetic profiles and history of the Russian cattle breeds. Heredity. 2018; 120(2):125-137. DOI 10.1038/s41437-017-0024-3.Zhang H., Paijmans J.L., Chang F., Wu X., Chen G., Lei C., Yang X., Wei Z., Bradley D.G., Orlando L., O’Connor T., Hofreiter M. Morphological and genetic evidence for early Holocene cattle management in northeastern China. Nat. Commun. 2013;4:2755. DOI 10.1038/ncomms3755.Zhang H., Paijmans J.L., Chang F., Wu X., Chen G., Lei C., Yang X., Wei Z., Bradley D.G., Orlando L., O’Connor T., Hofreiter M. Morphological and genetic evidence for early Holocene cattle management in northeastern China. Nat. Commun. 2013;4:2755. DOI 10.1038/ncomms3755.Zhu W., Wang L., Dong Z., Chen X., Song F., Liu N., Yang H., Fu J. Comparative transcriptome analysis identifies candidate genes related to skin color differentiation in red tilapia. Sci. Rep. 2016;6:31347. DOI 10.1038/srep31347.Zhu W., Wang L., Dong Z., Chen X., Song F., Liu N., Yang H., Fu J. Comparative transcriptome analysis identifies candidate genes related to skin color differentiation in red tilapia. Sci. Rep. 2016;6:31347. DOI 10.1038/srep31347.

The authors declare that there are no conflicts of interest present.