Signatures of selection and candidate genes for adaptation to extreme environmental factors in the genomes of Turano-Mongolian cattle breeds
https://doi.org/10.18699/VJ21.023
Abstract
Changes in the environment force populations of organisms to adapt to new conditions, either through phenotypic plasticity or through genetic or epigenetic changes. Signatures of selection, such as specific changes in the frequency of alleles and haplotypes, as well as the reduction or increase in genetic diversity, help to identify changes in the cattle genome in response to natural and artificial selection, as well as loci and genetic variants directly affecting adaptive and economically important traits. Advances in genetics and biotechnology enable a rapid transfer of unique genetic variants that have originated in local cattle breeds in the process of adaptation to local environments into the genomes of cosmopolitan high-performance breeds, in order to preserve their outstanding performance in new environments. It is also possible to use genomic selection approach to increase the frequency of already present adaptive alleles in cosmopolitan breeds. The review examines recent work on the origin and evolution of Turano-Mongolian cattle breeds, adaptation of Turano-Mongolian cattle to extreme environments, and summarizes available information on potential candidate genes for climate adaptation of Turano-Mongolian breeds, including cold resistance genes, immune response genes, and high-altitude adaptation genes. The authors conclude that the current literature data do not provide preference to one of the two possible scenarios of Turano-Mongolian breed origins: as a result of the domestication of a wild aurochs at East Asia or as a result of the migration of taurine proto-population from the Middle East. Turano-Mongolian breeds show a high degree of adaptation to extreme climatic conditions (cold, heat, lack of oxygen in the highlands) and parasites (mosquitoes, ticks, bacterial and viral infections). As a result of high-density genotyping and sequencing of genomes and transcriptomes, prospective candidate genes and genetic variants involved in adaptation to environmental factors have recently been identified.
Keywords
About the Authors
N. S. YudinRussian Federation
Novosibirsk
A. A. Yurchenko
Russian Federation
Novosibirsk
D. M. Larkin
Russian Federation
Novosibirsk;
London
References
1. Gendzhieva O.B., Sulimova G.E. The analysis of mutual relations between breeds of horned cattle of the TuranoMongolian group on the basis of DNA polymorphism. Aktual’nyye Voprosy Veterinarnoy Biologii = Actual Questions of Veterinary Biology. 2012;2:1416. (in Russian)
2. Dunin I.M., Dankvert A.G. (Eds.) Breeds and Types of Farm Animals in the Russian Federation. Moscow: AllRussia Research Institute of Animal Breeding, 2013. (in Russian)
3. Lazebnaya I.V., Perchun A.V., Lhasaranov B.B., Lazebny O.E., Stolpovskiy Yu.A. Analysis of GH1, GHR and PRL gene polymorphisms for estimation of the genetic diversity of Buryat and Altai cattle breeds. Vavilovskii Zhurnal Genetiki i Selektsii = Vavilov Journal of Genetics and Breeding. 2018;22(6):734741. DOI 10.18699/VJ18.417.
4. Moiseeva I.G., Ukhanov S.V., Stolpovsky Yu.A., Sulimova G.E., Kashtanov S.N. Gene Pools of Farm Animals. Moscow: Nauka Publ., 2006. (in Russian)
5. Achilli A., Bonfiglio S., Olivieri A., Malusà A., Pala M., Hooshiar Kashani B., Perego U.A., AjmoneMarsan P., Liotta L., Semino O., Bandelt H.J., Ferretti L., Torroni A. The multifaceted origin of taurine cattle reflected by the mitochondrial genome. PLoS One. 2009; 4(6):e5753. DOI 10.1371/journal.pone.0005753.
6. Achilli A., Olivieri A., Pellecchia M., Uboldi C., Colli L., AlZahery N., Accetturo M., Pala M., Hooshiar Kashani B., Perego U.A., Battaglia V., Fornarino S., Kalamati J., Houshmand M., Negrini R., Semino O., Richards M., Macaulay V., Ferretti L., Bandelt H.J., AjmoneMarsan P., Torroni A. Mitochondrial genomes of extinct aurochs survive in domestic cattle. Curr. Biol. 2008;18(4):R157158. DOI 10.1016/j.cub.2008.01.019.
7. Ai H., Fang X., Yang B., Huang Z., Chen H., Mao L., Zhang F., Zhang L., Cui L., He W., Yang J., Yao X., Zhou L., Han L., Li J., Sun S., Xie X., Lai B., Su Y., Lu Y., Yang H., Huang T., Deng W., Nielsen R., Ren J., Huang L. Adaptation and possible ancient interspecies introgression in pigs identified by wholegenome sequencing. Nat. Genet. 2015;47(3):217225. DOI 10.1038/ng.3199.
8. Alexander D.H., Lange K. Enhancements to the ADMIXTURE algorithm for individual ancestry estimation. BMC Bioinformatics. 2011; 12:246. DOI 10.1186/1471210512246.
9. Bartelt A., Bruns O.T., Reimer R., Hohenberg H., Ittrich H., Peldschus K., Kaul M.G., Tromsdorf U.I., Weller H., Waurisch C., Eychmüller A., Gordts P.L., Rinninger F., Bruegelmann K., Freund B., Nielsen P., Merkel M., Heeren J. Brown adipose tissue activity controls triglyceride clearance. Nat. Med. 2011;17(2):200205. DOI 10.1038/nm.2297.
10. Belgnaoui S.M., Paz S., Hiscott J. Orchestrating the interferon antiviral response through the mitochondrial antiviral signaling (MAVS) adapter. Curr. Opin. Immunol. 2011;23(5):564572. DOI 10.1016/j.coi.2011.08.001.
11. Bharti D., Kumar A., Mahla R.S., Kumar S., Ingle H., Shankar H., Joshi B., Raut A.A., Kumar H. The role of TLR9 polymorphism in susceptibility to pulmonary tuberculosis. Immunogenetics. 2014; 66(12):675681. DOI 10.1007/s0025101408061.
12. Bigham A., Bauchet M., Pinto D., Mao X., Akey J.M., Mei R., Scherer S.W., Julian C.G., Wilson M.J., López Herráez D., Brutsaert T.,Parra E.J., Moore L.G., Shriver M.D. Identifying signatures of natural selection in Tibetan and Andean populations using dense genome scan data. PLoS Genet. 2010;6(9):e1001116. DOI 10.1371/journal.pgen.1001116.
13. Boitard S., Boussaha M., Capitan A., Rocha D., Servin B. Uncovering adaptation from sequence data: lessons from genome resequencing of four cattle breeds. Genetics. 2016;203(1):433450. DOI 10.1534/genetics.115.181594.
14. Bollongino R., Burger J., Powell A., Mashkour M., Vigne J.D., Thomas M.G. Modern taurine cattle descended from small number of neareastern founders. Mol. Biol. Evol. 2012;29(9):21012104. DOI 10.1093/molbev/mss092.
15. Bradley D.G., Magee D.A. Genetics and the origins of domestic cattle. In: Zeder M.A., Bradley D.G., Emshwiller E., Smith B.D. (Eds.). Documenting Domestication: New Genetic and Archaeological Paradigms. Berkeley: Univ. of California Press, 2006;317328.
16. CaetanoAnolles K., Kim K., Kwak W., Sung S., Kim H., Choi B.H., Lim D. Genome sequencing and protein domain annotations of Korean Hanwoo cattle identify Hanwoospecific immunityrelated and other novel genes. BMC Genet. 2018;19(1):37. DOI 10.1186/s128630180623x.
17. Cai X., Chen H., Wang S., Xue K., Lei C. Polymorphisms of two Y chromosome microsatellites in Chinese cattle. Genet. Sel. Evol. 2006;38(5):525534.
18. Cardona A., Pagani L., Antao T., Lawson D.J., Eichstaedt C.A., Yngvadottir B., Shwe M.T., Wee J., Romero I.G., Raj S., Metspalu M., Villems R., Willerslev E., TylerSmith C., Malyarchuk B.A., Derenko M.V., Kivisild T. Genomewide analysis of cold adaptation in indigenous Siberian populations. PLoS One. 2014;9(5):e98076. DOI 10.1371/journal.pone.0098076.
19. Chan E.K., Nagaraj S.H., Reverter A. The evolution of tropical adaptation: comparing taurine and zebu cattle. Anim. Genet. 2010;41(5): 467477. DOI 10.1111/j.13652052.2010.02053.x.
20. Chen H.H., Tsai L.J., Lee K.R., Chen Y.M., Hung W.T., Chen D.Y. Genetic association of complement component 2 polymorphism with systemic lupus erythematosus. Tissue Antigens. 2015;86(2): 122133. DOI 10.1111/tan.12602.
21. Chen N., Cai Y., Chen Q., Li R., Wang K., Huang Y., Hu S., Huang S., Zhang H., Zheng Z., Song W., Ma Z., Ma Y., Dang R., Zhang Z., Xu L., Jia Y., Liu S., Yue X., Deng W., Zhang X., Sun Z., Lan X., Han J., Chen H., Bradley D.G., Jiang Y., Lei C. Wholegenome resequencing reveals worldwide ancestry and adaptive introgression events of domesticated cattle in East Asia. Nat. Commun. 2018a; 9(1):2337. DOI 10.1038/s41467018047370.
22. Chen N., Huang J., Zulfiqar A., Li R., Xi Y., Zhang M., Dang R., Lan X., Chen H., Ma Y., Lei C. Population structure and ancestry of Qinchuan cattle. Anim. Genet. 2018b;49(3):246248. DOI 10.1111/age.12658.
23. Chen Y., Zeng B., Shi P., Xiao H., Chen S. Comparative analysis of the liver and spleen transcriptomes between Holstein and Yunnan humped cattle. Animals (Basel). 2019;9(8):527. DOI 10.3390/ani9080527.
24. Choy Y.H., Seo J.H., Park B., Lee S., Choi J., Jung K., Kong H. Studies on genetic diversity and phylogenetic relationships of Chikso (Korea native brindle cattle) using the microsatellite marker. J. Life Sci. 2015;25:624630. DOI 10.5352/JLS.2015.25.6.624.
25. Decker J.E., McKay S.D., Rolf M.M., Kim J., Molina Alcalá A., Sonstegard T.S., Hanotte O., Götherström A., Seabury C.M., Praharani L., Babar M.E., Correia de Almeida Regitano L., Yildiz M.A., Heaton M.P., Liu W.S., Lei C.Z., Reecy J.M., SaifUrRehman M., Schnabel R.D., Taylor J.F. Worldwide patterns of ancestry, divergence, and admixture in domesticated cattle. PLoS Genet. 2014; 10(3):e1004254. DOI 10.1371/journal.pgen.1004254.
26. Dho S.H., Lim J.C., Kim L.K. Beyond the role of CD55 as a complement component. Immune Netw. 2018;18(1):e11. DOI 10.4110/in.2018.18.e11.
27. Dmitriev N.G., Ernst L.K. (Eds.). Animal Genetics Resources of the USSR. Rome, Italy: Food and Agriculture Organization of the United Nations, 1989. Available at http://www.fao.org/3/ah759e/ah759e00.htm. Retrieved at October 2, 2019.
28. Ermert D., Blom A.M. C4bbinding protein: the good, the bad and the deadly. Novel functions of an old friend. Immunol. Lett. 2016;169: 8292. DOI 10.1016/j.imlet.2015.11.014.
29. Felius M., Koolmees P.A., Theunissen B., European Cattle Genetic Diversity Consortium, Lenstra J.A. On the breeds of cattle – historic and current classifications. Diversity. 2011;3:660692. DOI 10.3390/d3040660.
30. Ferreira J.V., Fôfo H., Bejarano E., Bento C.F., Ramalho J.S., Girão H., Pereira P. STUB1/CHIP is required for HIF1A degradation by chaperonemediated autophagy. Autophagy. 2013;9(9):13491366. DOI 10.4161/auto.25190.
31. Gao Y., Gautier M., Ding X., Zhang H., Wang Y., Wang X., Faruque M.O., Li J., Ye S., Gou X., Han J., Lenstra J.A., Zhang Y. Species composition and environmental adaptation of indigenous Chinese cattle. Sci. Rep. 2017;7(1):16196. DOI 10.1038/s41598017164387.
32. Garvie C.W., Stagno J.R., Reid S., Singh A., Harrington E., Boss J.M. Characterization of the RFX complex and the RFX5(L66A) mutant: implications for the regulation of MHC class II gene expression. Biochemistry. 2007;46(6):15971611.
33. Gautier M., MoazamiGoudarzi K., Levéziel H., Parinello H., Grohs C., Rialle S., Kowalczyk R., Flori L. Deciphering the wisent demographic and adaptive histories from individual wholegenome sequences. Mol. Biol. Evol. 2016;33(11):28012814. DOI 10.1093/molbev/msw144.
34. Glatz J.F., Luiken J.J., Bonen A. Membrane fatty acid transporters as regulators of lipid metabolism: implications for metabolic disease. Physiol. Rev. 2010;90(1):367417. DOI 10.1152/physrev.00003.2009.
35. Gotoh T., Nishimura T., Kuchida K., Mannen H. The Japanese Wagyu beef industry: current situation and future prospects – a review. Asian-Australas. J. Anim. Sci. 2018;31(7):933950. DOI 10.5713/ajas.18.0333.
36. Higgins C.A., Petukhova L., Harel S., Ho Y.Y., Drill E., Shapiro L., Wajid M., Christiano A.M. FGF5 is a crucial regulator of hair length in humans. Proc. Natl. Acad. Sci. USA. 2014;111(29):1064810653. DOI 10.1073/pnas.1402862111.
37. Hou Q., Huang J., Ju Z., Li Q., Li L., Wang C., Sun T., Wang L., Hou M., Hang S., Zhong J. Identification of splice variants, targeted microRNAs and functional single nucleotide polymorphisms of the BOLA-DQA2 gene in dairy cattle. DNA Cell Biol. 2012;31(5):739744. DOI 10.1089/dna.2011.1402.
38. Huai Q., Zhiyong J., Zhijie C. A survey of cattle production in China. World Review Animal. FAO. 1993;76:1218.
39. Islam F., Gopalan V., Lam A.K. RETREG1 (FAM134B): a new player in human diseases: 15 years after the discovery in cancer. J. Cell. Physiol. 2018;233(6):44794489. DOI 10.1002/jcp.26384.
40. IsoTouru T., Tapio M., Vilkki J., Kiseleva T., Ammosov I., Ivanova Z., Popov R., Ozerov M., Kantanen J. Genetic diversity and genomic signatures of selection among cattle breeds from Siberia, eastern and northern Europe. Anim. Genet. 2016;47(6):647657. DOI 10.1111/age.12473.
41. Jeong J., Kwon E.G., Im S.K., Seo K.S., Baik M. Expression of fat deposition and fat removal genes is associated with intramuscular fat content in longissimus dorsi muscle of Korean cattle steers. J. Anim. Sci. 2012;90(6):20442053. DOI 10.2527/jas.20114753.
42. Jo C., Cho S.H., Chang J., Nam K.C. Keys to production and processing of Hanwoo beef: a perspective of tradition and science. Anim. Front. 2012;2(4):3238. DOI 10.2527/af.20120060.
43. Johnson H., Scorrano L., Korsmeyer S.J., Ley T.J. Cell death induced by granzyme C. Blood. 2003;101(8):30933101.
44. Kaempfer R., Arad G., Levy R., Hillman D., Nasie I., Rotfogel Z. CD28: direct and critical receptor for superantigen toxins. Toxins (Basel). 2013;5(9):15311542. DOI 10.3390/toxins5091531.
45. Kantanen J., Edwards C.J., Bradley D.G., Viinalass H., Thessler S., Ivanova Z., Kiselyova T., Cinkulov M., Popov R., Stojanović S., Ammosov I., Vilkki J. Maternal and paternal genealogy of Eurasian taurine cattle (Bos taurus). Heredity. 2009;103(5):404415. DOI 10.1038/hdy.2009.68.
46. Kantanen J., Lovendahl P., Strandberg E., Eythorsdottir E., Li M.H., KettunenPraebel A., Berg P., Meuwissen T. Utilization of farm animal genetic resources in a changing agroecological environment in the Nordic countries. Front. Genet. 2015;6:52. DOI 10.3389/fgene.2015.00052.
47. Kasanmoentalib E.S., Valls Seron M., Ferwerda B., Tanck M.W., Zwinderman A.H., Baas F., van der Ende A., Schwaeble W.J., Brouwer M.C., van de Beek D. Mannosebinding lectinassociated serine protease 2 (MASP2) contributes to poor disease outcome in humans and mice with pneumococcal meningitis. J. Neuroinflammation. 2017;14(1):2. DOI 10.1186/s1297401607709.
48. KawaharaMiki R., Tsuda K., Shiwa Y., AraiKichise Y., Matsumoto T., Kanesaki Y., Oda S., Ebihara S., Yajima S., Yoshikawa H., Kono T. Wholegenome resequencing shows numerous genes with nonsynonymous SNPs in the Japanese native cattle KuchinoshimaUshi. BMC Genom. 2011;12:103. DOI 10.1186/1471216412103.
49. Kiermayer C., Northrup E., Schrewe A., Walch A., de Angelis M.H., Schoensiegel F., Zischka H., Prehn C., Adamski J., Bekeredjian R., Ivandic B., Kupatt C., Brielmeier M. Heartspecific knockout of the mitochondrial thioredoxin reductase (Txnrd2) induces metabolic and contractile dysfunction in the aging myocardium. J. Am. Heart Assoc. 2015;4(7):e002153. DOI 10.1161/JAHA.115.002153.
50. Kurth I., Pamminger T., Hennings J.C., Soehendra D., Huebner A.K., Rotthier A., Baets J., Senderek J., Topaloglu H., Farrell S.A., Nürnberg G., Nürnberg P., De Jonghe P., Gal A., Kaether C., Timmerman V., Hübner C.A. Mutations in FAM134B, encoding a newly identified Golgi protein, cause severe sensory and autonomic neuropathy. Nat. Genet. 2009;41(11):11791181. DOI 10.1038/ng.464.
51. KussDuerkop S.K., KeestraGounder A.M. NOD1 and NOD2 activation by diverse stimuli: a possible role for sensing pathogeninduced endoplasmic reticulum stress. Infect. Immun. 2020;88:e0089819. DOI 10.1128/IAI.0089819.
52. Lai S.J., Liu Y.P., Liu Y.X., Li X.W., Yao Y.G. Genetic diversity and origin of Chinese cattle revealed by mtDNA Dloop sequence variation. Mol. Phylogenet. Evol. 2006;38(1):146154.
53. Larson G., Burger J. A population genetics view of animal domestication. Trends Genet. 2013;29(4):197205. DOI 10.1016/j.tig.2013.01.003.
54. Lee S.H., Park B.H., Sharma A., Dang C.G., Lee S.S., Choi T.J., Choy Y.H., Kim H.C., Jeon K.J., Kim S.D., Yeon S.H., Park S.B., Kang H.S. Hanwoo cattle: origin, domestication, breeding strategies and genomic selection. J. Anim. Sci. Technol. 2014;56:2. DOI 10.1186/20550391562.
55. Lee T., Cho S., Seo K.S., Chang J., Kim H., Yoon D. Genetic variants and signatures of selective sweep of Hanwoo population (Korean native cattle). BMB Rep. 2013;46(7):346351.
56. Li M.H., Kantanen J. Genetic structure of Eurasian cattle (Bos taurus) based on microsatellites: clarification for their breed classification. Anim. Genet. 2010;41(2):150158. DOI 10.1111/j.13652052.2009.01980.x.
57. Li M.H., Tapio I., Vilkki J., Ivanova Z., Kiselyova T., Marzanov N., Cinkulov M., Stojanovic S., Ammosov I., Popov R., Kantanen J. The genetic structure of cattle populations (Bos taurus) in northern Eurasia and the neighbouring Near Eastern regions: implications for breeding strategies and conservation. Mol. Ecol. 2007;16(18):38393853.
58. Li Y., Tran Q., Shrestha R., Piao L., Park S., Park J., Park J. LETM1 is required for mitochondrial homeostasis and cellular viability (review). Mol. Med. Rep. 2019;19(5):33673375. DOI 10.3892/mmr.2019.10041.
59. Librado P., Der Sarkissian C., Ermini L., Schubert M., Jónsson H., Albrechtsen A., Fumagalli M., Yang M.A., Gamba C., SeguinOrlando A., Mortensen C.D., Petersen B., Hoover C.A., LorenteGaldos B., Nedoluzhko A., Boulygina E., Tsygankova S., Neuditschko M., Jagannathan V., Thèves C., Alfarhan A.H., Alquraishi S.A., AlRasheid K.A., SicheritzPonten T., Popov R., Grigoriev S., Alekseev A.N., Rubin E.M., McCue M., Rieder S., Leeb T., Tikhonov A., Crubézy E., Slatkin M., MarquesBonet T., Nielsen R., Willerslev E., Kantanen J., Prokhortchouk E., Orlando L. Tracking the origins of Yakutian horses and the genetic basis for their fast adaptation to subarctic environments. Proc. Natl. Acad. Sci. USA. 2015; 112(50):E6889E6897. DOI 10.1073/pnas.1513696112.
60. Liu G.E., Bickhart D.M. Copy number variation in the cattle genome. Funct. Integr. Genomics. 2012;12(4):609624. DOI 10.1007/s1014201202899.
61. Lu P., Brunson K., Yuan J., Li Z. Zooarchaeological and genetic evidence for the origins of domestic cattle in ancient China. Asian Perspect. 2017;56:92120. DOI 10.1353/asi.2017.0003.
62. Mannen H., Kohno M., Nagata Y., Tsuji S., Bradley D.G., Yeo J.S., Nyamsamba D., Zagdsuren Y., Yokohama M., Nomura K., Amano T. Independent mitochondrial origin and historical genetic differentiation in North Eastern Asian cattle. Mol. Phylogenet. Evol. 2004; 32(2):539544.
63. Mei C., Junjvlieke Z., Raza S.H.A., Wang H., Cheng G., Zhao C., Zhu W., Zan L. Copy number variation detection in Chinese indigenous cattle by whole genome sequencing. Genomics. Available online 2019. Publ. 2020;112(1):831836. DOI 10.1016/j.ygeno.2019.05.023.
64. Mei C., Wang H., Zhu W., Wang H., Cheng G., Qu K., Guang X., Li A., Zhao C., Yang W., Wang C., Xin Y., Zan L. Wholegenome sequencing of the endangered bovine species Gayal (Bos frontalis) provides new insights into its genetic features. Sci. Rep. 2016;6:19787. DOI 10.1038/srep19787.
65. Motwani M., Pesiridis S., Fitzgerald K.A. DNA sensing by the cGASSTING pathway in health and disease. Nat. Rev. Genet. 2019; 20(11):657674. DOI 10.1038/s4157601901511.
66. Mukherjee S., Huda S., Sinha Babu S.P. Tolllike receptor polymorphism in host immune response to infectious diseases: a review. Scand. J. Immunol. 2019;90(1):e12771. DOI 10.1111/sji.12771.
67. Mustafa H., Khan W., Kuthu Z., EuiSoo K., Ajmal A., Javed K., Pasha T., Ali A., Javed M.T., Sonstegard T.S. Genomewide survey of selection signatures in Pakistani cattle breeds. Pak. Vet. J. 2018;38(2):214218. DOI 10.29261/pakvetj/2018.051.
68. Niture S., Moore J., Kumar D. TNFAIP8: inflammation, immunity and human diseases. J. Cell Immunol. 2019;1(2):2934.
69. Pautasso M. Ten simple rules for writing a literature review. PLoS Comput. Biol. 2013;9(7):e1003149. DOI 10.1371/journal.pcbi.1003149.
70. Peilieu С. Livestock Breeds of China (FAO Animal Production and Health Paper 46). Rome: Food and Agriculture Organization of the United Nations, 1984. Available at http://www.fao.org/3/x6549e/x6549e00.pdf. Retrieved on April 10, 2020.
71. Piao L., Li Y., Kim S.J., Byun H.S., Huang S.M., Hwang S.K., Yang K.J., Park K.A., Won M., Hong J., Hur G.M., Seok J.H., Shong M., Cho M.H., Brazil D.P., Hemmings B.A., Park J. Association of LETM1 and MRPL36 contributes to the regulation of mitochondrial ATP production and necrotic cell death. Cancer Res. 2009;69(8):33973404. DOI 10.1158/00085472.CAN083235.
72. Pokharel K., Weldenegodguad M., Popov R., Honkatukia M., Huuki H., Lindeberg H., Peippo J., Reilas T., Zarovnyaev S., Kantanen J. Whole blood transcriptome analysis reveals footprints of cattle adaptation to subarctic conditions. Anim. Genet. 2019;50(3):217227. DOI 10.1111/age.12783.
73. Porter V., Alderson L., Hall S.J.G., Sponenberg D.P. (Eds.) Mason’s World Encyclopedia of Livestock Breeds and Breeding. Wallingford, UK: CABI Publ., 2016.
74. PortoNeto L.R., Lee S.H., Sonstegard T.S., Van Tassell C.P., Lee H.K., Gibson J.P., Gondro C. Genomewide detection of signatures of selection in Korean Hanwoo cattle. Anim. Genet. 2014;45(2):180190. DOI 10.1111/age.12119.
75. Putri M., Syamsunarno M.R., Iso T., Yamaguchi A., Hanaoka H., Sunaga H., Koitabashi N., Matsui H., Yamazaki C., Kameo S., Tsushima Y., Yokoyama T., Koyama H., Abumrad N.A., Kurabayashi M. CD36 is indispensable for thermogenesis under conditions of fasting and cold stress. Biochem. Biophys. Res. Commun. 2015;457(4):520525. DOI 10.1016/j.bbrc.2014.12.124.
76. Qiu Q., Zhang G., Ma T., Qian W., Wang J., Ye Z., Cao C., Hu Q., Kim J., Larkin D.M., Auvil L., Capitanu B., Ma J., Lewin H.A., Qian X., Lang Y., Zhou R., Wang L., Wang K., Xia J., Liao S., Pan S., Lu X., Hou H., Wang Y., Zang X., Yin Y., Ma H., Zhang J., Wang Z., Zhang Y., Zhang D., Yonezawa T., Hasegawa M., Zhong Y., Liu W., Zhang Y., Huang Z., Zhang S., Long R., Yang H., Wang J., Lenstra J.A., Cooper D.N., Wu Y., Wang J., Shi P., Wang J., Liu J. The yak genome and adaptation to life at high altitude. Nat. Genet. 2012; 44(8):946949. DOI 10.1038/ng.2343.
77. Quarta S., Mitrić M., Kalpachidou T., Mair N., SchiefermeierMach N., Andratsch M., Qi Y., Langeslag M., Malsch P., RoseJohn S., Kress M. Impaired mechanical, heat, and cold nociception in a murine model of genetic TACE/ADAM17 knockdown. FASEB J. 2019; 33(3):44184431. DOI 10.1096/fj.201801901R.
78. Randhawa I.A., Khatkar M.S., Thomson P.C., Raadsma H.W. A metaassembly of selection signatures in cattle. PLoS One. 2016;11(4): e0153013. DOI 10.1371/journal.pone.0153013.
79. Reynés B., Klein Hazebroek M., GarcíaRuiz E., Keijer J., Oliver P., Palou A. Specific features of the hypothalamic leptin signaling response to cold exposure are reflected in peripheral blood mononuclear cells in rats and ferrets. Front. Physiol. 2017;8:581. DOI 10.3389/fphys.2017.00581.
80. Sambarey A., Devaprasad A., Baloni P., Mishra M., Mohan A., Tyagi P., Singh A., Akshata J.S., Sultana R., Buggi S., Chandra N. Metaanalysis of host response networks identifies a common core in tuberculosis. NPJ Syst. Biol. Appl. 2017;3:4. DOI 10.1038/s4154001700054.
81. Seelige R., SaddawiKonefka R., Adams N.M., Picarda G., Sun J.C., Benedict C.A., Bui J.D. Interleukin17D and Nrf2 mediate initial innate immune cell recruitment and restrict MCMV infection. Sci. Rep. 2018;8(1):13670. DOI 10.1038/s41598018320112.
82. Sermyagin A.A., Dotsev A.V., Gladyr E.A., Traspov A.A., Deniskova T.E., Kostyunina O.V., Reyer H., Wimmers K., Barbato M., Paronyan I.A., Plemyashov K.V., Sölkner J., Popov R.G., Brem G., Zinovieva N.A. Wholegenome SNP analysis elucidates the genetic structure of Russian cattle and its relationship with Eurasian taurine breeds. Genet. Sel. Evol. 2018;50(1):37. DOI 10.1186/s1271101804088.
83. Shen J., Hanif Q., Cao Y., Yu Y., Lei C., Zhang G., Zhao Y. Whole genome scan and selection signatures for climate adaption in Yanbian cattle. Front. Genet. 2020;11:94. DOI 10.3389/fgene.2020. 00094.
84. Shi Q., Mu X., Hong L., Zheng S. SERPINE1 rs1799768 polymorphism contributes to sepsis risk and mortality. J. Renin-AngiotensinAldosterone Syst. 2015;16(4):12181224. DOI 10.1177/1470320315614714.
85. Simonsen M., Mailund T., Pedersen C.N. Inference of large phylogenies using neighbourjoining. In: International Joint Conference on Biomedical Engineering Systems and Technologies (BIOSTEC 2010), Valencia, Spain, 20–23 January 2010. Berlin; Heidelberg: Springer, 2010;334344.
86. Stranden I., Kantanen J., Russo I.M., OrozcoterWengel P., Bruford M.W., Climgen Consortium. Genomic selection strategies for breeding adaptation and production in dairy cattle under climate change. Heredity (Edinb.). 2019;123(3):307317. DOI 10.1038/s4143701902071.
87. Sun W., Chen H., Lei C., Lei X., Zhang Y. Genetic variation in eight Chinese cattle breeds based on the analysis of microsatellite markers. Genet. Sel. Evol. 2008;40(6):68166892. DOI 10.1051/gse:2008027.
88. Svishcheva G., Babayan O., Lkhasaranov B., Tsendsuren A., Abdurasulov A., Stolpovsky Y. Microsatellite diversity and phylogenetic relationships among East Eurasian Bos taurus breeds with an emphasis on rare and ancient local cattle. Animals (Basel). 2020;10(9):1493. DOI 10.3390/ani10091493.
89. Takatsu K. Interleukin5 and IL5 receptor in health and diseases. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci. 2011;87(8):463485. DOI 10.2183/pjab.87.463.
90. Tapio I., Tapio M., Li M.H., Popov R., Ivanova Z., Kantanen J. Estimation of relatedness among nonpedigreed Yakutian cryobank bulls using molecular data: implications for conservation and breed management. Genet. Sel. Evol. 2010;42:28. DOI 10.1186/129796864228.
91. Tom Tang Y., Emtage P., Funk W.D., Hu T., Arterburn M., Park E.E., Rupp F. TAFA: a novel secreted family with conserved cysteine residues and restricted expression in the brain. Genomics. 2004;83(4): 727734. DOI 10.1016/j.ygeno.2003.10.006.
92. Tsuda K., KawaharaMiki R., Sano S., Imai M., Noguchi T., Inayoshi Y., Kono T. Abundant sequence divergence in the native Japanese cattle MishimaUshi (Bos taurus) detected using wholegenome sequencing. Genomics. 2013;102(4):372378. DOI 10.1016/j.ygeno.2013.08.002.
93. Tsukamoto H., Takeuchi S., Kubota K., Kobayashi Y., Kozakai S., Ukai I., Shichiku A., Okubo M., Numasaki M., Kanemitsu Y., Matsumoto Y., Nochi T., Watanabe K., Aso H., Tomioka Y. Lipopolysaccharide (LPS)binding protein stimulates CD14dependent Tolllike receptor 4 internalization and LPSinduced TBK1IKKϵIRF3 axis activation. J. Biol. Chem. 2018;293(26):1018610201. DOI 10.1074/jbc.M117.796631.
94. Wang M.S., Li Y., Peng M.S., Zhong L., Wang Z.J., Li Q.Y., Tu X.L., Dong Y., Zhu C.L., Wang L., Yang M.M., Wu S.F., Miao Y.W., Liu J.P., Irwin D.M., Wang W., Wu D.D., Zhang Y.P. Genomic analyses reveal potential independent adaptation to high altitude in Tibetan сhickens. Mol. Biol. Evol. 2015;32(7):18801889. DOI 10.1093/molbev/msv071.
95. Wang Z., Ma H., Xu L., Zhu B., Liu Y., Bordbar F., Chen Y., Zhang L., Gao X., Gao H., Zhang S., Xu L., Li J. Genomewide scan identifies selection signatures in Chinese Wagyu сattle using a highdensity SNP array. Animals (Basel). 2019;9(6):pii:E296. DOI 10.3390/ani9060296.
96. Weldenegodguad M., Popov R., Pokharel K., Ammosov I., Ming Y., Ivanova Z., Kantanen J. Wholegenome sequencing of three native cattle breeds originating from the northernmost cattle farming regions. Front. Genet. 2019;9:728. DOI 10.3389/fgene.2018.00728.
97. Wu D.D., Ding X.D., Wang S., Wójcik J.M., Zhang Y., Tokarska M., Li Y., Wang M.S., Faruque O., Nielsen R., Zhang Q., Zhang Y.P. Pervasive introgression facilitated domestication and adaptation in the Bos species complex. Nat. Ecol. Evol. 2018;2(7):11391145. DOI 10.1038/s415590180562y.
98. Wu S., De Croos J.N., Storey K.B. Cold acclimationinduced upregulation of the ribosomal protein L7 gene in the freeze tolerant wood frog, Rana sylvatica. Gene. 2008;424(12):4855. DOI 10.1016/j.gene.2008.07.023.
99. Xia X., Qu K., Zhang G., Jia Y., Ma Z., Zhao X., Huang Y., Chen H., Huang B., Lei C. Comprehensive analysis of the mitochondrial DNA diversity in Chinese cattle. Anim. Genet. 2019;50(1):7073. DOI 10.1111/age.12749.
100. Xu Y., Jiang Y., Shi T., Cai H., Lan X., Zhao X., Plath M., Chen H. Wholegenome sequencing reveals mutational landscape underlying phenotypic differences between two widespread Chinese cattle breeds. PLoS One. 2017;12(8):e0183921. DOI 10.1371/journal.pone.0183921.
101. Yamamoto H., Fara A.F., Dasgupta P., Kemper C. CD46: the ‘multitasker’ of complement proteins. Int. J. Biochem. Cell. Biol. 2013; 45(12):28082820. DOI 10.1016/j.biocel.2013.09.016.
102. Yeh T.Y., Beiswenger K.K., Li P., Bolin K.E., Lee R.M., Tsao T.S., Murphy A.N., Hevener A.L., Chi N.W. Hypermetabolism, hyperphagia, and reduced adiposity in tankyrasedeficient mice. Diabetes. 2009; 58(11):24762485. DOI 10.2337/db081781.
103. Yurchenko A.A., Daetwyler H.D., Yudin N., Schnabel R.D., Vander Jagt C.J., Soloshenko V., Lhasaranov B., Popov R., Taylor J.F., Larkin D.M. Scans for signatures of selection in Russian cattle breed genomes reveal new candidate genes for environmental adaptation and acclimation. Sci. Rep. 2018a;8(1):12984. DOI 10.1038/s4159801831304w.
104. 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. Genomewide genotyping uncovers genetic profiles and history of the Russian cattle breeds. Heredity (Edinb.). 2018b;120(2):125137. DOI 10.1038/s4143701700243.
105. 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.
106. Zhang T., Chen H., Qi L., Zhang J., Wu R., Zhang Y., Sun Y. Transcript profiling identifies early response genes against FMDV infection in PK15 cells. Viruses. 2018;10(7):364. DOI 10.3390/v10070364.
107. Zhang W., Gao X., Zhang Y., Zhao Y., Zhang J., Jia Y., Zhu B., Xu L., Zhang L., Gao H., Li J., Chen Y. Genomewide assessment of genetic diversity and population structure insights into admixture and introgression in Chinese indigenous cattle. BMC Genet. 2018;19: 114. DOI 10.1186/s1286301807059.
108. Zhang X., Wang K., Wang L., Yang Y., Ni Z., Xie X., Shao X., Han J., Wan D., Qiu Q. Genomewide patterns of copy number variation in the Chinese yak genome. BMC Genom. 2016;17:379. DOI 10.1186/s1286401627026.
109. Zhang Y., Hu Y., Wang X., Jiang Q., Zhao H., Wang J., Ju Z., Yang L., Gao Y., Wei X., Bai J., Zhou Y., Huang J. Population structure, and selection signatures underlying highaltitude adaptation inferred from genomewide copy number variations in Chinese indigenous cattle. Front. Genet. 2020;10:1404. DOI 10.3389/fgene.2019.01404.
110. Zhao Y.X., Yang J., Lv F.H., Hu X.J., Xie X.L., Zhang M., Li W.R., Liu M.J., Wang Y.T., Li J.Q., Liu Y.G., Ren Y.L., Wang F., Hehua E., Kantanen J., Arjen Lenstra J., Han J.L., Li M.H. Genomic reconstruction of the history of native sheep reveals the peopling patterns of nomads and the expansion of early pastoralism in East Asia. Mol. Biol. Evol. 2017;34(9):23802395. DOI 10.1093/molbev/msx181.