PLANT BIOLOGY
ANIMAL BIOLOGY
SUBSCRIPTION
E-SUBSCRIPTION
 
MAP
MAIN PAGE

 

 

 

 

Abdelmanova A.S., Fornara M.S., Bardukov N.V., Sermyagin A.A., Dotsev A.V., Zinovieva N.A. Whole genome study of single nucleotide polymorphisms’ associations with withers height in local and transboundary breeds in Russia. Sel'skokhozyaistvennaya Biologiya [Agricultural Biology], 2021, Vol. 56, № 6, p. 1111-1122.
(how to cite this article)

doi: 10.15389/agrobiology.2021.6.1099eng

UDC: 636.2:577.2

Acknowledgements:
The equipment of the Center for Biological Resources and Bioengineering of Agricultural Animals (Ernst Federal Research Center for Animal Husbandry) was used.

Supported financially by the Russian Science Foundation (No. 21-66-00007)

 

WHOLE GENOME STUDY OF SINGLE NUCLEOTIDE POLYMORPHISMS’ ASSOCIATIONS WITH WITHERS HEIGHT IN LOCAL AND TRANSBOUNDARY BREEDS IN RUSSIA

A.S. Abdelmanova ✉, M.S. Fornara, N.V. Bardukov, A.A. Sermyagin,
A.V. Dotsev, N.A. Zinovieva

Ernst Federal Science Center for Animal Husbandry, 60, pos. Dubrovitsy, Podolsk District, Moscow Province, 142132 Russia, e-mail preevetic@mail.ru (✉ corresponding author), margaretfornara@gmail.com, bardukv-nikolajj@mail.ru, alex_sermyagin85@mail.ru, asnd@mail.ru, n_zinovieva@mail.ru

ORCID:
Abdelmanova A.S. orcid.org/0000-0003-4752-0727
Sermyagin A.A. orcid.org/0000-0002-1799-6014
Fornara M.S. orcid.org/0000-0002-8844-177X
Dotsev A.V. orcid.org/0000-0003-3418-2511
Bardukov N.V. orcid.org/0000-0002-5497-2409
Zinovieva N.A. orcid.org/0000-0003-4017-6863

Received September 14, 2021

 

The stature of an animal is a classic quantitative trait that affects the predisposition to certain diseases and is associated with the productivity of farm animals. Currently, many quantitative trait loci (QTL) have been mapped that affect the cattle’s growth constituents, which confirms its polygenic determinism. An assessment of the frequencies of SNPs alleles associated with withers height in cattle populations bred in Russia has been carried out firstly in this work. The prevalence of alleles associated with high stature of animals in three out of four identified single nucleotide polymorphisms in Russian local breeds was revealed. The aim of the work was to identify loci that are under selection pressure and associated with body size in populations of Russian local breeds and transboundary breeds bred in the territory of the Russian Federation, belonging to different types of productivity, as well as with an unequal degree of pressure of artificial selection and distribution in the world. Thirteen cattle breeds (n = 670) subjected to our study including Angus (n = 39), Ayrshire (n = 144), Black-and-White (n = 50), Holstein (n = 184), Istoben (n = 22), Jersey (n = 32), Kalmyk (n = 27), Kholmogor (n = 26), Kyrgyz (n = 24), Mongolian (n = 26), Tagil (n = 26), Yakut (n = 29) and Yaroslavl (n = 41). Samples of blood, tissue and sperm stored in UNU “Genetic material bank of domestic and wild animal species and birds” of the Ernst Federal Research Center for Animal Husbandry were used as a source of DNA for this study. The samples were genotyped using DNA arrays GGP Bovine 150K and BovineHD BeadChip (Illumina Inc., USA) with the different density. In the course of data processing, SNPs common for the two arrays were determined and were used for further analysis. The genome-wide study of the associations of genotyping data with measurements of physical development of animals was carried out by the PLINK 1.9 program using filters (--geno 0.1), (--mind 0.2), (--maf 0.05). Height at withers for the studied breeds was obtained from the FAO database. All studied breeds were divided into groups according to the following criteria: growth (tall, short), type of productivity (dairy, meat), the degree of pressure of artificial selection (primitive, commercial) and distribution in the world (local, transboundary). Four SNPs were identified in total. Three of them were localized on chromosome 4 (ARS-BFGL-NGS-116590, Hapmap53144-ss46525999, BovineHD0400021479), and one on chromosome 14 (BovineHD1400007259). The alternative alleles in the detected SNPs significantly differ in their frequency in different groups of breeds, and also have significant positive or negative correlations with the height at the withers. The diversity and heterogeneity of the breeds presented in the study allows us to consider the identified traces of selection not as characteristic of one breed, region or type of productivity, but as for a group of breeds of the species Bos taurus taurus, the distribution of which from the center of domestication proceeded along the Danube Route. Thus, the identified SNPs can be used as genetic markers in breeding programs in order to increase the stature of animals and their productivity.

Keywords: Bos taurus, cattle, local breeds, transboundary breeds, QTL, SNP markers, DNA arrays, GWAS, PLAG1, withers’ height.

 

REFERENCES

  1. Petrova M.Yu., Chernigov Yu.V., Kuznetsova T.Sh. Vestnik OmGAU, 2019, 2(34): 120-125 (in Russ.).
  2. Goddard M., Hayes B. Mapping genes for complex traits in domestic animals and their use in breeding programmes. Nature Reviews Genetics,2009, 10: 381-391 CrossRef
  3. Sermyagin A.A., Bykova O.A., Loretts O.G., Kostyunina O.V., Zinov'eva N.A. Genomic variability assess for breeding traits in Holsteinizated Russian Black-and-White cattle using GWAS analysis and ROH patterns. Sel'skokhozyaistvennaya biologiya [Agricultural Biology], 2020, 55(2): 257-274 CrossRef
  4. Matukumalli L.K., Lawley C.T., Schnabel R.D., Taylor J.F., Allan M.F., Heaton M.P., O'Connell J., Moore S.S., Smith T.P.L., Sonstegard T.S., Van Tassell C.P. Development and characterization of a high density SNP genotyping assay for cattle. PLoS ONE, 2009, 4(4): e5350 CrossRef
  5. Pant S.D., Schenkel F.S., Verschoor C.P., You Q., Kelton D.F., Moore S.S., Karrow N.A. A principal component regression based genome wide analysis approach reveals the presence of a novel QTL on BTA7 for MAP resistance in Holstein cattle. Genomics, 2010, 95(3): 176-182 CrossRef
  6. Crispim A.C., Kelly M.J., Guimarães S.E., e Silva F.F., Fortes M.R., Wenceslau R.R., Moore S. Multi-trait GWAS and new candidate genes annotation for growth curve parameters in Brahman cattle. PLoS ONE, 2015, 10(10): e0139906 CrossRef
  7. Hoshiba H., Setoguchi K., Watanabe T., Kinoshita A., Mizoshita K., Sugimoto Y., Takasuga A. Comparison of the effects explained by variations in the bovine PLAG1 and NCAPG genes on daily body weight gain, linear skeletal measurements and carcass traits in Japanese Black steers from a progeny testing program. Animal Science Journal, 2013, 84(7): 529-534 CrossRef
  8. Snelling W.M., Allan M.F., Keele J.W., Kuehn L.A., McDaneld T., Smith T.P.L., Sonstegard T.S., Thallman R.M., Bennett G.L. Genome-wide association study of growth in crossbred beef cattle. Journal of Animal Science, 2010, 88(3): 837-848 CrossRef
  9. Bolormaa S., Hayes B.J., Savin K., Hawken R., Barendse W., Arthur P.F., Herd R.M., Goddard M.E. Genome-wide association studies for feedlot and growth traits in cattle. Journal of Animal Science, 2011, 89(6): 1684-1697 CrossRef
  10. Barendse W. Haplotype analysis improved evidence for candidate genes for intramuscular fat percentage from a genome wide association study of cattle. PLoS ONE, 2011, 6(12): e29601 CrossRef
  11. Dang C.G., Cho S.H., Sharma A., Kim H.C., Jeon G.J., Yeon S.H., Hong S.K., Park B.Y., Kang H.S., Lee S.H. Genome-wide association study for Warner-Bratzler shear force and sensory traits in Hanwoo (Korean cattle). Asian-Australasian Journal of Animal Sciences, 2014, 27(9): 1328-1335 CrossRef
  12. Wu Y., Fan H., Wang Y., Zhang L., Gao X., Chen Y., Li J., Ren H., Gao H. Genome-wide association studies using haplotypes and individual SNPs in Simmental cattle. PLoS ONE, 2014, 9(10): e109330 CrossRef
  13. Weng Z.Q., Su H.L., Saatchi M., Lee J., Thomas M.G., Dunkelberger J.R., Garrick D.J. Genome-wide association study of growth and body composition traits in Brangus beef cattle. Livestock Science, 2016, 183: 4-11 CrossRef
  14. Littlejohn M., Grala T., Sanders K., Walker C., Waghorn G., Macdonald K., Coppieters W., Georges M., Spelman R., Hillerton E., Davis S., Snell R. Genetic variation in PLAG1 associates with early life body weight and peripubertal weight and growth in Bos taurus. Animal Genetics, 2012, 43(5): 591-594 CrossRef
  15. Bolormaa S., Pryce J.E., Kemper K., Savin K., Hayes B.J., Barendse W. Zhang Y., Reich C. M., Mason B.A., Bunch R.J., Harrison B.E., Reverter A., Herd R.M., Tier B., Graser H.-U., Goddard M.E. Accuracy of prediction of genomic breeding values for residual feed intake and carcass and meat quality traits in Bos taurus, Bos indicus, and composite beef cattle. Journal of Animal Science, 2013, 91(7): 3088-3104 CrossRef
  16. Sasaki S., Ibi T., Matsuhashi T., Takeda K., Ikeda S., Sugimoto M., Sugimoto Y. Genetic variants in the upstream region of activin receptor IIA are associated with female fertility in Japanese Black cattle. BMC Genetics, 2015, 16: 123.
  17. Galton F. Regression towards mediocrity in hereditary stature. The Journal of the Anthropological Institute of Great Britain and Ireland, 1886, 15: 246-263. Available: http://www.jstor.org/stable/2841583. Accessed: 10.10.2021.
  18. Fisher R.A. The correlation between relatives on the supposition of Mendelian inheritance. Earth and Environmental Science Transactions of the Royal Society of Edinburgh, 1918, 52(2): 399-433 CrossRef 
  19. Deniskova T.E., Petrov S.N., Sermyagin A.A., Dotsev A.V., Fornara M.S., Reyer H., Wimmers K., Bagirov V.A., Brem G., Zinov'eva N.A. A search for genomic variants associated with body weight in sheep based on high density SNP genotypes analysis. Sel'skokhozyaistvennaya biologiya [Agricultural Biology], 2021, 56(2): 279-291 CrossRef
  20. Visscher P.M. , Macgregor S., Benyamin B., Zhu G., Gordon S., Medland S., Hill W.G., Hottenga J.-J., Willemsen G., Boomsma D.I., Liu Y.-Z., Deng H.-W., Montgomery G.W., Martin N.G. Genome partitioning of genetic variation for height from 11,214 sibling pairs. The American Journal of Human Genetics, 2007, 81: 1104-1110 CrossRef
  21. Ajmone-Marsan P., Garcia J.F., Lenstra J.A. On the origin of cattle: how aurochs became cattle and colonized the world. Evolutionary Anthropology, 2010, 19(4): 148-157 CrossRef
  22. Nelsen T.C., Short R.E., Urick J.J., Reynolds W.L. Heritabilities and genetic correlations of growth and reproductive measurements in Hereford bulls. Journal of Animal Science, 1986, 63(2): 409-417 CrossRef
  23. Northcutt S.L., Wilson D.E. Genetic parameter estimates and expected progeny differences for mature size in Angus cattle. Journal of Animal Science, 1993, 71(5): 1148-1153 CrossRef
  24. McClure M.C., Morsci N.S., Schnabel R.D., Kim J.W., Yao P., Rolf M.M., McKay S.D., Gregg S.J., Chapple R.H., Northcutt S.L., TaylorJ.F. A genome scan for quantitative trait loci influencing carcass, post-natal growth and reproductive traits in commercial Angus cattle. Animal Genetics, 2010, 41(6): 597-607 CrossRef
  25. Karim L., Takeda H., Lin L., Druet T., Arias J.A., Baurain D., Cambisano N., Davis S.R., Farnir F., Grisart B., Harris B.L., Keehan M.D., Littlejohn M.D., Spelman R.J., Georges M., Coppieters W. Variants modulating the expression of a chromosome domain encompassing PLAG1 influence bovine stature. Nature Genetics, 2011, 43: 405-413 CrossRef
  26. Randhawa I.A.S., Khatkar M.S., Thomson P.C., Raadsma H.W. Composite selection signals for complex traits exemplified through bovine stature using multibreed cohorts of European and African Bos taurus. G3 Genes|Genomes|Genetics, 2015, 5(7): 1391-1401 CrossRef
  27. Zimin A.V., Delcher A.L., Florea L., Kelley D.R., Schatz M.C., Puiu D., Hanrahan F., Pertea G., Van Tassell C.P., Sonstegard T.S., Marçais G., Roberts M., Subramanian P., Yorke J.A., Salzberg S.L. A whole-genome assembly of the domestic cow, Bos taurus. Genome Biology, 2009, 10: R42 CrossRef
  28. 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): 433-450 CrossRef
  29. Kas K., Voz M.L., Röijer E., Åström A.K., Meyen E., Stenman G., Van de Ven W.J. Promoter swapping between the genes for a novel zinc finger protein and β-catenin in pleiomorphic adenomas with t(3;8)(p21;q12) translocations. Nature Genetics, 1997, 15: 170-174 CrossRef
  30. Wood A., Esko T., Yang J. et al. Defining the role of common variation in the genomic and biological architecture of adult human height. Nature Genetics, 2014, 46: 1173-1186 CrossRef
  31. Pryce J.E., Hayes B.J., Bolormaa S., Goddard M.E. Polymorphic regions affecting human height also control stature in cattle. Genetics, 2011, 187(3): 981-984 CrossRef
  32. Fortes M.R.S., Kemper K., Sasazaki S., Reverter A., Pryce J.E., Barendse W., Bunch R., McCulloch R., Harrison B., Bolormaa S., Zhang Y.D., Hawken R.J., Goddard M.E., Lehnert S.A. Evidence for pleiotropism and recent selection in the PLAG1 region in Australian Beef cattle. Animal Genetics, 2013, 44: 636-647 CrossRef
  33. Pausch H., Flisikowski K., Jung S., Emmerling R., Edel C., Götz K.U., Fries R. Genome-wide association study identifies two major loci affecting calving ease and growth-related traits in cattle. Genetics, 2011, 187(1): 289-297 CrossRef
  34. Nishimura S., Watanabe T., Mizoshita K., Tatsuda K., Fujita T., Watanabe N., Sugimoto Y., Takasuga A. Genome-wide association study identified three major QTL for carcass weight including the PLAG1-CHCHD7 QTN for stature in Japanese Black cattle. BMC Genetics, 2012, 13: 40 CrossRef
  35. Utsunomiya Y.T., Do Carmo A.S., Carvalheiro R., Neves H.H., Matos M.C., Zavarez L.B., Pérez O’Brien A.M., Sölkner J., McEwan J.C, Cole J.B., Van Tassell C.P., Schenkel F.S., da Silva M.V.G.B., Porto Neto L.R., Sonstegard T.S., Garcia J.F. Genome-wide association study for birth weight in Nellore cattle points to previously described orthologous genes affecting human and bovine height. BMC Genetics, 2013, 14: 52 CrossRef
  36. Zhong J.-L., Xu J.-W., Wang J., Wen Y.-F., Niu H., Zheng L., He H., Peng K., He P., Shi S.Y., Huang Y.-Q., Lei C.-Z., Dang R.-H., Lan X.-Y., Qi X.-L., Chen H., Huang Y.-Z. A novel SNP of PLAG1 gene and its association with growth traits in Chinese cattle. Gene, 2019, 689: 166-171 CrossRef
  37. Abdelmanova A.S., Kharzinova V.R., Volkova V.V., Mishina A.I., Dotsev A.V., Sermyagin A.A., Boronetskaya O.I., Petrikeeva L.V., Chinarov R.Y., Brem G., Zinovieva N.A. Genetic diversity of historical and modern populations of russian cattle breeds revealed by microsatellite analysis. Genes, 2020, 11(8): 940 CrossRef
  38. Abdelmanova A.S., Kharzinova V.R., Volkova V.V., Dotsev A.V., Sermyagin A.A., Chinarov R.Y., Zinovieva N.A., Boronetskaya O.I., Lutshikhina E.M., Sölkner J., Brem G. Comparative study of the genetic diversity of local steppe cattle breeds from Russia, Kazakhstan and Kyrgyzstan by microsatellite analysis of museum and modern samples. Diversity, 2021, 13(8): 351 CrossRef
  39. Zinov'eva N.A., Sermyagin A.A., Dotsev A.V., Boronetskaya O.I., Petrikeeva L.V., Abdel'manova A.S., Brem G. Animal genetic resources: developing the research of allele pool of Russian cattle breeds — minireview. Sel'skokhozyaistvennaya biologiya [Agricultural Biology], 2019, 54(4): 631-641 CrossRef
  40. 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. Whole-genome SNP analysis elucidates the genetic structure of Russian cattle and its relationship with Eurasian taurine breeds. Genetics Selection Evolution, 2018, 50(1): 37 CrossRef
  41. Chang C.C., Chow C.C., Tellier L.C., Vattikuti S., Purcell S.M., Lee J.J. Second-generation PLINK: rising to the challenge of larger and richer datasets. GigaScience, 2015, 4(1): s13742-015-0047-8 CrossRef
  42. Zinovieva N.A., Dotsev A.V., Sermyagin A.A., Deniskova T.E., Abdelmanova A.S., Kharzinova V.R., Sölkner J., Reyer H., Wimmers K., Brem G. Selection signatures in two oldest Russian native cattle breeds revealed using high-density single nucleotide polymorphism analysis. PLoS ONE, 2020, 15(11): e0242200 CrossRef
  43. Pryce J.E., Arias J., Bowman P.J., Davis S.R., Macdonald K.A., Waghorn G.C., Wales W.J., Williams Y.J., Spelman R.J., Hayes B.J. Accuracy of genomic predictions of residual feed intake and 250-day body weight in growing heifers using 625,000 single nucleotide polymorphism markers. Journal of Dairy Science, 2012, 95(4): 2108-2119 CrossRef
  44. de Las Heras-Saldana S., Clark S.A., Duijvesteijn N., Gondro C., van der Werf J.H.J., Chen Y. Combining information from genome-wide association and multi-tissue gene expression studies to elucidate factors underlying genetic variation for residual feed intake in Australian Angus cattle. BMC Genomics, 2019, 20(1): 939 CrossRef
  45. Cheruiyot E.K., Bett R.C., Amimo J.O., Zhang Y., Mrode R., Mujibi F.D.N. Signatures of Selection in admixed dairy cattle in Tanzania. Frontiers in Genetics, 2018, 9: 607 CrossRef
  46. Taye M., Yoon J., Dessie T., Cho S., Oh S.J., Lee H.K., Kim H. Deciphering signature of selection affecting beef quality traits in Angus cattle. Genes & Genomics, 2018, 40(1): 63-75 CrossRef
  47. Lee S.H., Zhu C., Peng Y., Johnson D. T., Lehmann L., Sun Z. Identification of a novel role of ZMIZ2 protein in regulating the activity of the Wnt/β-catenin signaling pathway. The Journal of biological chemistry, 2013, 288(50): 35913-35924 CrossRef
  48. Sanchez M.-P., Ramayo-Caldas Y., Wolf V, Laithier C., El Jabri M., Michenet A., Boussaha M., Taussat S., Fritz S., Delacroix-Buchet A., Brochard M., Boichard D. Sequence-based GWAS, network and pathway analyses reveal genes co-associated with milk cheese-making properties and milk composition in Montbéliarde cows. Genetics Selection Evolution, 2019, 51: 34 CrossRef
  49. Sanchez M.P., Govignon-Gion A., Croiseau P., Fritz S., Hozé C., Miranda G., Martin P., Barbat-Leterrier A., Letaïef R., Rocha D., Brochard M., Boussaha M., Boichard D. Within-breed and multi-breed GWAS on imputed whole-genome sequence variants reveal candidate mutations affecting milk protein composition in dairy cattle. Genetics Selection Evolution, 2017, 49(1): 68 CrossRef
  50. Huo N., Yu M., Li X., Zhou C., Jin X., Gao X. PURB is a positive regulator of amino acid-induced milk synthesis in bovine mammary epithelial cells. Journal of Cellular Physiology, 2019, 234(5): 6992-7003 CrossRef
  51. Lu D., Miller S., Sargolzaei M., Kelly M., Vander Voort G., Caldwell T., Wang Z., Plastow G., Moore S. Genome-wide association analyses for growth and feed efficiency traits in beef cattle. Journal of Animal Science, 2013, 91(8): 3612-3633 CrossRef
  52. Ghoreishifar S.M., Eriksson S., Johansson A.M., Khansefid M., Moghaddaszadeh-Ahrabi S., Parna N., Davoudi P., Javanmard A. Signatures of selection reveal candidate genes involved in economic traits and cold acclimation in five Swedish cattle breeds. Genetics Selection Evolution, 2020, 52(1): 52 CrossRef
  53. Setoguchi K., Furuta M., Hirano T., Nagao T., Watanabe T., Sugimoto Y., Takasuga A. Cross-breed comparisons identified a critical 591-kb region for bovine carcass weight QTL (CW-2) on chromosome 6 and the Ile-442-Met substitution in NCAPG as a positional candidate. BMC Genetics, 2009, 10: 43 CrossRef
  54. Vanvanhossou S., Scheper C., Dossa L.H., Yin T., Brügemann K., König S. A multi-breed GWAS for morphometric traits in four Beninese indigenous cattle breeds reveals loci associated with conformation, carcass and adaptive traits. BMC Genomics, 2020, 21(1): 783 CrossRef
  55. Bouwman A.C., Daetwyler H.D., Chamberlain A.J., Ponce C.H., Sargolzaei M., Schenkel F.S., Sahana G., Govignon-Gion A., Boitard S., Dolezal M., Pausch H., Brøndum R.F., Bowman P.J., Thomsen B., Guldbrandtsen B., Lund M.S., Servin B., Garrick D.J., Reecy J., Vilkki J., Bagnato A., Wang M., Hoff J.L., Schnabel R.D., Taylor J.F., Vinkhuyzen A.A.E., Panitz F., Bendixen C., Holm L.E., Gredler B., Hozé C., Boussaha M., Sanchez M.P., Rocha D., Capitan A., Tribout T., Barbat A., Croiseau P., Drögemüller C., Jagannathan V., Vander Jagt C., Crowley J.J., Bieber A., Purfield D.C., Berry D.P., Emmerling R., Götz K.U., Frischknecht M., Russ I., Sölkner J., Van Tassell C.P., Fries R., Stothard P., Veerkamp R.F., Boichard D., Goddard M.E., Hayes B.J. Meta-analysis of genome-wide association studies for cattle stature identifies common genes that regulate body size in mammals. Nature Genetics, 2018, 50: 362-367 CrossRef
  56. Doyle J.L., Berry D.P., Veerkamp R.F., Carthy T.R., Walsh S.W., Evans R.D., Purfield D.C. Genomic regions associated with skeletal type traits in beef and dairy cattle are common to regions associated with carcass traits, feed intake and calving difficulty. Frontiers in Genetics, 2020, 11: 20 CrossRef
  57. An B., Xu L., Xia J., Wang X., Miao J., Chang T., Song M., Ni J., Xu L., Zhang L., Li J., Gao H. Multiple association analysis of loci and candidate genes that regulate body size at three growth stages in Simmental beef cattle. BMC Genetics, 2020 21(1): 32 CrossRef
  58. Hou J., Qu K., Jia P., Hanif Q., Zhang J., Chen N., Dang R., Chen H., Huang B., Lei C. A SNP in PLAG1 is associated with body height trait in Chinese cattle. Animal Genetics, 51(1): 87-90 CrossRef

 

back

 


CONTENTS

 

 

Full article PDF (Rus)

Full article PDF (Eng)