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Polymorphisms in major histocompatibility complex genes and its associations with milk quality in Murrah buffaloes

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Abstract

Animal breeding programs have used molecular genetic tools as an auxiliary method to identify and select animals with superior genetic merit for milk production and milk quality traits as well as disease resistance. Genes of the major histocompatibility complex (MHC) are important molecular markers for disease resistance that could be applied for genetic selection. The aim of this study was to identify single nucleotide polymorphisms (SNPs) and haplotypes in DRB2, DRB3, DMA, and DMB genes in Murrah breed and to analyze the association between molecular markers and milk, fat, protein and mozzarella production, fat and protein percentage, and somatic cell count. Two hundred DNA samples from Murrah buffaloes were used. The target regions of candidate genes were amplified by polymerase chain reaction (PCR) followed by sequencing and identification of polymorphisms. Allele and genotype frequencies, as well as linkage disequilibrium between SNPs, were calculated. Genotypes were used in association analyses with milk production and quality traits. Except for the DMA gene, identified as monomorphic, the other genes presented several polymorphisms. The DMB, DRB2, and DRB3 genes presented two, six, and seven SNPs, respectively. Fifty-seven haplotype blocks were constructed from 15 SNPs identified, which was used in association analyses. All the studied traits had at least one associated haplotype. In conclusion, it is suggested that the haplotypes found herein can be associated with important traits related to milk production and quality.

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References

  • Altiero, V., Moio, L. and Addeo, F., 1989. Previsione della resa in mozzarella sulla base del contenuto in grasso e proteine del latte di bufala. Scienza e Tecnica Lattiero-Casearia, 40, 425–433.

    CAS  Google Scholar 

  • Ardlie, K.G., Kruglyak, L. and Seielstad, M., 2002. Patterns of linkage disequilibrium in the human genome. Nature Reviews Genetics, 3, 299–309.

    CAS  PubMed  Google Scholar 

  • Barrett, J.C., Fry, B., Maller, J. and Daly, M.J., 2005. Haploview: Analysis and visualization of LD and haplotype maps. Bioinformatics, 21, 263–265.

    CAS  PubMed  Google Scholar 

  • Batavani, R.A., Asri, S., Naebzadeh, H., 2007. The effect of subclinical mastitis on milk composition in dairy cows. Iran Journal of Veterinary Research, 8, 205–211.

    Google Scholar 

  • Behl, J.D., Verma, N., Tyagi, N., Mishra, P., Behl, R. and Joshi, B., 2012. The major histocompatibility complex in bovines: A review. ISRN Veterinary Science, 2012, 872710.

    PubMed  PubMed Central  Google Scholar 

  • Brown, J.H., Jardetzky, T.S., Gorga, J.C., Stern, L.J., Urban, R.G., Strominger, J.L. and Wiley, D.C., 1993. Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1. Nature, 364, 33–39.

    CAS  PubMed  Google Scholar 

  • Cargill, M., Altshuler, D., Ireland, J., Sklar, P., Ardlie, K., Patil, N., Shaw, N., Lane, C.R., Lim, E.P., Kalyanaraman, N., Nemesh, J. and Ziaugra, L., 1999. Characterization of single-nucleotide polymorphisms in coding regions of human genes. Nature Genetics, 23, 373–373.

    CAS  Google Scholar 

  • Ceron-Munoz, M., Tonhati, H., Duarte, J., Oliveira, J., Munoz-Berrocal, M. and Jurado-Gamez, H., 2002. Factors affecting somatic cell counts and their relations with milk and milk constituent yield in buffaloes. Journal of Dairy Science, 85, 2885–2889.

    CAS  PubMed  Google Scholar 

  • Chamary, J.V., Parmley, J.L. and Hurst, L.D., 2006. Hearing silence: Non-neutral evolution at synonymous sites in mammals. Nature Reviews Genetics, 7, 98–108.

    CAS  PubMed  Google Scholar 

  • Dabdoub, S. and Shook, G., 1984. Phenotypic relations among milk yield, somatic cell count and clinical mastitis. Journal of Dairy Science, 67, 163–164.

    Google Scholar 

  • Dairy, U.S.D.A., 2007. Part I: Reference of Dairy Cattle Health and Management Practices in the United States. Fort Collins: USDA: APHIS: VS CEAH, National Animal Health Monitoring System. https://www.aphis.usda.gov/animal_health/nahms/dairy/downloads/dairy07/Dairy07_dr_PartI.pdf. Accessed 07 Sep 2018.

    Google Scholar 

  • De, S., Singh, R.K. and Butchaiah, G., 2002. MHC-DRB exon 2 allele polymorphism in Indian river buffalo (Bubalus bubalis). Animal Genetics, 33, 215–219.

    CAS  PubMed  Google Scholar 

  • Du, C., Deng, T., Zhou, Y., Ye, T., Zhou, Z., Zhang, S., Shao, B., Wei, P., Sun, H., Khan, F.A., Yang, L. and Hua G., 2019. Systematic analyses for candidate genes of milk production traits in water buffalo (Bubalus Bubalis). Animal Genetics, 50, 207–216.

    CAS  PubMed  Google Scholar 

  • El Nahas, S.M., El Kasas, A.H., Abou Mossallem, A.A., Abdelhamid, M.I. and Warda, M., 2017. A study on IL8RB gene polymorphism as a potential immuno-compromised adherent in exaggeration of parenteral and mammo-crine oxidative stress during mastitis in buffalo. Journal of Advanced Research, 8, 617–625.

    PubMed  PubMed Central  Google Scholar 

  • Falconer, D.S., Mackay, T.F. and Frankham, R., 1996. Introduction to quantitative genetics (4th edn), (Oliver And Boyd, Edinburgh).

    Google Scholar 

  • FAOSTAT. 2017. Food and Agriculture Organization of the United Nations. [cited 23 May 2019]. Available from URL: http://www.fao.org/faostat/en/#data/QA/visualize. Accessed 23 May 2019.

  • Fernandez, I.G., Ramirez, J.G.R., Vazquez, A.G., Arvizu, R.U. and Morales, R.A.A., 2008. Polymorphism of locus DRB3.2 in populations of creole cattle from northern Mexico. Genetics and Molecular Biology, 31, 880–886.

    CAS  Google Scholar 

  • Flint, A.P.F. and Woolliams, J.A., 2008. Precision animal breeding Philosophical transactions of the Royal Society of London. Series B, Biological Sciences, 363, 573–590.

    CAS  PubMed  Google Scholar 

  • Forsbäck, L., Lindmark-Månsson, H., Andrén, A., Åkerstedt, M., and Svennersten-Sjaunja, K., 2009. Udder quarter milk composition at different levels of somatic cell count in cow composite milk. Animal, 3, 710–717.

    PubMed  Google Scholar 

  • Gabriel, S.B., Schaffner, S.F., Nguyen, H., Moore, J.M., Roy, J., Blumenstiel, B., Higgins, J., DeFelice, M., Lochner, A., Faggart, M. and Liu-Cordero, S.N., 2002. The structure of haplotype blocks in the human genome. Science, 296, 2225–2229.

    CAS  PubMed  Google Scholar 

  • Hill, W. and Robertson, A., 1968. Linkage disequilibrium in finite populations. Theoretical and Applied Genetics, 38, 226–231.

    CAS  PubMed  Google Scholar 

  • Hill, W.G., 1981. Estimation of effective population-size from data on linkage disequilibrium. Genetical Research, 38, 209–216.

    Google Scholar 

  • Hill, W.G. and Robertson, A., 2007. The effect of linkage on limits to artificial selection. Genetical Research, 89, 311–336.

    CAS  PubMed  Google Scholar 

  • Ibrahim, E.A., Allam, N.A., Kotb, E.E., El-Rafey, G.A., El-Deen, M.M.A. and Fadlallah, M.G., 2012. Sequence-based typing-study on the relationship between subclinical mastitis and BoLA-DRB3. 2* allelic polymorphism in egyptian cows. Global Veterinaria, 9, 8–22.

    CAS  Google Scholar 

  • Jeretina, J., Škorjanc, D., and Babnik, D., 2017. A new somatic cell count index to more accurately predict milk yield losses. Archives Animal Breeding, 60, 373–383.

    Google Scholar 

  • Kumar, S., Sangwan, M.L., and Rupender, 2008. Polymorphism in DRB3 exon 2 by PCR-RFLP and its association with mastitis in Nili-Ravi breed. Indian Journal of Biotechnology, 7, 398–400.

    CAS  Google Scholar 

  • Litwinczuk, Z., Krol, J., Brodziak, A. and Barlowska, J., 2011. Changes of protein content and its fractions in bovine milk from different breeds subject to somatic cell count. Journal of Dairy Science, 94, 684–691.

    CAS  PubMed  Google Scholar 

  • Mosafer, J., Heydarpour, M., Manshad, E., Russell, G. and Sulimova, G.E., 2012. Distribution of BoLA-DRB3 allelic frequencies and identification of two new alleles in Iranian buffalo breed. The Scientific World Journal, 2012, 863024.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pasquini, M., Osimani, A., Tavoletti, S., Moreno, I., Clementi, F. and Trombetta, M. F., 2018. Trends in the quality and hygiene parameters of bulk Italian Mediterranean buffalo (Bubalus bubalis) milk: A three year study. Animal Science Journal, 89, 176–185.

    CAS  PubMed  Google Scholar 

  • Penn, D. and Ilmonen, P., 2005. Major Histocompatibility Complex (MHC). In Encyclopedia of Life Sciences (ELS). Chichester: John Wiley & Sons.

  • Purcell, S., Neale, B., Todd-Brown, K., Thomas, L., Ferreira, M.A.R., Bender, D., Maller, J., Sklar, P., de Bakker, P.I.W., Daly, M.J. and Sham, P.C., 2007. Plink: A tool set for whole-genome association and population-based linkage analyses. American Journal of Human Genetics, 81, 559–575.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ramos, T., Costa, F., Pinto, I., Pinto, S. and Abreu, L., 2015. Effect of somatic cell count on bovine milk protein fractions. Journal of Analytical & Bioanalytical Techniques, 6, 2.

    Google Scholar 

  • Ryder, L.P., Svejgaard, A. and Dausset, J., 1981. Genetics of HLA disease association. Annual Review of Genetics, 15, 169–187.

    CAS  PubMed  Google Scholar 

  • Sermyagin, A., Kovalyuk, N., Ermilov, A., Yanchukov, I., Satsuk, V., Dotsev, A., Deniskova, T., Brem, G. and Zinovieva, N., 2016. Associations of BoLA-DRB3 genotypes with breeding values for milk production traits in russian dairy cattle population. Agricultural Biology, 51, 775–781.

    Google Scholar 

  • Sambrook, J., Fritsch, E.F. and Maniatis, T., 1989. Molecular cloning: A Laboratory Manual (2nd ed). New York:Cold Spring Harbor laboratory press.

  • Stafuzza, N.B., Abbey, C.A., Gill, C.A., Womack, J.E. and Amaral, M.E.J., 2012. Construction and preliminary characterization of a river buffalo bacterial artificial chromosome library. Genetics and Molecular Research, 11, 3013–3019.

    CAS  PubMed  Google Scholar 

  • Stafuzza, N.B., Greco, A.J., Grant, J.R., Abbey, C.A., Gill, C.A., Raudsepp, T., Skow, L.C., Womack, J.E., Riggs, P.K. and Amaral, M.E.J., 2013. A high-resolution radiation hybrid map of the river buffalo major histocompatibility complex and comparison with BoLA. Animal Genetics, 44, 369–376.

    CAS  PubMed  Google Scholar 

  • Trowsdale, J., 1995. Both man and bird and beast - comparative organization of MHC genes. Immunogenetics, 41, 1–17.

    CAS  PubMed  Google Scholar 

  • Untergasser, A., Nijveen, H., Rao, X., Bisseling, T., Geurts, R. and Leunissen, J.A.M., 2007. Primer3plus, an enhanced web interface to primer3. Nucleic Acids Research, 35, W71-W74.

    PubMed  PubMed Central  Google Scholar 

  • Vaneijk, M.J.T., Stewarthaynes, J.A. and Lewin, H.A., 1992. Extensive polymorphism of the BoLA-DRB3 gene distinguished by PCR-RFLP. Animal Genetics, 23, 483–496.

    CAS  Google Scholar 

  • Van Soest, F. J., Santman-Berends, I. M., Lam, T. J., and Hogeveen, H., 2016. Failure and preventive costs of mastitis on Dutch dairy farms. Journal of dairy science, 99, 8365–8374.

    PubMed  Google Scholar 

  • Wiseman, R.W., Karl, J.A., Bohn, P.S., Nimityongskul, F.A., Starrett, G.J. and O'Connor, D.H., 2013. Haplessly hoping: Macaque major histocompatibility complex made easy. ILAR Journal, 54, 196–210.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao, X. and Lacasse, P., 2008. Mammary tissue damage during bovine mastitis: Causes and control. Journal of Animal Science, 86, 57–65.

    CAS  PubMed  Google Scholar 

  • Zinkernagel, R.M. and Doherty, P.C., 1979. MHC-restricted cytotoxic T cells: Studies on the biological role of polymorphic major transplantation antigens determining t-cell restriction-specificity, function, and responsiveness. Advances in Immunology, 27, 51–177.

    CAS  PubMed  Google Scholar 

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Acknowledgments

São Paulo Research Foundation (FAPESP) for provided the financial support (grant 2014/25309-7) to conduct the research project. ACF (grant 88881.133033/2016-01) and NBS were supported by fellowship from Coordination for the Improvement of Higher Education Personnel (CAPES grant 88881.133033/2016-01), while DJAS was supported by a fellowship from FAPESP (grant 2015/12396-1). HT received a productivity research fellowship from National Counsel of Technological and Scientific Development (CNPq).

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Authors and Affiliations

  1. Department of Animal Science, School of Agricultural and Veterinarian Sciences (FCAV), São Paulo State University (UNESP), Jaboticabal, SP, 14884-900, Brazil

    Ana C. Freitas, Marina M. D. Barbero, Daniel J. A. Santos & Humberto Tonhati

  2. Department of Exact Sciences, School of Agricultural and Veterinarian Sciences (FCAV), São Paulo State University (UNESP), Jaboticabal, SP, 14884-900, Brazil

    Nedenia B. Stafuzza

  3. School of Chemistry and Molecular Biosciences, The University of Queensland, Saint Lucia Campus, Brisbane, QLD, 4067, Australia

    Marina R. S. Fortes

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  1. Ana C. Freitas
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  2. Nedenia B. Stafuzza
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  3. Marina M. D. Barbero
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Correspondence to Ana C. Freitas.

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Freitas, A.C., Stafuzza, N.B., Barbero, M.M.D. et al. Polymorphisms in major histocompatibility complex genes and its associations with milk quality in Murrah buffaloes. Trop Anim Health Prod 52, 415–423 (2020). https://doi.org/10.1007/s11250-019-02030-w

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