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Association of SNP variants of MHC Class II DRB gene with thermo-physiological traits in tropical goats

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Abstract

Host defense in vertebrates depend on many secreted regulatory proteins such as major histocompatibility complex (MHC) class II which provide important regulatory and effector functions of T cells. Gene polymorphism in the second exon of Capra-DRB gene in three major Nigerian goat breeds [West African Dwarf (WAD), Red Sokoto (RS), and Sahel (SH)] was analyzed by restriction fragment length polymorphisms (RFLP). Four restriction enzymes, BsaHI, AluI, HaeIII, and SacII, were utilized. The association between the polymorphic sites and some heat tolerance traits were also investigated in a total of 70 WAD, 90 RS, and 50 SH goats. Fourteen different types of alleles identified in the Nigerian goats, four of which were found in the peptide coding region (A57G, Q89R, G104D, and T112I), indicate a high degree of polymorphism at the DRB locus in this species. An obvious excess (P < 0.01) of non-synonymous substitutions than synonymous (dN/dS) in this locus is a reflection of adaptive evolution and positive selection. The phylogenetic trees revealed largely species-wise clustering in DRB gene. BsaHI, AluI, HaeIII, and SacII genotype frequencies were in Hardy-Weinberg equilibrium (P > 0.05), except AluI in RS goats and HaeIII in WAD goats (P < 0.05). The expected heterozygosity (H), which is a measure of gene diversity in the goat populations, ranged from 0.16 to 0.50. Genotypes AA (BsaHI), GG, GC and CC (AluI) and GG, GA, AA (HaeIII) appeared better in terms of heat tolerance. The heat-tolerant ability of SH and RS goats to the hot and humid tropical environment of Nigeria seemed better than that of the WAD goats. Sex effect (P < 0.05) was mainly on pulse rate and heat stress index, while there were varying interaction effects on heat tolerance. Variation at the DRB locus may prove to be important in possible selection and breeding for genetic resistance to heat stress in the tropics.

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References

  • Adedeji, T.A., Ozoje, M.O., Peters, S.O., Ojedapo, L.O., Sanusi, A.O., 2011. Effect of season and sex on the body morphometrics, Heat tolerance and faecal egg counts of West African Dwarf (WAD) goats. Journal of Environmental Issues and Agriculture in Developing Countries, 3 (3), 50-57.

  • Alasaad, S., Fickel, J., Rossi, L., Sarasa, M., Benítez-Camacho, B., Granados, J.E., Soriguer, R.C., 2012. Applicability of major histocompatibility complex DRB1 alleles as markers to detect vertebrate hybridization: a case study from Iberian ibex × domestic goat in southern Spain. Acta Veterinaria Scandinavica, 54, 56 http://www.actavetscand.com/content/54/1/56.

    Article  PubMed  PubMed Central  Google Scholar 

  • Amills, M., Francino, O., Sanchez, A., 1995. Nested PCR allows the characterization of TaqI and PstI RFLPs in the second exon of the caprine MHC class II DRB gene. Veterinary Immunology and Immunopathology, 48, 313-321.

    Article  CAS  PubMed  Google Scholar 

  • Baghizadeh, A., Bahaaddini, M., Mohamadabadi, M.R., Askari, N., 2009. Allelic Variations in Exon 2 of Caprine MHC Class II DRB3 Gene in Raeini Cashmere Goat. American-Eurasian J. Agric. & Environ. Sci., 6 (4), 454-459.

  • Brinkmeyer-Langford, C.L., Cai, J.J., Gill, C.A. and Skow, L.C., 2012. Microsatellite variation in the equine MHC. Animal Genetics 44 (3), 267-275.

    Article  PubMed  Google Scholar 

  • Cappuccio, I., Pariset, L., Ajmorne-Marsan, P., Dunner, S., Cortes, O., Erhardt, G., Luhken, G., Gutscher, K., Joost, S., Nijman, I.J., Lenstra, J.A., England, P.R., Zundel, S., Obexer-Ruff, G., Beja-Pereira, A., Valentini, A., The ECOGENE CONSORTIUM 2006. Allele frequencies and diversity parameters of 27 single nucleotide polymorphisms within and across goat breeds. Molecular Ecology Notes, 6, 992–997.

    Article  CAS  Google Scholar 

  • Carrington, M., Nelson, G.W., Martin, M.P., Kissner, T., Vlahov, D., Goedert, J.J., Kaslow, R., Buchbinder, S., Hoots, K., O’Brien, S.J., 1999. HLA and HIV-1: heterozygote advantage and B*35-Cw*04 disadvantage. Science 283, 1748–1752.

    Article  CAS  PubMed  Google Scholar 

  • Das, D.N., Sri Hari, V.G., Hatkar, D.N., Rengarajan, K., Saravanan, R., Suryanarayana, V.V.S. and Murthy, L.K., 2012. Genetic diversity and population genetic analysis of bovine MHC class II DRB3.2 locus in three Bos indicus cattle breeds of Southern India. International Journal of Immunogenetics, 39, 508–517.

    Article  CAS  PubMed  Google Scholar 

  • De, S., Singh, R.K., Brahma, B., 2011. Allelic Diversity of Major Histocompatibility Complex Class II DRB Gene in Indian Cattle and Buffalo. Molecular Biology International, doi:10.4061/2011/120176.

  • De, S., Singh R.K., Butchaiah, G., 2003. MHC-DRB exon 2 allele polymorphism in Indian river buffalo (Bubalus bubalis). Animal Genetics, 33, 215-219.

    Article  Google Scholar 

  • Dikmen, S., Cole, J.B., Null, D.J., Hansen, P.J., 2013. Genome-Wide Association Mapping for Identification of Quantitative Trait Loci for Rectal Temperature during Heat Stress in Holstein Cattle. PLoS ONE, 8(7), e69202. doi:10.1371/journal.pone.0069202.

  • Dongxiao, S. and Yuan, Z., 2004. Polymorphisms of the Second Exon of MHC-DRB Gene in Chinese Local Sheep and Goat. Biochemical Genetics, 42, 385-390.

  • Downing, T., Cormican, P., O’Farrelly, C., Bradley, D.G., Lloyd, A.T., 2009. Evidence of the adaptive evolution of immune genes in chicken. BMC Research Notes, 2, 254 doi:10.1186/1756-0500-2-254.

    Article  PubMed  PubMed Central  Google Scholar 

  • Doxiadis, G.G.M., Hoof, I., de Groot, N., Bontrop, R.E., 2012. Evolution of HLA-DRB genes. Mol. Biol. Evol., 29, 3843–3853.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fadare, A.O., Peters, S.O., Yakubu, A., Sonibare, A.O., Adeleke, M.A., Ozoje, M.O., Imumorin, I.G., 2012. Physiological and haematological indices suggest superior heat tolerance of white-coloured West African Dwarf sheep in the hot humid tropics. Tropical Animal Health and Production, 45 (1), 157-165.

    Article  PubMed  Google Scholar 

  • Falconer, D.S. and Mackay, T.F.C., 1996. Introduction to quantitative genetics. 4th ed, (Harlow, England, Longman).

    Google Scholar 

  • FAO., 2012. The State of Food Insecurity in the World. Food and Agriculture Organization of the United Nations, Rome.

  • Fan, X., Lan, B., Xie, Y., Liu, Z., Zhen, G., Fu, Y., Xu, A., 2005. Single nucleotide polymorphisms in the regulatory regions of the HLA-DRB-expressed genes. Hum. Immuno., 66, 290-294.

    Article  CAS  Google Scholar 

  • FAOSTAT., 2011. Food and Agriculture Organization of the United Nations. Available at http://faostat.fao.org/default.aspx. Accessed 11 August, 2014.

  • Fontanesi L., Martelli P. L., Beretti F., Riggio V., Dall’Olio S., Colombo M., et al., 2010. An initial comparative map of copy number variations in the goat (Capra hircus) genome. BMC Genomics, 11, 639.10.1186/1471-2164-11-639.

    Article  PubMed  PubMed Central  Google Scholar 

  • Froeschke, G., Sommer, S., 2012. Insights into the complex associations between MHC Class II DRB polymorphism and multiple gastrointestinal parasite infestations in the striped mouse. PLoS ONE, 7, e31820. doi:10.1371/journal.pone.0031820.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gaudieri, S., Dawkins, R.L., Habara, K., Kulski, J.K., Gojobori, T., 2000. SNP profile within the human major histocompatibility complex reveals an extreme and interrupted level of nucleotide diversity. Genome Research, 10 (10), 1578-1586.

    Article  Google Scholar 

  • Kamath, P.L., Getz, W.M., 2011. Adaptive molecular evolution of the Major Histocompatibility Complex genes, DRA and DQA in the genus Equus. BMC Evolutionary Biology, 11:128http://www.biomedcentral.com/1471-2148/11/128.

  • Lallo, C.H.O., Paul, I., Bourne, G., 2011. Thermoregulation and performance of British Anglo-Nubian and Saanen goats reared in an intensive system in Trinidad. Tropical Animal Health and Production, 44 (3), 491-496.

    Article  PubMed  Google Scholar 

  • Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., Thompson, J.D., Gibson, T.J., Higgins, D.G., 2007. Clustal W and Clustal X version 2.0. Bioinformatics, 23 (21): 2947-2948.

    Article  CAS  PubMed  Google Scholar 

  • Lenstra, J.A., Groeneveld, L.F., Eding, H., Kantanen, J., Williams, J.L., Taberlet, P., Nicolazzi, E.L., Solkner, J., Simianer, H., Ciani, E., Garcia, J.F., Bruford, M.W., Ajmone-Marsan, P., Weigend, S., 2012. Molecular tools and analytical approaches for the characterization of farm animal genetic diversity. Animal Genetics, 43, 483–502.

    Article  CAS  PubMed  Google Scholar 

  • Li, L., Ying, Z., Yunfa, G. and QiuHong, W., 2012. Characterization of major histocompatibility complex DRA and DRB genes of the forest musk deer (Moschus berezovskii). Chinese Science Bulletin, doi: 10.1007/s11434-012-5581-5.

    Google Scholar 

  • Li, R.Y., Hui, W.Q., Jia, B., Shi, G.Q., Zhao, Z.S., Shen, H., Peng, Q., Lv, L.M., Zhou, Q.W., Li, H.T., 2011. The relationship between MHC-DRB1 gene second exon polymorphism and hydatidosis resistance of Chinese Merino (Sinkiang Junken Type), Kazakh and Duolang sheep. Parasite, 18, 163-169.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McDonald, J.H., Kreitman, M., 1991. Adaptive protein evolution at the Adh locus in Drosophila. Nature, 351, 652-654.

    Article  CAS  PubMed  Google Scholar 

  • Mehla, K., Magotra, A., Choudhary, J., Singh, A.K., Mohanty, A.K., Upadhyay, R.C., Srinivasan, S., Gupta, P., Choudhary, N., Antony, B., Khan, F., 2014. Genome-wide analysis of the heat stress response in Zebu (Sahiwal) cattle. Gene, 533 (2), 500-507.

    Article  CAS  PubMed  Google Scholar 

  • Mikko, S., Røed, K., Schmutz, S., Andersson, L., 1999. Monomorphism and polymorphism at MHC DRB loci in domestic and wild ruminants,” Immunological Reviews, 167, 169–178.

    Article  CAS  PubMed  Google Scholar 

  • Naskar, S., Deb, S.M., Niranjan, S.K., Kumar, S., Sharma, D., Sakaram, D. and Sharma, A., 2012. Molecular characterization of MHC-DRB cDNA in water buffalo (Bubalus bubalis). Genetics and Molecular Biology, 35 (1), 95-98.

    Article  PubMed  PubMed Central  Google Scholar 

  • Nikbakht, G., Rezaii, H., Stear, M.J., Talebi, M.A., Mahmoudzadeh H., 2012. Allelic polymorphism in the second exon of Ovar-DRB1 in fat-tailed sheep. Veterinary Journal 192, 547-549.

    Article  CAS  Google Scholar 

  • Oladimeji, B.S., Osinowo, O.A., Alawa, J.P., Hambolu, J.O., 1996. Estimation of average values for pulse rate, respiratory rate and rectal temperature and development of a heat stress index for adult Yankasa sheep. Bulletin of Animal Health and Production in Africa, 44, 105-107.

    Google Scholar 

  • Oliver, M.K., Piertney, S.B., 2012. Selection Maintains MHC diversity through a natural population bottleneck. Mol. Biol. Evol., 29 (7), 1713–1720.

  • Pariset, L., Cureti, A., Ligda, C., Ajmorne-Marsan, P., Valentini, A., 2009. Econogene Consortium: geographical patterning of sixteen goat breeds from Italy, Albania and Greece assessed by single nucleotide polymorphisms. BMC Ecol., 9, 20.

    Article  PubMed  PubMed Central  Google Scholar 

  • Pisoni, G., Bertoni, G., Manarolla, G., Vogt, H. R., Scaccabarozzi, L., Locatelli, C., Moroni, P., 2010. Genetic analysis of small ruminant lentiviruses following lactogenic transmission. Virology, 407, 91–99.

    Article  CAS  PubMed  Google Scholar 

  • Renord, C., Vaiman, M., 1989. Possible relationships between SLA and porcine reproduction. Reprod. Nutr. Dev., 29, 569-575.

    Article  Google Scholar 

  • Sanni, T., Gbolabo, O.O., Adefenwa, M.A., Yakubu, A., Ikeobi, C.O.N., Adebambo, A.O., Talabi, A.O., Ozoje, M.O., Wheto, M., Takeet, M.I., Peters, S.O., De Donato, M., Thomas, B. N., Imumorin, I. G. 2013. Molecular diagnosis of subclinical African Trypanosoma vivax infection and association with physiological indices and serum metabolites in extensively managed goats in the tropics. Open Journal of Veterinary Science 3, 39–45.

  • SAS., 2010. Statistical Analysis System. Base SAS® 9.2 Procedures Guide: Statistical Procedures, Third Edition. Cary, NC: SAS Institute Inc. SAS Inst., Inc., Cary, NC, USA.

  • Sheikh, F.D., Bhattacharya, T.K., Kumar, P., Sharma, A., 2009. DRB3.2 gene polymorphism and its association with pashmina production Changthangi goat. Int. J. of Immunogenet., 33, 271-276.

    Article  Google Scholar 

  • Singh, P.K., Singh, S.V., Singh, M.K., Saxena, V.K., Singh, A.V., Sohal, J.S., 2012. Genetic analysis of MHC Class 11 DRB gene in an endangered Jamunapari goat breeds. Indian Journal of Biotechnology, 11, 220-223.

    Google Scholar 

  • Sommer, S., 2005. The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Front. Zool., 2, 16.

    Article  PubMed  PubMed Central  Google Scholar 

  • Spurgin, L.G., Richardson, D.S., 2010. How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proc. R. Soc. Lond. B Biol. Sci., 277, 979–988.

    Article  CAS  Google Scholar 

  • Stear, M.J., Innocent, G.T., Buitkamp, J., 2005. The evolution and maintenance of polymorphism in the major histocompatibility complex. Veterinary Immunology and Immunopathology, 108, 53–57.

    Article  CAS  PubMed  Google Scholar 

  • Taberlet, P., Coissac, E., Pansu, J. and Pompanon, F., 2011. Conservation genetics of cattle, sheep, and goats. C.R. Biologies, 334, 247-254.

  • Takada, T., Kikkawa, Y., Yonekawa, H., Amano, T., 1998. Analysis of goat MHC class II DRA and DRB genes: identification of the expressed gene and new DRB alleles. Immunogenetics, 48, 408-412.

    Article  CAS  PubMed  Google Scholar 

  • Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., Kumar, S., 2011. MEGA5: Molecular Evolutionary Genetics Analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Molecular Biology and Evolution 28, 2731-2739.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomas, P.D., Campbell, M.J., Kejariwal, A., Mi, H., Karlak, B., Daverman, R., Diemer, K., Muruganujan, A., Narechania, A., 2003. PANTHER: A library of protein families and subfamilies indexed by function. Genome Research 13, 2129-2141.

  • Vignal, A., Milan, D., Sancristobal, M., Eggen, A., 2002. A review on SNP and other types of molecular markers and their use in animal genetics. Genet. Sel. Evol. 34, 275-305.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yakubu, A., Abimiku, H.K., Musa-Azara, I.S., Barde, R.E., Raji, A.O., 2014. Preliminary investigation of haemoglobin polymorphism and association with morphometric traits in West African Dwarf goats in north central Nigeria. Mljekarstvo, 64 (1), 57-63.

    CAS  Google Scholar 

  • Yakubu, A., Salako, A.E., De Donato, M., Takeet, M.I., Peters, S.O., Adefenwa, M.A., Okpeku, M., Wheto, M., Agaviezor, B.O., Sanni, T.M., Ajayi, O.O., Onasanya, G.O., Ekundayo, O.J., Ilori, B.M., Amusan, S.A., Imumorin, I.G., 2013. Genetic diversity in Exon 2 at the major histocompatibility complex DQB1 locus in Nigerian indigenous goats. Biochemical Genetics, 51, 954-966.

    Article  CAS  PubMed  Google Scholar 

  • Yakubu, A., Salako, A.E., and Imumorin, I.G., 2011. Comparative multivariate analysis of biometric traits of West African Dwarf and Red Sokoto goats. Tropical Animal Health and Production, 43, 561-566.

    Article  PubMed  Google Scholar 

  • Yeh, F.C., Yang, R.C., Boyle, T., Ye, Z.H., Mao, J.X., 1999. POPGENE, the user friendly software for population genetic analysis. Molecular Biology and Biotechnology Center, University of Alberta.

  • Zhao, Y., Xu, H., Shi, L., Zhang, J., 2011. Polymorphisms in Exon 2 of MHC Class II DRB3 Gene of 10 Domestic Goats in Southwest China. Asian-Australasian Journal of Animal Science, 24 (6), 752-756.

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Acknowledgements

Funding for this project was provided by the College of Agriculture & Life Sciences and Mario Einaudi Center for International Studies of Cornell University, Ithaca, NY through National Research Initiative Competitive Grant Program (Grant No. 2006-35205-16864) from the USDA National Institute of Food and Agriculture and is gratefully acknowledged. The research visit of A.Y. (ETF/DOPS/AST&D/UNIV/KEFFI/VOL.2) and M.I.T. to Cornell was made possible through the fellowships from the Nigerian Government Educational Trust Fund (ETF) now known as Tertiary Educational Trust Fund (TETFUND).

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Yakubu, A., Salako, A.E., De Donato, M. et al. Association of SNP variants of MHC Class II DRB gene with thermo-physiological traits in tropical goats. Trop Anim Health Prod 49, 323–336 (2017). https://doi.org/10.1007/s11250-016-1196-1

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