Abstract
The aim of the present study was to assess genetic variation that is characteristic for Sudanese goat breeds in the milk whey protein genes (LALBA and BLG). Four Sudanese goat breeds were screened for variability in LALBA and BLG genes at the DNA level by comparative sequencing of five animals per breed. Sixteen SNPs were identified in LALBA: seven in the upstream region, six synonymous, and three in the 3´-UTR. Three novel synonymous SNPs in exon 2 (ss5197800003, ss5197800012, and ss5197800004) were found in Nubian, Desert, and Nilotic, but not in Taggar goats. One SNP in the promoter of LALBA (rs642745519) modifies a predicted transcription factor binding site for Tcfe2a. The SNPs in the 3'-UTR (rs657915405, rs641559728, and rs664225585) affect predicted miRNA target sites. With respect to haplotypes in the exonic region, haplotype LALBA-A is most frequent in Nubian, Desert, and Nilotic goats, while haplotype LALBA-D is prevalent in Taggar goats. In BLG, 30 SNPs were detected: eight in the upstream gene region, two synonymous, 17 intronic, and three in the 3'-UTR. Among the 30 identified SNPs, 15 were novel. Four of these novel SNPs were located in the upstream gene region, one was synonymous, and ten were intronic. The novel synonymous SNP (ss5197800017), located in exon 2, was only found in Nubian and Nilotic goats. The SNPs ss5197800010 and rs635615192 in the promoter are located in predicted binding sites of transcription factors (M6097, Elk3, Elf5, and GABPA). Among seven haplotypes detected in the coding region, haplotype BLG-A is most frequent in Nubian and Nilotic goats while haplotype BLG-B is most frequent in Desert and Taggar goats. The high variability in regulatory gene regions among Sudanese goats could potentially affect the quality and yield of whey proteins in goat milk and provide a wide resource for genetic improvement of milk production and milk technology characteristics.
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References
Acton, Q.A., 2013. Dietary Proteins-Advances in Research and Application, (ScholarlyBrief, Atlanta, Georgia)
Ağaoğlu, Ö.K., Saatci, M., Elmaz, O., Çolak, M., Kocamüftüoğlu, M., and Zeytünlü, E., 2014. Mva I PCR-RFLP identifies single nucleotide polymorphism of the alpha-lactalbumin gene in some goat breeds reared in Turkey, Turkish Journal of Veterinary and Animal Sciences, 38, 225-229
Agudelo, D., Nafisi, S., and Tajmir-Riahi, H.-A., 2013. Encapsulation of milk β-lactoglobulin by chitosan nanoparticles, The Journal of Physical Chemistry B, 117, 6403-6409
Ariyarathne, H.B.P.C., Ariyaratne, H.B.S., and Lokugalappatti, L.G.S., 2017. Single nucleotide polymorphism of candidate genes in non-descript local goats of Sri Lanka, Livestock Science, 196, 49-54
Aschaffenburg, R., and Drewry, J., 1955. Occurrence of different beta-lactoglobulins in cow's milk, Nature, 176, 218-219
Ballester, M., Sánchez, A., and Folch, J.M., 2005. Polymorphisms in the goat β-lactoglobulin gene, Journal of Dairy Research, 72, 379-384
Barbiroli, A., Rasmussen, P., Beringhelli, T., Scanu, S., Ferranti, P., and Lametti, S., 2008. Investigating the drug stabilizing ability of Beta-lactoglobulin. 53rd National meeting of Italian society of biochemistry and molecular biology and National meeting of chemistry of biological systems, 2008, (Frienze University press, Italy), 15.17
Betel, D., Wilson, M., Gabow, A., Marks, D.S., and Sander, C., 2008. The microRNA.org resource: targets and expression, Nucleic Acids Res, 36, D149-153
Bevilacqua, C., Ferranti, P., Garro, G., Veltri, C., Lagonigro, R., Leroux, C., Pietrola, E., Addeo, F., Pilla, F., Chianese, L., and Martin, P., 2002. Interallelic recombination is probably responsible for the occurrence of a new alpha(s1)-casein variant found in the goat species, Eur J Biochem, 269, 1293-1303
Bickhart, D.M., Rosen, B.D., Koren, S., Sayre, B.L., Hastie, A.R., Chan, S., Lee, J., Lam, E.T., Liachko, I., Sullivan, S.T., Burton, J.N., Huson, H.J., Nystrom, J.C., Kelley, C.M., Hutchison, J.L., Zhou, Y., Sun, J., Crisa, A., Ponce de Leon, F.A., Schwartz, J.C., Hammond, J.A., Waldbieser, G.C., Schroeder, S.G., Liu, G.E., Dunham, M.J., Shendure, J., Sonstegard, T.S., Phillippy, A.M., Van Tassell, C.P., and Smith, T.P., 2017. Single-molecule sequencing and chromatin conformation capture enable de novo reference assembly of the domestic goat genome, Nat Genet, 49, 643-650
Bleck, G.T., and Bremel, R.D., 1993. Correlation of the alpha-lactalbumin (+15) polymorphism to milk production and milk composition of Holsteins, J Dairy Sci, 76, 2292-2298
Braunschweig, M.H., and Leeb, T., 2006. Aberrant low expression level of bovine beta-lactoglobulin is associated with a C to A transversion in the BLG promoter region, J Dairy Sci, 89, 4414-4419
Brew, K., 2011. Milk Proteins | α-Lactalbumin. In: John W. Fuquay, Paul L. H. McSweeney and P.F. Fox (eds), Encyclopedia of Dairy Sciences, 2 edition, Academic Press, Oxford, 780-786
Bushara, I., and Abu Nikhaila, M.M.A.A., 2012. Productivity Performance of Taggar Female Kids under Grazing Condition, J. Anim. Prod. Adv., 2, 74-79
Cannas, A., and Francescon, G.P.A.H.D., 2008. Dairy Goats Feeding and Nutrition, (CAB, UK)
Caroli, A.M., Chessa, S., and Erhardt, G.J., 2009. Invited review: milk protein polymorphisms in cattle: effect on animal breeding and human nutrition, J Dairy Sci, 92, 5335-5352
Chaneton, L., Perez Saez, J.M., and Bussmann, L.E., 2011. Antimicrobial activity of bovine beta-lactoglobulin against mastitis-causing bacteria, J Dairy Sci, 94, 138-145
Chianese, L., Portolano B, Troncone E, Pizzolongo F, Ferranti P, Addeo F, Alicata ML, Pilla F, and Calagna, G., 2000. The quality of Girgentana goat milk. Proceedings of the Proc VII Int Conf Goats, Tours, France, 2000, 946–949
Cosenza, G., Gallo, D., Illario, R., di Gregorio, P., Senese, C., Ferrara, L., and Ramunno, L., 2003. A Mval PCR-RFLP detecting a silent allele at the goat alpha-lactalbumin locus, J Dairy Res, 70, 355-357
Cui, Y., Cao, Y., Ma, Y., Qu, X., and Dong, A., 2012. Genetic variation in the Beta-lactoglobulin of Chinese yak (Bos grunniens), J Genet, 91, e44-48
Dettori, M.L., Pazzola, M., Paschino, P., Pira, M.G., and Vacca, G.M., 2015a. Variability of the caprine whey protein genes and their association with milk yield, composition and renneting properties in the Sarda breed. 1. The LALBA gene J Dairy Res, 82, 434-441
Dettori, M.L., Pazzola, M., Pira, E., Puggioni, O., and Vacca, G.M., 2015b. Variability of the caprine whey protein genes and their association with milk yield, composition and renneting properties in the Sarda breed: 2. The BLG gene. J Dairy Res, 82, 442-448
El-Hanafy, A.A.-E.M., Qureshi, M.I., Sabir, J.S.M., Mutwakil, M., Ramadan, H.A.-M.I., El-Ashmaoui, H., Abou-Alsoud, M., and Ahmed, M.M.M., 2016. Allele mining in the caprine alpha-lactalbumin (LALBA) gene of native Saudi origin, Biotechnology & Biotechnological Equipment, 30, 1115-1121
El-Hanafy, A.A., El-Saadani, M.A., Eissa, M., Maharem, G.M., and Khalifa, Z.A., 2010. Polymorphism of β-lactoglobulin gene in Barki and Damascus and their cross bred goats in relation to milk yield, Biotechnology in Animal Husbandry, 26, 1-12
FAO, 2011. Molecular Genetic Characterization of Animal Genetic Resources, (Rome, Italy)
Flower, D.R., 1996. The lipocalin protein family: structure and function, Biochem J, 318 ( Pt 1), 1-14
Fox, P.F., McSweeney, P.L.H., Cogan, T.M., and Guinee, T.P., 2000. Fundamentals of Cheese Science, (Springer Science & Business Media, 2000, Gaithersburg, Maryland)
Graziano, M., D’Andrea, M., Angiolillo, A., Lagonigro, R., and Pilla, F., 2003. A new polymorphism in goat β -lactoglobulin promoter region, Italian Journal of Animal Science, 1, 65–68
Hanafy, A.A.M.E., Qureshi, M.I., Sabir, J., Mutawakil, M., Ahmed, M.M.M., Ashmaoui, H.E., Ramadan, H.A.M.I., Abou-Alsoud, M., and Sadek, M.A., 2015. Nucleotide sequencing and DNA polymorphism studies of Beta-lactoglobulin gene in native Saudi goat breeds in relation to milk yield. zech J Anim. Sci., 60, 132-138
Hayes, H.C., and Petit, E.J., 1993. Mapping of the beta-lactoglobulin gene and of an immunoglobulin M heavy chain-like sequence to homoeologous cattle, sheep, and goat chromosomes, Mamm Genome, 4, 207-210
Ismail, A.M., Yousif, I.A., and Fadlelmoula, A.A., 2011. Phenotypic variations in birth and body weights of the Sudanese Desert goats., Livestock Research for Rural Development., 23
Kontopidis, G., Holt, C., and Sawyer, L., 2004. Invited review: beta-lactoglobulin: binding properties, structure, and function, J Dairy Sci, 87, 785-796
Korhonen, H.J., 2011. Bioactive milk proteins, peptides and lipids and other functional components derived from milk and bovine colostrum. In: M. Saarela (ed), Functional Foods: Concept to Product, 2011, (Elsevier, 2011, Cambridge, UK), 672 pages
Kumar, A., Rout, P.K., and Roy, R., 2006. Polymorphism of β-lacto globulin gene in Indian goats and its effect on milk yield, Journal of Applied Genetics, 47, 49-53
Kumar, P., Rout, P.K., Shukla, R.N., Mandal, A., and Roy, R., 2002. Genetics of milk protein variants in different Indian goats. Proceedings of the 10th Int. Cong. Asian-Aust. Assoc. Anim. Prod. Soc. (AAAP), India, 2002, pp.168
Lan, X.Y., Chen, H., Tian, Z.Q., Liu, S.Q., Zhang, Y.B., Wang, X., and Fang, X.T., 2008. Correlations between SNP of LALBA gene and economic traits in Inner Mongolian white cashmere goat, Yi Chuan, 30, 169-174
Lan, X.Y., Pan, C.Y., Chen, H., Zhang, C.L., Zhang, A.L., Zhang, L., Li, J.Y., and Lei, C.Z., 2007. An Msp I PCR-RFLP detecting a single nucleotide polymorphism at alpha-lactalbumin gene in goat Czech J. Anim. Sci., 52, 138–142
Layman, D.K., Lonnerdal, B., and Fernstrom, J.D., 2018. Applications for alpha-lactalbumin in human nutrition, Nutr Rev, 76, 444-460
Lozinsky, E., Iametti, S., Barbiroli, A., Likhtenshtein, G.I., Kálai, T., Hideg, K., and Bonomi, F., 2006. Structural features of transiently modified beta-lactoglobulin relevant to the stable binding of large hydrophobic molecules, The Protein Journal, 25, 1-15
Macha, J., 1970. Protein Polymorphism in goats’ milk., Zivocisna ́Vy ́roba, 15, 801–805
Mahmood, A., and Usman, S., 2010. A Comparative study on the physicochemical parameters of milk samples collected from buffalo, cow, goat and sheep of Gujrat, Pakistan, Pakistan Journal of Nutrition, 9, 1192-1197
Marshall, K., 2004. Therapeutic applications of whey protein, Altern Med Rev, 9, 136-156
Moioli, B., Pilla, F., and Tripaldi, C., 1998. Detection of milk protein genetic polymorphisms in order to improve dairy traits in sheep and goats: a review, Small Ruminant Research, 27, 185-195
Ng-Kwai-Hang, K.F., and Grosclaude, F., 1992. Genetic Polymorphism of Milk Proteins. In: P.F. Fox and P.L.H. McSweeney (eds), Advanced Dairy Chemistry—1 Proteins, 1992, (Springer, Boston), 739-816
O'Mahony, J.A., and Fox, P.F., 2014. Milk: An Overview In: M. Boland, H. Singh and A. Thompson (eds), Milk Proteins: From Expression to Food. (Academic Press London ),
Oftedal, O.T., 2012. The evolution of milk secretion and its ancient origins, Animal, 6, 355-368
Osman, M., Nadia, J., Ghada, H., and Rahman, A., 2008. Susceptibility of Sudanese Nubian goats, Nilotic dwarf goats and Garag ewes to experimental infection with a mechanically transmitted Trypanosoma vivax stock. , Pak J Biol Sci., 11, 472–475
Ouwehand, A.C., Salminen, S.J., Skurnik, M., and Conway, P.L., 1997. Inhibition of pathogen adhesion by β-lactoglobulin, International Dairy Journal, 7, 685-692
Ozdemir, M., Kopuzlu, S., Topal, M., and Bilgin, O.C., 2018. Relationships between milk protein polymorphisms and production traits in cattle: a systematic review and meta-analysis, Arch. Anim. Breed, 61, 197-206
Pena, R.N., Sanchez, A., and Folch, J.M., 2000. Characterization of genetic polymorphism in the goat beta-lactoglobulin gene, J Dairy Res, 67, 217-224
Perez, M.D., Sanchez, L., Aranda, P., Ena, J.M., Oria, R., and Calvo, M., 1992. Effect of beta-lactoglobulin on the activity of pregastric lipase. A possible role for this protein in ruminant milk. Biochim Biophys Acta, 1123, 151-155
Permyakov, E.A., and Berliner, L.J., 2000. alpha-Lactalbumin: structure and function, FEBS Lett, 473, 269-274
Rahmatalla, S.A., Arends, D., Reissmann, M., Ahmed, A.S., Wimmers, K., Reyer, H., and Brockmann, G.A., 2017. Whole genome population genetics analysis of Sudanese goats identifies regions harboring genes associated with major traits, BMC Genetics, 18, 92
Sardina, M.T., Rosa, A.J.M., Davoli, R., Braglia, S., and Portolano, B.J.M.B.R., 2012. Polymorphisms of beta-lactoglobulin promoter region in three Sicilian goat breeds, 39, 3203-3210
Shannon, P., and Richards, M., 2017. MotifDb: An annotated collection of protein-DNA binding sequence motifs. R package version 1.20.0, 2017,
Steele, M., 1996. The Tropical Agriculturalist: Goats, (Macmillan Press Ltd., Basingstoke, UK)
Sun, D.-W., 2012. Thermal Food Processing: New Technologies and Quality Issues, Second Edition, (France)
Tetens, J.L., Qanbari, S., Drogemuller, C., Pimentel, E.C., Bennewitz, J., Thaller, G., and Tetens, J., 2014. Bos indicus introgression into (peri-)alpine cattle breeds - evidence from the analysis of bovine whey protein variants, Anim Genet, 45, 585-588
Untergasser, A., Cutcutache, I., Koressaar, T., Ye, J., Faircloth, B.C., Remm, M., and Rozen, S.G., 2012. Primer3--new capabilities and interfaces, Nucleic Acids Res, 40, e115
Ushida, Y., Shimokawa, Y., Toida, T., Matsui, H., and Takase, M., 2007. Bovine alpha-lactalbumin stimulates mucus metabolism in gastric mucosa, J Dairy Sci, 90, 541-546
Vargas-Bello-Perez, E., Marquez-Hernandez, R.I., and Hernandez-Castellano, L.E., 2019. Bioactive peptides from milk: animal determinants and their implications in human health, J Dairy Res, 86, 136-144
Vilotte, J.L., 2002. Lowering the milk lactose content in vivo: potential interests, strategies and physiological consequences, Reprod Nutr Dev, 42, 127-132
Walzem, R.L., Dillard, C.J., and German, J.B., 2002. Whey components: millennia of evolution create functionalities for mammalian nutrition: what we know and what we may be overlooking, Crit Rev Food Sci Nutr, 42, 353-375
Wilson, T., 1991. Small ruminant production and the small ruminant genetic resource in tropical Africa, FAO Animal Production and Health Paper, 88
Yahyaoui, M.H., Pena, R.N., Sánchez, A., and Folch, J.M., 2000. Rapid communication: polymorphism in the goat β-lactoglobulin proximal promoter region1, Journal of Animal Science, 78, 1100-1101
Yang, F., Li, L., Liu, H., Cai, Y., and Wang, G., 2012. Polymorphism in the exon 4 of beta-lactoglobulin variant B precursor gene and its association with milk traits and protein structure in Chinese Holstein, Mol Biol Rep, 39, 3957-3964
Zidi, A., Casas, E., Amills, M., Jordana, J., Carrizosa, J., Urrutia, B., and Serradilla, J.M., 2014. Genetic variation at the caprine lactalbumin, alpha (LALBA) gene and its association with milk lactose concentration, Anim Genet, 45, 612-613
Zimet, P., and Livney, Y.D., 2009. Beta-lactoglobulin and its nanocomplexes with pectin as vehicles for ω-3 polyunsaturated fatty acids, Food Hydrocolloids, 23, 1120-1126
Acknowledgments
The authors thank the goat owners in Sudan, the management staff of the Goat Research Stations Wad Medani, Kuku and Dongola, as well as the farms of Bahri and the Sudan University for providing goat samples.
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SR and this study were funded by Georg Foster Research Fellowship provided by Alexander von Humboldt Foundation, Germany.
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Rahmatalla, S.A., Arends, D., Ahmed, A.S. et al. Whey protein polymorphisms in Sudanese goat breeds. Trop Anim Health Prod 52, 1211–1222 (2020). https://doi.org/10.1007/s11250-019-02119-2
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DOI: https://doi.org/10.1007/s11250-019-02119-2