Skip to main content
SpringerLink
Log in

Milk protein polymorphisms and casein haplotypes in Butana cattle

  • Animal Genetics • Short Communication
  • Published:
Journal of Applied Genetics Aims and scope Submit manuscript

Abstract

Butana is a Bos indicus dairy cattle breed that is well adapted to the local environment of Sudan. The breed has been gradually declining in number due to breed substitution. Therefore, conservation and improvement strategies are required to maintain this breed. The aim of the present study was to assess genetic variation that is characteristic for Butana cattle in the milk protein genes CSN1S1, CSN2, CSN1S2, CSN3, LALBA, and LGB. In a first step, genomic DNA of five unrelated individuals was comparatively sequenced across all exon and flanking sequences. Ninety-three single nucleotide polymorphisms (SNPs) were identified in Butana cattle compared with the Bos taurus reference sequence at Ensembl. We confirmed the recently identified protein variants CSN2*J, CSN2*L, and LALBA*E. Fifty-two SNPs in non-coding regions are novel. Among the novel SNPs, five are located in promoter regions, three of them are in putative transcription factor binding sites (TFBSs) of the CSN1S2 promoter. Fifteen SNPs potentially affect miRNA target sites. In a second step, 50 unrelated Butana cattle were genotyped. This allowed deriving haplotypes for the casein gene cluster on BTA6. The most frequent haplotype was CSN1S1*C-CSN2*A 2 -CSN1S2*A-CSN3*A (C-A 2 -A-A, frequency 0.1546). Considering the newly identified CSN1S2 promoter variants, the most frequent haplotype was C-A 2 -TTC-A-A (0.1046), with TTC as the promoter variant. The information on protein and promoter variants can be used for the development of conservation and breeding strategies for this local breed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

References

  • Betel D, Wilson M, Gabow A, Marks DS, Sander C (2008) The microRNA.org resource: targets and expression. Nucleic Acids Res 36:D149–D153

    Article  CAS  PubMed  Google Scholar 

  • Boettcher PJ, Caroli A, Stella A, Chessa S, Budelli E, Canavesi F, Ghiroldi S, Pagnacco G (2004) Effects of casein Haplotypes on milk production traits in Italian Holstein and Brown Swiss Cattle. J Dairy Sci 87:4311–4317. doi:10.3168/jds.S0022-0302(04)73576-6

    Article  CAS  PubMed  Google Scholar 

  • Bonfatti V, Di Martino G, Cecchinato A, Degano L, Carnier P (2010a) Effects of β-κ-casein (CSN2-CSN3) haplotypes, β-lactoglobulin (BLG) genotypes, and detailed protein composition on coagulation properties of individual milk of Simmental cows. J Dairy Sci 93:3809–3817. doi:10.3168/jds.2009-2779

    Article  CAS  PubMed  Google Scholar 

  • Bonfatti V, Di Martino G, Cecchinato A, Vicario D, Carnier P (2010b) Effects of β-κ-casein (CSN2-CSN3) haplotypes and β-lactoglobulin (BLG) genotypes on milk production traits and detailed protein composition of individual milk of Simmental cows. J Dairy Sci 93:3797–3808. doi:10.3168/jds.2009-2778

    Article  CAS  PubMed  Google Scholar 

  • Bonfatti V, Cecchinato A, Di Martino G, De Marchi M, Gallo L, Carnier P (2011) Effect of κ-casein B relative content in bulk milk κ-casein on Montasio, Asiago, and Caciotta cheese yield using milk of similar protein composition. J Dairy Sci 94:602–613. doi:10.3168/jds.2010-3368

    Article  CAS  PubMed  Google Scholar 

  • Caroli A, Chessa S, Bolla P, Budelli E, Gandini GC (2004) Genetic structure of milk protein polymorphisms and effects on milk production traits in a local dairy cattle. J Anim Breed Genet 121:119–127. doi:10.1111/j.1439-0388.2003.00443.x

    Article  CAS  Google Scholar 

  • Caroli A, Chessa S, Chiatti F, Rignanese D, Meléndez B, Rizzi R, Ceriotti G (2008) Short communication: Carora cattle show high variability in alpha(s1)-casein. J Dairy Sci 91:354–359. doi:10.3168/jds.2007-0420

    Article  CAS  PubMed  Google Scholar 

  • Caroli AM, Chessa S, Erhardt GJ (2009) Invited review: milk protein polymorphisms in cattle: effect on animal breeding and human nutrition. J Dairy Sci 92:5335–5352. doi:10.3168/jds.2009-2461

    Article  CAS  PubMed  Google Scholar 

  • Caroli A, Rizzi R, Lühken G, Erhardt G (2010) Short communication: milk protein genetic variation and casein haplotype structure in the Original Pinzgauer cattle. J Dairy Sci 93:1260–1265. doi:10.3168/jds.2009-2521

    Article  CAS  PubMed  Google Scholar 

  • Celik S (2003) β-Lactoglobulin genetic variants in Brown Swiss breed and its association with compositional properties and rennet clotting time of milk. Int Dairy J 13:727–731. doi:10.1016/S0958-6946(03)00093-1

    Article  CAS  Google Scholar 

  • Ceriotti G, Marletta D, Caroli A, Erhardt G (2004) Milk protein loci polymorphism in taurine (Bos taurus) and zebu (Bos indicus) populations bred in hot climate. J Anim Breed Genet 121:404–415. doi:10.1111/j.1439-0388.2004.00471.x

    Article  CAS  Google Scholar 

  • Di Stasio L, Mariani P (2000) The role of protein polymorphism in the genetic improvement of milk production. Zootecnica e Nutrizione Animale 26:69–90

    Google Scholar 

  • Erhardt G (1996) Detection of a new k-casein variant in milk of Pinzgauer cattle. Anim Genet 27:105–108. doi:10.1111/j.1365-2052.1996.tb00477.x

    Article  CAS  PubMed  Google Scholar 

  • Erhardt G, Juszczak J, Panicke L, Krick-Saleck H (1998) Genetic polymorphism of milk proteins in Polish Red Cattle: a new genetic variant of β-lactoglobulin. J Anim Breed Genet 115:63–71. doi:10.1111/j.1439-0388.1998.tb00328.x

    Article  CAS  Google Scholar 

  • Farrell HM Jr, Jimenez-Flores R, Bleck GT, Brown EM, Butler JE, Creamer LK, Hicks CL, Hollar CM, Ng-Kwai-Hang KF, Swaisgood HE (2004) Nomenclature of the proteins of cows’ milk—sixth revision. J Dairy Sci 87:1641–1674

    Article  CAS  PubMed  Google Scholar 

  • Ferretti L, Leone P, Sgaramella V (1990) Long range restriction analysis of the bovine casein genes. Nucleic Acids Res 18:6829–6833. doi:10.1093/nar/18.23.6829

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Food and Agriculture Organization of the United Nations (FAO) (2011) Molecular genetic characterization of animal genetic resources. FAO Animal Production and Health Guidelines. No. 9. Rome

  • Gallinat JL, Qanbari S, Drögemüller C, Pimentel EC, Thaller G, Tetens J (2013) DNA-based identification of novel bovine casein gene variants. J Dairy Sci 96:699–709

    Article  CAS  PubMed  Google Scholar 

  • Griffiths-Jones S, Grocock RJ, Van Dongen S, Bateman A, Enright AJ (2006) miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res 34:D140–D144

    Article  CAS  PubMed  Google Scholar 

  • Gustavsson F, Buitenhuis AJ, Johansson M, Bertelsen HP, Glantz M, Poulsen NA, Lindmark Månsson H, Stålhammar H, Larsen LB, Bendixen C, Paulsson M, Andrén A (2014) Effects of breed and casein genetic variants on protein profile in milk from Swedish Red, Danish Holstein, and Danish Jersey cows. J Dairy Sci 97:3866–3877. doi:10.3168/jds.2013-7312

    Article  CAS  PubMed  Google Scholar 

  • Hallén E, Allmere T, Näslund J, Andrén A, Lundén A (2007) Effect of genetic polymorphism of milk proteins on rheology of chymosin-induced milk gels. Int Dairy J 17:791–799. doi:10.1016/j.idairyj.2006.09.011

    Article  Google Scholar 

  • Hayes HC, Petit EJ (1993) Mapping of the β-lactoglobulin gene and of an immunoglobulin M heavy chain-like sequence to homoeologous cattle, sheep, and goat chromosomes. Mamm Genome 4:207–210

    Article  CAS  PubMed  Google Scholar 

  • Huang W, Peñagaricano F, Ahmad KR, Lucey JA, Weigel KA, Khatib H (2012) Association between milk protein gene variants and protein composition traits in dairy cattle. J Dairy Sci 95:440–449. doi:10.3168/jds.2011-4757

    Article  CAS  PubMed  Google Scholar 

  • Ibeagha-Awemu EM, Prinzenberg E-M, Erhardt G (2005) High variability of milk protein genes in Bos indicus cattle breeds of Cameroon and Nigeria and characterization of a new αs1-casein promoter allele. J Dairy Res 72:1–9. doi:10.1017/s0022029904000445

    Article  CAS  PubMed  Google Scholar 

  • Ibeagha-Awemu EM, Prinzenberg EM, Jann OC, Lühken G, Ibeagha AE, Zhao X, Erhardt G (2007) Molecular characterization of bovine CSN1S2*B and extensive distribution of zebu-specific milk protein alleles in European cattle. J Dairy Sci 90:3522–3529. doi:10.3168/jds.2006-679

    Article  CAS  PubMed  Google Scholar 

  • Jann OC, Ibeagha-Awemu EM, Ozbeyaz C, Zaragoza P, Williams JL, Ajmone-Marsan P, Lenstra JA, Moazami-Goudarzi K, Erhardt G (2004) Geographic distribution of haplotype diversity at the bovine casein locus. Genet Sel Evol 36:243–257. doi:10.1186/1297-9686-36-2-243

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kamiński S, Cieślińska A, Kostyra E (2007) Polymorphism of bovine beta-casein and its potential effect on human health. J Appl Genet 48:189–198. doi:10.1007/BF03195213

    Article  PubMed  Google Scholar 

  • Kertesz M, Iovino N, Unnerstall U, Gaul U, Segal E (2007) The role of site accessibility in microRNA target recognition. Nat Genet 39:1278–1284

    Article  CAS  PubMed  Google Scholar 

  • Kreuzer S, Reissmann M, Brockmann GA (2013) Gene test to elucidate the ETEC F4ab/F4ac receptor status in pigs. Vet Microbiol 162:293–295. doi:10.1016/j.vetmic.2012.07.049

    Article  CAS  PubMed  Google Scholar 

  • Lisson M, Lochnit G, Erhardt G (2013) Genetic variants of bovine beta- and kappa-casein result in different immunoglobulin E-binding epitopes after in vitro gastrointestinal digestion. J Dairy Sci 96:5532–5543. doi:10.3168/jds.2013-6684

    Article  CAS  PubMed  Google Scholar 

  • Lisson M, Lochnit G, Erhardt G (2014) In vitro gastrointestinal digestion of bovine αS1- and αS2-casein variants gives rise to different IgE-binding epitopes. Int Dairy J 34:47–55. doi:10.1016/j.idairyj.2013.06.012

    Article  CAS  Google Scholar 

  • Lühken G, Caroli A, Ibeagha-Awemu EM, Erhardt G (2009) Characterization and genetic analysis of bovine αs1-casein I variant. Anim Genet 40:479–485

    Article  PubMed  Google Scholar 

  • Mancini G, Nicolazzi EL, Valentini A, Chillemi G, Ajmone Marsan P, Santus E, Pariset L (2013) Association between single nucleotide polymorphisms (SNPs) and milk production traits in Italian Brown cattle. Livest Sci 157:93–99. doi:10.1016/j.livsci.2013.07.008

    Article  Google Scholar 

  • Mir SN, Ullah O, Sheikh R (2014) Genetic polymorphism of milk protein variants and their association studies with milk yield in Sahiwal cattle. Afr J Biotechnol 13:555–565. doi:10.5897/AJB2013.13216

    Article  CAS  Google Scholar 

  • Nilsen H, Olsen HG, Hayes B, Sehested E, Svendsen M, Nome T, Meuwissen T, Lien S (2009) Casein haplotypes and their association with milk production traits in Norwegian Red cattle. Genet Sel Evol 41:24

    Article  PubMed  PubMed Central  Google Scholar 

  • Poulsen NA, Bertelsen HP, Jensen HB, Gustavsson F, Glantz M, Månsson HL, Andrén A, Paulsson M, Bendixen C, Buitenhuis AJ, Larsen LB (2013) The occurrence of noncoagulating milk and the association of bovine milk coagulation properties with genetic variants of the caseins in 3 Scandinavian dairy breeds. J Dairy Sci 96:4830–4842. doi:10.3168/jds.2012-6422

    Article  CAS  PubMed  Google Scholar 

  • Rachagani S, Gupta ID (2008) Bovine kappa-casein gene polymorphism and its association with milk production traits. Genet Mol Biol 31:893–897

    Article  CAS  Google Scholar 

  • Rachagani S, Gupta ID, Gupta N, Gupta SC (2006) Genotyping of β-lactoglobulin gene by PCR-RFLP in Sahiwal and Tharparkar cattle breeds. BMC Genet 7:31

    Article  PubMed  PubMed Central  Google Scholar 

  • Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tetens JL, Qanbari S, Drögemüller C, Pimentel EC, Bennewitz J, Thaller G, 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

    Article  CAS  PubMed  Google Scholar 

  • Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3—new capabilities and interfaces. Nucleic Acids Res 40:e115–e115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Visker MH, Heck JM, van Valenberg HJ, van Arendonk JA, Bovenhuis H (2012) Short communication: A new bovine milk–protein variant: alpha-lactalbumin variant D. J Dairy Sci 95:2165–2169. doi:10.3168/jds.2011-4794

    Article  CAS  PubMed  Google Scholar 

  • Zepeda-Batista JL, Alarcón-Zúñiga B, Ruíz-Flores A, Núñez-Domínguez R, Ramírez-Valverde R (2015) Polymorphism of three milk protein genes in Mexican Jersey cattle. Electron J Biotechnol 18:1–4. doi:10.1016/j.ejbt.2014.10.002

    Article  CAS  Google Scholar 

Download references

Acknowledgments

A. Said Ahmed was supported by the German Academic Exchange Service (DAAD) and the University of Gezira, Sudan. The authors thank the cattle owners in Sudan for providing samples from Butana cattle, as well as the management team and staff of the Atbara Research Station. We thank Ahmed M. Musa for the help in sample collection.

Author information

Authors and Affiliations

  1. Albrecht Daniel Thaer-Institute of Agricultural and Horticultural Sciences, Humboldt-Universität zu Berlin, Invalidenstrasse 42, 10115, Berlin, Germany

    A. Said Ahmed, S. Rahmatalla, R. Bortfeldt, D. Arends, M. Reissmann & G. A. Brockmann

  2. Department of Dairy Production, University of Khartoum, P.O. Box 32, Khartoum North, Sudan

    S. Rahmatalla

Authors
  1. A. Said Ahmed
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. Rahmatalla
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. R. Bortfeldt
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. D. Arends
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. Reissmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. G. A. Brockmann
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to G. A. Brockmann.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All international, national, and institutional guidelines for the care and use of animals were followed.

Additional information

Communicated by: Maciej Szydlowski

Electronic supplementary material

Below are the links to the electronic supplementary material.

Table S1

(DOC 94 kb)

Table S2

(DOC 44 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ahmed, A.S., Rahmatalla, S., Bortfeldt, R. et al. Milk protein polymorphisms and casein haplotypes in Butana cattle. J Appl Genetics 58, 261–271 (2017). https://doi.org/10.1007/s13353-016-0381-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13353-016-0381-2

Keywords

Search

Navigation