Asian-Australasian Journal of Animal Sciences

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
권호 표지
DOI QR코드

DOI QR Code

Association of UDP-galactose-4-epimerase with milk protein concentration in the Chinese Holstein population

  • Li, Cong (Shaanxi Key Laboratory of Molecular Biology for Agriculture, College of Animal Science and Technology, Northwest A&F University) ;
  • Cai, Wentao (College of Animal Science and Technology, Key Laboratory of Animal Genetics and Breeding of Ministry of Agriculture, National Engineering Laboratory for Animal Breeding, China Agricultural University) ;
  • Liu, Shuli (College of Animal Science and Technology, Key Laboratory of Animal Genetics and Breeding of Ministry of Agriculture, National Engineering Laboratory for Animal Breeding, China Agricultural University) ;
  • Zhou, Chenghao (College of Animal Science and Technology, Key Laboratory of Animal Genetics and Breeding of Ministry of Agriculture, National Engineering Laboratory for Animal Breeding, China Agricultural University) ;
  • Cao, Mingyue (College of Animal Science and Technology, Key Laboratory of Animal Genetics and Breeding of Ministry of Agriculture, National Engineering Laboratory for Animal Breeding, China Agricultural University) ;
  • Yin, Hongwei (College of Animal Science and Technology, Key Laboratory of Animal Genetics and Breeding of Ministry of Agriculture, National Engineering Laboratory for Animal Breeding, China Agricultural University) ;
  • Sun, Dongxiao (College of Animal Science and Technology, Key Laboratory of Animal Genetics and Breeding of Ministry of Agriculture, National Engineering Laboratory for Animal Breeding, China Agricultural University) ;
  • Zhang, Shengli (College of Animal Science and Technology, Key Laboratory of Animal Genetics and Breeding of Ministry of Agriculture, National Engineering Laboratory for Animal Breeding, China Agricultural University) ;
  • Loor, Juan J. (Mammalian NutriPhysioGenomics, Department of Animal Sciences and Division of Nutritional Sciences, University of Illinois)
  • Received : 2019.07.08
  • Accepted : 2020.02.14
  • Published : 2020.11.01
Download PDF
⟨ Previous Next ⟩

Abstract

Objective: An initial RNA-Sequencing study revealed that UDP-galactose-4-epimerase (GALE) was one of the most promising candidates for milk protein concentration in Chinese Holstein cattle. This enzyme catalyzes the interconversion of UDP-galactose and UDP-glucose, an important step in galactose catabolism. To further validate the genetic effect of GALE on milk protein traits, genetic variations were identified, and genotypes-phenotypes associations were performed. Methods: The entire coding region and the 5'-regulatory region (5'-UTR) of GALE were re-sequenced using pooled DNA of 17 unrelated sires. Association studies for five milk production traits were performed using a mixed linear animal model with a population encompassing 1,027 Chinese Holstein cows. Results: A total of three variants in GALE were identified, including two novel variants (g.2114 A>G and g.2037 G>A) in the 5'-UTR and one previously reported variant (g.3836 G>C) in an intron. All three single nucleotide polymorphisms (SNPs) were associated with milk yield (p<0.0001), fat yield (p = 0.0006 to <0.0001), protein yield (p = 0.0232 to <0.0001) and protein percentage (p<0.0001), while no significant associations were detected between the SNPs and fat percentage. A strong linkage disequilibrium (D' = 0.96 to 1.00) was observed among all three SNPs, and a 5 Kb haplotype block involving three main haplotypes with GAG, AGC, and AGG was formed. The results of haplotype association analyses were consistent with the results of single locus association analysis (p<0.0001). The phenotypic variance ratio above 3.00% was observed for milk protein yield that was explained by SNP-g.3836G >C. Conclusion: Overall, our findings provided new insights into the polymorphic variations in bovine GALE gene and their associations with milk protein concentration. The data indicate their potential uses for marker-assisted breeding or genetic selection schemes.

Keywords

References

  1. Dallas DC, Murray NM, Gan JN. Proteolytic systems in milk: perspectives on the evolutionary function within the mammary gland and the infant. J Mammary Gland Biol Neoplasia 2015;20:133-47. https://doi.org/10.1007/s10911-015-9334-3
  2. Carta A, Casu S, Salaris S. Invited review: Current state of genetic improvement in dairy sheep. J Dairy Sci 2009;92:5814-33. https://doi.org/10.3168/jds.2009-2479
  3. Chen HY, Zhang Q, Yin CC, Wang CK, Gong WJ, Mei G. Detection of quantitative trait loci affecting milk production traits on bovine chromosome 6 in a Chinese Holstein population by the daughter design. J Dairy Sci 2006;89:782-90. https://doi.org/10.3168/jds.S0022-0302(06)72140-3
  4. Gebreyesus G, Lund MS, Janss L, et al. Short communication: Multi-trait estimation of genetic parameters for milk protein composition in the Danish Holstein. J Dairy Sci 2016;99:2863-6. https://doi.org/10.3168/jds.2015-10501
  5. Kolbehdari D, Wang Z, Grant JR, et al. A whole genome scan to map QTL for milk production traits and somatic cell score in Canadian Holstein bulls. J Anim Breed Genet 2009;126:216-27. https://doi.org/10.1111/j.1439-0388.2008.00793.x
  6. Sanchez MP, Ferrand M, Gele M, et al. Short communication: Genetic parameters for milk protein composition predicted using mid-infrared spectroscopy in the French Montbeliarde, Normande, and Holstein dairy cattle breeds. J Dairy Sci 2017;100:6371-5. https://doi.org/10.3168/jds.2017-12663
  7. Li C, Cai W, Zhou C, et al. RNA-Seq reveals 10 novel promising candidate genes affecting milk protein concentration in the Chinese Holstein population. Sci Rep 2016;6:26813. https://doi.org/10.1038/srep26813
  8. Amado M, Almeida R, Schwientek T, Clausen H. Identification and characterization of large galactosyltransferase gene families: galactosyltransferases for all functions. Biochim Biophys Acta Gen Subj 1999;1473:35-53. https://doi.org/10.1016/S0304-4165(99)00168-3
  9. Shahbazkia HR, Aminlari M, Cravador A. Association of polymorphism of the beta(1, 4)-galactosyltransferase-I gene with milk production traits in Holsteins. Mol Biol Rep 2012;39:6715-21. https://doi.org/10.1007/s11033-012-1495-1
  10. Xu Q, Mei G, Sun DX, et al. Detection of genetic association and functional polymorphisms of UGDH affecting milk production trait in Chinese Holstein cattle. BMC Genomics 2012;13:590 https://doi.org/10.1186/1471-2164-13-590
  11. Barrett JC, Fry B, Maller J, Daly MJ. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 2005;21:263-5. https://doi.org/10.1093/bioinformatics/bth457
  12. Browning SR, Browning BL. Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering. Am J Hum Genet 2007;81:1084-97. https://doi.org/10.1086/521987
  13. Gabriel SB, Schaffner SF, Nguyen H, et al. The structure of haplotype blocks in the human genome. Science 2002;296:2225-9. https://doi.org/10.1126/science.1069424
  14. Falconer DS, Mackay TFC. Introduction to quantitative genetics, 4th edn. New York, USA: Longman Scientific and Technical; 1996.
  15. Huang YZ, Li MX, Wang J, et al. A 5 '-regulatory region and two coding region polymorphisms modulate promoter activity and gene expression of the growth suppressor gene ZBED6 in cattle. Plos One 2013;8:e79744 https://doi.org/10.1371/journal.pone.0079744
  16. Nott A, Muslin SH, Moore MJ. A quantitative analysis of intron effects on mammalian gene expression. RNA 2003;9:607-17. https://doi.org/10.1261/rna.5250403
  17. Park HJ, Lee S, Ju E, Jones JA, Choi I. Alternative transcription of sodium/bicarbonate transporter SLC4A7 gene enhanced by single nucleotide polymorphisms. Physiol Genomics 2017;49:167-76. https://doi.org/10.1152/physiolgenomics.00112. 2016
  18. Sagne C, Marcel V, Amadou A, Hainaut P, Olivier M, Hall J. A meta-analysis of cancer risk associated with the TP53 intron 3 duplication polymorphism (rs17878362): geographic and tumor-specific effects. Cell Death Dis 2013;4:e492 https://doi.org/10.1038/cddis.2013.24
  19. Visser M, Palstra RJ, Kayser M. Human skin color is influenced by an intergenic DNA polymorphism regulating transcription of the nearby BNC2 pigmentation gene. Hum Mol Genet 2014;23:5750-62. https://doi.org/10.1093/hmg/ddu289
  20. Akey J, Jin L, Xiong MM. Haplotypes vs single marker linkage disequilibrium tests: what do we gain? Eur J Hum Genet 2001;9:291-300. https://doi.org/10.1038/sj.ejhg.5200619
  21. Martin ER, Lai EH, Gilbert JR, et al. SNPing away at complex diseases: Analysis of single-nucleotide polymorphisms around APOE in Alzheimer disease. Am J Hum Genet 2000;67:383-94. https://doi.org/10.1086/303003
  22. Daenzer JM, Sanders RD, Hang D, Fridovich-Keil JL. UDP- galactose 4'-epimerase activities toward UDP-Gal and UDP- GalNAc play different roles in the development of Drosophila melanogaster. PLoS Genet 2012;8:e1002721. https://doi.org/10.1371/journal.pgen.1002721
  23. Schulz JM, Ross KL, Malmstrom K, Krieger M, Fridovich-Keil JL. Mediators of galactose sensitivity in UDP-galactose 4'-epimerase-impaired mammalian cells. J Biol Chem 2005;280:13493-502. https://doi.org/10.1074/jbc.M414045200
  24. Roper JR, Guther MLS, Milne KG, Ferguson MAJ. Galactose metabolism is essential for the African sleeping sickness parasite Trypanosoma brucei. Proc Natl Acad Sci USA 2002;99:5884-9. https://doi.org/10.1073/pnas.092669999
  25. Seo A, Gulsuner S, Pierce S, et al. Inherited thrombocytopenia associated with mutation of UDP-Galactose-4-Epimerase (GALE). Hum Mol Genet 2019;28:133-42. https://doi.org/10.1093/hmg/ddy334
  26. Sanders RD, Sefton JMI, Moberg KH, Fridovich-Keil JL. UDP- galactose 4 ' epimerase (GALE) is essential for development of Drosophila melanogaster. Dis Model Mech 2010;3:628-38. https://doi.org/10.1242/dmm.005058
  27. Song HB, He M, Cai ZP, et al. UDP-glucose 4-epimerase and-1,4-galactosyltransferase from the oyster Magallana gigas as valuable biocatalysts for the production of galactosylated products. Int J Mol Sci 2018;19:1600. https://doi.org/10.3390/ijms19061600

Cited by

  1. Genetic Markers Associated with Milk Production Traits in Dairy Cattle vol.11, pp.10, 2021, https://doi.org/10.3390/agriculture11101018
  2. Proteomic Analysis Explores Interactions between Lactiplantibacillus plantarum and Saccharomyces cerevisiae during Sourdough Fermentation vol.9, pp.11, 2020, https://doi.org/10.3390/microorganisms9112353