Abstract
The uncoupling proteins (UCPs) belong to the mitochondrial inner membrane anion carrier superfamily and play an important role in energy homeostasis. Genetic studies have demonstrated that Ucp2 and Ucp3 gene variants are involved in obesity and metabolic syndrome. The aim of this study was to identify associations between polymorphisms of Ucp2 and Ucp3 genes and economically-important traits in Qinchuan cattle. In the present study, one single-nucleotide polymorphism (SNP) in the 5 ′UTR region (SNP1: g.C-754G) of the Ucp2 gene was identified by direct sequencing of 441 Qinchuan cattle. Two SNPs in exon 3 (SNP2: g.G4877A; SNP3: g.C4902T) of the Ucp3 gene were identified by sequencing and polymerase chain reaction-restriction fragment length polymorphism (PCR-RFLP) among 441 Qinchuan cattle. Association analysis showed that SNP1 and SNP2 were associated with the meat quality traits (MQTs) including back fat thickness, loin muscle area and intramuscular fat content. SNP3 was found to be associated with part of the body measurement traits (BMTs) which referred to withers height and chest depth. In addition, QTL pyramiding analysis showed that individuals with diplotype P3P3 (GG–GG–CC) exhibited the best performance in terms of back fat thickness, loin muscle area, intramuscular fat content, rump length, hip width, chest depth and chest circumference. With regard to the G4877A mutation, real time PCR analysis revealed that individuals with AA genotype of the Ucp3 gene expressed higher mRNA levels than those with GG genotype. These results suggest that the diplotype P3P3 (GG–GG–CC) could be used as a molecular marker of the combined genotypes for future selection of body measurement traits and meat quality traits in Qinchuan cattle.
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References
Andersen G., Dalgaard L. T., Justesen J. M., Anthonsen S., Nielsen T., Thorner L. W. et al. 2013 The frequent UCP2 −866G >A polymorphism protects against insulin resistance and is associated with obesity: a study of obesity and related metabolic traits among 17,636 Danes. Int. J. Obes. (Lond.) 37, 175–181.
An X. P., Hou J. X., Zhao H. B., Li G., Bai L., Peng J. Y. et al. 2013 Polymorphism identification in goat GNRH1 and GDF9 genes and their association analysis with litter size. Anim. Genet. 44, 234–238.
Akey J., Jin L. and Xiong M. M. 2001 Haplotypes vs single marker linkage disequilibrium tests: what do we gain? Eur. J. Hum. Genet. 9, 291–300.
Ardlie K. G., Kruglyak L. and Seielstad M. 2002 Patterns of linkage disequilibrium in the human genome. Nat. Rev. Genet. 3, 299–309.
Ashikari M. and Matsuoka M. 2006 Identification, isolation and pyramiding of quantitative trait loci for rice breeding. Trends Plant Sci. 11, 344–350.
Azzu V. and Brand M. D. 2010 The on–off switches of the mitochondrial uncoupling proteins. Trends Biochem. Sci. 35, 298–307.
Brand M. D. and Esteves T. C. 2005 Physiological functions of the mitochondrial uncoupling proteins UCP2 and UCP3. Cell Metab. 2, 85–93.
Cieslak J., Nowacka-Woszuk J., Bartz M., Fijak-Nowak H., Grzes M., Szydlowski M. et al. 2009 Association studies on the porcine RETN, UCP1, UCP3 and ADRB3 genes polymorphism with fatness traits. Meat Sci. 83, 551–554.
de Almeida Brondani L, de Souza B. M., Assmann T. S., Boucas A. P., Bauer A. C., Canani L. H. et al. 2014 Association of the UCP polymorphisms with susceptibility to obesity: case–control study and meta-analysis. Mol. Biol. Rep. 41, 5053–5067.
Donadelli M., Dando I., Fiorini C. and Palmieri M. 2014 UCP2, a mitochondrial protein regulated at multiple levels. Cell Mol. Life Sci. 71, 1171–1190.
Gilbert R. P., Bailey D. R. and Shannon N. H. 1993 Linear body measurements of cattle before and after 20 years of selection for postweaning gain when fed two different diets. J. Anim. Sci. 71, 1712–1720.
Gibson G. and Honeycutt E. 2002 The evolution of developmental regulatory pathways. Curr. Opin. Genet. Dev. 12, 695–700.
Han X., Jiang T., Yang H., Zhang Q., Wang W., Fan B. et al. 2012 Investigation of four porcine candidate genes (H-FABP, MYOD1, UCP3 and MASTR) for meat quality traits in large white pigs. Mol. Biol. Rep. 39, 6599–6605.
Hideyuki M. 2011 Identification and utilization of genes associated with beef qualities. Anim. Sci. J. 82, 1–7.
Hirwa C. A., Wallace P., Shen X., Nie Q., Yang G. and Zhang X. 2011 Genes related to economically important traits in beef cattle. Asian J. Anim. Sci. 5, 34–45.
Kimchi S. C., Oh J. M., Kim I. W., Sauna Z. E., Calcagno A. M., Ambudkar S. V. et al. 2007 A “silent” polymorphism in the MDR1 gene changes substrate specificity. Science 315, 525–528.
Li H., Brahi O. H., Zhao X., Xu N. and Zhao X. 2012 Association of pig UCP3 gene mutations and back fat thickness in the sixth and seventh rib. Mol. Biol. Rep. 39, 1823–1829.
Liu B. H. 1998 Statistical genomics: linkage, mapping and QTL analysis, pp. 404–409. CRC Press LLC, Boca Raton, FL, USA.
Mayo A. E., Setty Y., Shavit S., Zaslaver A. and Alon U. 2006 Plasticity of the cis-regulatory input function of a gene. PLoS Biol. 4, e45.
Morris R. W. and Kaplan N. L. 2002 On the advantage of haplotype analysis in the presence of multiple disease susceptibility alleles. Genet. Epidemiol. 23, 221–233.
Motoyuki A. and Makoto M. 2006 Identification, isolation and pyramiding of quantitative trait loci for rice breeding. Trends Plant Sci. 11, 344–350.
Muhammad I. K., Cheorun J. and Muhammad R. T. 2015 Meat flavor precursors and factors influencing flavor precursors—a systematic review. Meat Sci. 110, 278–284.
Musa C. V., Mancini A., Alfieri A., Labruna G., Valerio G., Franzese A. et al. 2012 Four novel UCP3 gene variants associated with childhood obesity: effect on fatty acid oxidation and on prevention of triglyceride storage. Int. J. Obes. (Lond.) 36, 207–217.
Pan C., Wu C., Jia W., Xu Y., Lei C., Hu S. et al. 2013 A critical functional missense mutation H173R in the bovine PROP1 gene significantly affects 338 growth traits in cattle. Gene 531, 398–402.
Pedersen L. D., Sorensen A. C. and Berg P. 2009 Marker-assisted selection can reduce true as well as pedigree-estimated inbreeding. J. Dairy Sci. 92, 2214–2223.
Raymond M. and Rousset F. 1995 GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J. Hered. 86, 248–249.
Ricquier D. and Bouillaud F. 2000 The uncoupling protein homologues: UCP1, UCP2, UCP3, StUCP and AtUCP. Biochem. J. 345, 161–179.
Ruengphayak S., Chaichumpoo E., Phromphan S., Kamolsukyunyong W., Sukhaket W., Phuvanartnarubal E. et al. 2015 Pseudo-backcrossing design for rapidly pyramiding multiple traits into a preferential rice variety. Rice 8, 7.
Say Y. H., Ban Z. L., Arumugam Y., Kaur T., Tan M. L., Chia P. P. et al. 2014 Uncoupling protein 2 gene (UCP2) 45-bp I/D polymorphism is associated with adiposity among Malaysian women. J. Biosci. 39, 867–875.
Sherman E. L., Nkrumah J. D., Murdoch B. M., Li C., Wang Z., Fu A. et al. 2008 Polymorphisms and haplotypes in the bovine neuropeptide Y, growth hormone receptor, ghrelin, insulin-like growth factor 2, and uncoupling proteins 2 and 3 genes and their associations with measures of growth, performance, feed efficiency, and carcass merit in beef cattle. J. Anim. Sci. 86, 1–16.
Srivastava N., Prakash J., Lakhan R., Agarwal C. G., Pant D. C. and Mittal B. 2010 A common polymorphism in the promoter of UCP2 is associated with obesity and hyperinsulenemia in northern Indians. Mol. Cell Biochem. 337, 293–298.
Stefan K., Chen Y. -Z. and Bradford B. L. 2005 The mitochondrial uncoupling-protein homologues. Nat. Rev. Mol. Cell. Biol. 6, 248–261.
Tizioto P. C., Coutinho L. L., Decker J. E., Schnabel R. D., Rosa K. O., Oliveira P. S. et al. 2015 Global liver gene expression differences in Nelore steers with divergent residual feed intake phenotypes. BMC Genomics 16, 242.
Wang G., Zhang S., Wei S., Zhang Y., Li Y., Fu C. et al. 2014 Novel polymorphisms of SIX4 gene and their association with body measurement traits in Qinchuan cattle. Gene 539, 107–110.
Wang J., Hua L. S., Pan H., Zhang L. Z., Li M. X., Huang Y. Z. et al. 2015a Haplotypes in the promoter region of the CIDEC gene associated with growth traits in Nanyang cattle. Sci. Rep. 5, 12075.
Wang W., Liu S., Li F., Pan X., Li C., Zhang X. et al. 2015b Polymorphisms of the Ovine BMPR-IB, BMP-15 and FSHR and their associations with litter size in two chinese indigenous sheep breeds. Int. J. Mol. Sci. 16, 11385–11397.
Xue J., Sun Y. J., Guo W. J., Yang Z. Q., Tian H. B., Zhang C. L. et al. 2013 Haplotypes and effects on growth traits of bovine Wnt7a gene in Chinese Qinchuan cattle. Gene 524, 241–245.
Acknowledgements
We thank members of the Linsen Zan lab for helpful discussions. We especially thank Dr Yang for help and consultations on the experimental design, data analyses and paper revisions. The research was supported by the National 863 Program of China (nos. 2013AA102505; 2011AA100307-02), Natural Science Foundation of Shaanxi Province (2015JQ3064), National Natural Science Foundation of China (CN) (nos. 31272411; 31402044), National Beef and Yak Industrial Technology System (CARS-38) and National Science-Technology Support Plan Projects (2012BAD28B04-03).
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Corresponding editor: Indrajit Nanda
Yaning Wang and Wucai Yang contributed equally to this work
[Wang Y., Yang W., Gui L., Wang H. and Zan L. 2016 Association and expression analyses of the Ucp2 and Ucp3 gene polymorphisms with body measurement and meat quality traits in Qinchuan cattle. J. Genet. 95, xx–xx]
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WANG, Y., YANG, W., GUI, L. et al. Association and expression analyses of the Ucp2 and Ucp3 gene polymorphisms with body measurement and meat quality traits in Qinchuan cattle. J Genet 95, 939–946 (2016). https://doi.org/10.1007/s12041-016-0720-4
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DOI: https://doi.org/10.1007/s12041-016-0720-4