Abstract
Correlation between expression level of the bovine DNAJA1 gene and meat tenderness was recently found in Charolais longissimus thoracis muscle samples, suggesting that this gene could play an important role in meat tenderness. Here, we report the validation of polymorphisms within the bovine DNAJA1 gene, and the haplotype variability and extent of linkage disequilibrium in the three main French beef breeds (Blonde d’Aquitaine, Charolais, Limousin). Genotyping 18 putative SNPs revealed that 16 SNPs were polymorphic within the breeds tested. Two SNPs were removed from further analyses as one SNP had a low genotyping call rate, while the other SNP was not in Hardy–Weinberg equilibrium. The degree of heterozygosity observed for the remaining 14 SNPs varied between breeds, with Charolais being the breed with the highest genetic variation and Blonde d’Aquitaine the lowest. Linkage disequilibrium and haplotype structure of DNAJA1 were different between breeds. Eighteen different haplotypes, including three shared by all breeds, were discovered, and two to three tag SNPs (depending on the breed) are sufficient to capture all the genetic variability seen in these haplotypes. The results of this study will facilitate the design of optimal future association studies evaluating the role of the DNAJA1 gene in meat tenderness.
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Casas, E., Keele, J. W., Shackelford, S. D., Koohmaraie, M., Sonstegard, T. S., Smith, T. P. L., et al. (1998). Association of the muscle hypertrophy locus with carcass traits in beef cattle. Journal of Animal Science, 76, 468–473.
Keele, J. W., Shackelford, S. D., Kappes, S. M., Koohmaraie, M., & Stone, R. T. (1999). A region on bovine chromosome 15 influences beef longissimus tenderness in steers. Journal of Animal Science, 77, 1364–1371.
Casas, E., Shackelford, S. D., Keele, J. W., Stone, R. T., Kappes, S. M., & Koohmaraie, M. (2000). Quantitative trait loci affecting growth and carcass composition of cattle segregating alternate forms of myostatin. Journal of Animal Science, 78, 560–569.
Casas, E., Stone, R. T., Keele, J. W., Shackelford, S. D., Kappes, S. M., & Koohmaraie, M. (2001). A comprehensive search for quantitative trait loci affecting growth and carcass composition of cattle segregating alternative forms of the myostatin gene. Journal of Animal Science, 79, 854–860.
Casas, E., Shackelford, S. D., Keele, J. W., Koohmaraie, M., Smith, T. P. L., & Stone, R. T. (2003). Detection of quantitative trait loci for growth and carcass composition in cattle. Journal of Animal Science, 81, 2976–2983.
Drinkwater, R. D., Li, Y., Lenane, I., Davis, G. P., Shorthose, R., Harrison, B. E., et al. (2006). Detecting quantitative trait loci affecting beef tenderness on bovine chromosome 7 near calpastatin and lysil oxidase. Australian Journal of Experimental Agriculture, 46, 159–164.
Alexander, L. J., MacNeil, M. D., Geary, T. W., Snelling, W. M., Rule, D. C., & Scanga, J. A. (2007). Quantitative trait loci with additive effects on palatability and fatty acid composition of meat in a Wagyu-Limousin F2 population. Animal Genetics, 38, 506–513.
Davis, G. P., Moore, S. S., Drinkwater, R. D., Shorthose, W. R., Loxton, I. D., Barendse, W., et al. (2007). QTL for meat tenderness in the M. Longissimus lumborum of cattle. Animal Genetics, 39, 40–45.
Gutiérrez-Gil, B., Wiener, P., Nute, G. R., Burton, D., Gill, J. L., Wood, J. D., et al. (2008). Detection of quantitative trait loci for meat quality traits in cattle. Animal Genetics, 39, 51–61.
Barendse, W. J. (2002). DNA markers for meat tenderness. International patent application PCT/AU02/00122; International patent publication WO 02/064820 A1.
Schenkel, F. S., Miller, S. P., Jiang, Z., Mandell, I. B., Ye, X., Li, H., et al. (2006). Association of a single nucleotide polymorphism in the calpastatin gene with carcass and meat quality traits of beef cattle. Journal of Animal Science, 84, 291–299.
Page, B. T., Casas, E., Heaton, M. P., Cullen, N. G., Hyndman, D. L., Morris, C. A., et al. (2002). Evaluation of single-nucleotide polymorphism in CAPN1 for association with meat tenderness in cattle. Journal of Animal Science, 80, 3077–3085.
White, S. N., Casas, E., Wheeler, T. L., Shackelford, S. D., Koohmaraie, M., Riley, D. G., et al. (2005). A new single nucleotide polymorphism in CAPN1 extends the current tenderness marker test to include cattle of Bos indicus, Bos Taurus, and crossbred descent. Journal of Animal Science, 83, 2001–2008.
Page, B. T., Casas, E., Quaas, R. L., Thallman, R. M., Wheeler, T. L., Shackelford, S. D., et al. (2004). Association of markers in the bovine CAPN1 gene with meat tenderness in large crossbred populations that sample influential industry sires. Journal of Animal Science, 82, 3474–3481.
Casas, E., White, S. N., Wheeler, T. L., Shackelford, S. D., Koohmaraie, M., Riley, D. G., et al. (2006). Effects of calpastatin and μ-calpain markers in beef cattle on tenderness traits. Journal of Animal Science, 84, 520–525.
Morris, C. A., Cullen, N. G., Hickey, S. M., Dobbie, P. M., Veenvliet, B. A., Manley, T. R., et al. (2006). Genotypic effects of calpain 1 and calpastatin on the tenderness of cooked M. longissimu dorsi steaks from Jersey x Limousin, Angus and Hereford-cross cattle. Animal Genetics, 37, 411–414.
Costello, S., O’Doherty, E., Troy, D. J., Ernst, C. W., Kim, K.-S., Stapelton, P., et al. (2007). Association of polymorphisms in the calpain I, calpain II and growth hormone genes with tenderness in bovine M. longissimus dorsi. Meat Science, 75, 551–557.
Van Eenennaam, A. L., Li, J., Thallman, R. M., Quaas, R. L., Dikeman, M. E., Gill, C. A., et al. (2007). Validation of commercial DNA tests for quantitative beef quality traits. Journal of Animal Science, 85, 891–900.
Wheeler, T. L., Shackelford, S. D., Casas, E., Cundiff, L. V., & Koohmaraie, M. (2001). The effects of Piedmontese inheritance and myostatin genotype on the palatability of longissimus thoracis, gluteus medius, semimembranosus, and biceps femoris. Journal of Animal Science, 79, 3069–3074.
Lines, S. S., Pitchford, W. S., Kruk, Z. A., & Bottema, C. D. K. (2009). Limousin myostatin F94L variants affects semitendinosus tenderness. Meat Science, 81, 126–131.
Di Stasio, L., Brugiapaglia, A., Destefanis, G., Albera, A., & Sartore, S. (2003). GH1 as candidate gene for variability of meat production traits in Piemontese cattle. Journal of Animal Breeding and Genetics, 120, 358–361.
Schenkel, F. S., Miller, S. P., Ye, X., Moore, S. S., Nkrumah, J. D., Li, C., et al. (2005). Association of single nucleotide polymorphisms in the leptin gene with carcass and meat quality traits of beef cattle. Journal of Animal Science, 83, 2009–2020.
Barendse, W., Harrison, B. E., Bunch, R. J., & Thomas, M. B. (2008). Variation at the Calpain 3 gene is associated with meat tenderness in zebu and composite breeds of cattle. BMC Genetics, 9, 41.
Bernard, C., Cassar-Malek, I., Le Cunff, M., Dubroeucq, H., Renand, G., & Hocquette, J.-F. (2007). New indicators of beef sensory quality revealed by expression of specific genes. Journal of Agricultural and Food Chemistry, 55, 5229–5237.
Gotoh, T., Terada, K., Oyadomari, S., & Mori, M. (2004). Hsp70-DnaJ chaperone pair prevents nitric oxide- and CHOP-induced apoptosis by inhibiting translocation of Bax to mitochondria. Cell Death and Differentiation, 11, 390–402.
Lin, C. H., Yeakley, J. M., McDaniel, T. K., & Shen, R. (2009). Medium- to high-throughput SNP genotyping using VeraCode microbeads. Methods in Molecular Biology, 496, 129–142.
Barrett, J. C., Fry, B., Maller, J., & Daly, M. J. (2005). Haploview: Analysis and visualization of LD and haplotype maps. Bioinformatics, 21, 263–265.
Wang, N., Akey, J. M., Zhang, K., Chakraborty, R., & Jin, L. (2002). Distribution of recombination crossovers and the origin of haplotype blocks: The interplay of population history, recombination, and mutation. American Journal of Human Genetics, 71, 1227–1234.
Stephens, M., Smith, N. J., & Donnelly, P. (2001). A new statistical method for haplotype reconstruction from population data. American Journal of Human Genetics, 68, 978–989.
De Bakker, P. I., Yelensly, R., Pe’er, I., Gabriel, S. B., Daly, M. J., & Altshuler, D. (2005). Efficiency and power in genetic association studies. Nature Genetics, 37, 1217–1223.
The Bovine HapMap Consortium. (2009). Genome-wide survey of SNP variation uncovers the genetic structure of cattle breeds. Science, 324, 528–532.
Moazami-Goudarzi, K., Laloe, D., Furet, J. P., & Grosclaude, F. (1997). Analysis of genetic relationships between 10 cattle breeds with 17 microsatellites. Animal Genetics, 28, 338–345.
Loftus, R. T., Ertugrul, O., Harba, A. H., El-Barody, A., MacHugh, D. E., Park, S. D. E., et al. (1999). A microsatellite survey of cattle from a centre of origin: The Near East. Molecular Ecology, 8, 2015–2022.
Maudet, C., Luikart, G., & Taberlet, P. (2002). Genetic diversity and assignment tests among seven French cattle breeds based on microsatellite DNA analysis. Journal of Animal Science, 80, 942–950.
Mateus, J. C., Penedo, M. C. D., Alves, V. C., Ramos, M., & Rangel-Figueiredo, T. (2004). Genetic diversity and differentiation in Portuguese cattle breeds using microsatellites. Animal Genetics, 35, 106–113.
European Cattle Genetic Diversity Consortium. (2006). Marker-assisted conservation of European cattle breeds: An evaluation. Animal Genetics, 37, 475–481.
MacNeil, M. D., Cronin, M. A., Blackburn, H. D., Richards, C. M., Lockwood, D. R., & Alexander, L. J. (2007). Genetic relationships between feral cattle from Chirikof Island, Alaska and other breeds. Animal Genetics, 38, 193–197.
Zhang, G. X., Wang, Z. G., Chen, W. S., Wu, C. X., Han, X., Chang, H., et al. (2007). Genetic diversity and population structure of indigenous yellow cattle breeds of China using 30 microsatellite markers. Animal Genetics, 38, 550–559.
Lewontin, R. C. (1964). The interaction of selection and linkage. I. General considerations; heterotic models. Genetics, 40, 250–256.
Hill, W. G., & Robertson, A. (1968). Linkage disequilibrium in finite populations. Theoretical and Applied Genetics, 38, 226–231.
Ardlie, K. G., Kruglyak, L., & Seielstad, M. (2002). Patterns of linkage disequilibrium in the human genome. Nature Review Genetics, 3, 299–309.
Du, F.-X., Clutter, A., & Lohuis, M. M. (2007). Characterizing linkage disequilibrium in pig populations. International Journal of Biological Sciences, 3, 166–178.
Zhao, H., Nettleton, D., & Dekkers, J. C. M. (2007). Evaluation of linkage disequilibrium measures between multi-allelic markers as predictors of linkage disequilibrium between single nucleotide polymorphisms. Genetics Research, 89, 1–6.
Sargolzaei, M., Schenkel, F. S., Jansen, G. B., & Schaeffer, L. R. (2008). Extent of linkage disequilibrium in Holstein cattle in North America. Journal of Dairy Science, 91, 2106–2117.
McKay, S. D., Schnabel, R. D., Murdoch, B. M., Matukumalli, L. K., Aerts, J., Coppieters, W., et al. (2007). Whole genome linkage disequilibrium maps in cattle. BMC Genetics, 8, 74.
Khatkar, M. S., Nicholas, F. W., Collins, A. R., Zenger, K. R., Cavanagh, J. A. L., Barris, W., et al. (2008). Extent of genome-wide linkage disequilibrium in Australian Holstein-Friesian cattle based on a high-density SNP panel. BMC Genomics, 9, 197.
Kim, E.-S., & Kirkpatrick, B. W. (2009). Linkage disequilibrium in the North American Holstein population. Animal Genetics, 40, 279–288.
Acknowledgements
The authors are grateful to the International Bovine Genome Sequencing Consortium for the identification and submission into the public domain of the bovine SNPs used during this work. The authors also would like to thank the following breeding companies for providing blood samples for the animals tested in this study: Midatest, UALC, UCATRC and UCEF. This work was funded by INRA, the Université de Limoges, Agence Nationale de la Recherche (contracts ANR-05-GANI-005 and ANR-05-GANI-017-01) and APIS GENE (contract 01-2005-QualviGenA-02).
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Marty, A., Amigues, Y., Servin, B. et al. Genetic Variability and Linkage Disequilibrium Patterns in the Bovine DNAJA1 Gene. Mol Biotechnol 44, 190–197 (2010). https://doi.org/10.1007/s12033-009-9228-y
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DOI: https://doi.org/10.1007/s12033-009-9228-y