Discovery and trait association of single nucleotide polymorphisms from gene regions of influence on meat tenderness and long-chain omega-3 fatty acid content in Australian lamb
M. I. Knight A B , H. D. Daetwyler A B , B. J. Hayes A B , M. J. Hayden B , A. J. Ball A D , D. W. Pethick A E and M. B. McDonagh A C F
+ Author Affiliations
- Author Affiliations
A Cooperative Research Centre for Sheep Industry Innovation, CJ Hawkins Homestead Building, University of New England, Armidale, NSW 2351, Australia.
B Biosciences Research Division, Department of Primary Industries, 1 Park Drive, Bundoora, Vic. 3083, Australia.
C Future Farming Research Division, Department of Primary Industries, 1 Park Drive, Bundoora, Vic. 3083, Australia.
D Meat and Livestock Australia, CJ Hawkins Homestead Building, University of New England, Armidale, NSW 2351, Australia.
E School of Veterinary and Biomedical Science, Murdoch University, Murdoch, WA 6150, Australia.
F Corresponding author. Email: matthew.mcdonagh@dpi.vic.gov.au
Animal Production Science 52(7) 591-600 https://doi.org/10.1071/AN11229
Submitted: 13 October 2011 Accepted: 23 February 2012 Published: 24 April 2012
Abstract
Whole genome association studies in humans have shown a strong relationship between omega-3 levels in plasma and single nucleotide polymorphisms (SNP) located close to genes whose protein products are involved in the biosynthesis of long-chain omega-3 fatty acids. In sheep and other livestock species, the calpain/calpastatin system is the principal influence on natural variation in meat tenderness between animals. Using targeted next generation sequencing, we sequenced the fatty acid desaturase locus (FADS1/2/3), ELOVL2 and SLC26A10 and the calpain/calpastatin (CAPN1/2/3 and CAST) gene loci of 35 industry sires from the Australian flock. A total of 753 SNP were identified and 182 of these SNP were selected for incorporation onto a research SNP panel that represented the genetic variation across the nine genes. A total of 1252 animals were genotyped from the Australian Sheep CRC Information Nucleus Flock for these SNP and the genomic association was calculated for omega-3 fatty acid content and objective meat tenderness in lamb. Six SNP within CAST and CAPN2 showed association with shear force at Day 5 post-mortem at a significance level of P ≤ 0.01. When these were fitted simultaneously in a mixed-model analysis with fixed effects and covariates, three SNP remained significant. These SNP each had an unfavourable effect on shear force of between 1.1 and 1.8 N, with a combined effect of 4.1 N. The frequency of the favourable alleles in the progeny measured indicates that these SNP hold good potential for improving the management of meat tenderness across Merino, Border Leicester and Terminal sire types. No SNP within the FADS1/2/3, ELOVL2 and SLC26A10 gene regions were associated with lamb muscle omega-3 levels. This indicates that genetic variation in the long-chain omega-3 biosynthesis pathway genes analysed here may not be important for omega-3 content in lamb within the Information Nucleus Flock population.
References
Barendse W (2002) DNA markers for meat tenderness. Commonwealth Scientific and Industrial Research Organisation, Meat and Livestock Australia Limited, New South Wales Department of Agriculture, Queensland Department of Primary Industries, and University of New England. Patent Application WO02064820.Barendse W (2007) Assessing the tenderness of meat from an animal by testing the animal for a genetic marker in the calpain3 (CAPN3) gene associated with Warner-Bratzler peak force variation or for a genetic marker located other than in CAPN3. Commonwealth Scientific and Industrial Research Organisation, Meat and Livestock Australia Limited, New South Wales Department of Agriculture, Queensland Department of Primary Industries, and University of New England, assignees. Patent Application WO2007053891.
Barendse W, Harrison BE, Bunch RJ, Thomas MB (2008) Variation at the Calpain 3 gene is associated with meat tenderness in zebu and composite breeds of cattle. BMC Genetics 9, 41
| Variation at the Calpain 3 gene is associated with meat tenderness in zebu and composite breeds of cattle.Crossref | GoogleScholarGoogle Scholar |
Bolormaa S, Neto LRP, Zhang YD, Bunch RJ, Harrison BE, Goddard ME, Barendse W (2011) A genome-wide association study of meat and carcass traits in Australian cattle. Journal of Animal Science 89, 2297–2309.
| A genome-wide association study of meat and carcass traits in Australian cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXps1yqtbY%3D&md5=28b65730dce0e13791c727a4f8e577bcCAS |
Brenna JT (2002) Efficiency of conversion of alpha-linolenic acid to long chain n-3 fatty acids in man. Current Opinion in Clinical Nutrition and Metabolic Care 5, 127–132.
| Efficiency of conversion of alpha-linolenic acid to long chain n-3 fatty acids in man.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XitVKnu7c%3D&md5=dbc562d27cedca1275dd4d8ca0ccaeacCAS |
Casas E, Shackelford SD, Keele JW, Koohmaraie M, Smith TP, Stone RT (2003) Detection of quantitative trait loci for growth and carcass composition in cattle. Journal of Animal Science 81, 2976–2983.
Casas E, White SN, Wheeler TL, Shackelford SD, Koohmaraie M, Riley DG, Chase CC, Johnson DD, Smith TP (2006) Effects of calpastatin and micro-calpain markers in beef cattle on tenderness traits. Journal of Animal Science 84, 520–525.
Curi RA, Chardulo LA, Mason MC, Arrigoni MD, Silveira AC, de Oliveira HN (2009) Effect of single nucleotide polymorphisms of CAPN1 and CAST genes on meat traits in Nellore beef cattle (Bos indicus) and in their crosses with Bos taurus. Animal Genetics 40, 456–462.
| Effect of single nucleotide polymorphisms of CAPN1 and CAST genes on meat traits in Nellore beef cattle (Bos indicus) and in their crosses with Bos taurus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVaiurfJ&md5=18ea83a3ff4774a4043424df35bbeb02CAS |
Gilmour AR, Gogel B, Cullis BR, Thompson R (2009) ‘2009 ASReml user guide. Release 3.0.’ (VSN International Ltd: Hemel Hempstead, UK)
Goll DE, Thompson VF, Li H, Wei W, Cong J (2003) The calpain system. Physiological Reviews 83, 731–801.
| The calpain system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmtVGmsL8%3D&md5=bd3de0791b749a05e3174d72bfddc1e1CAS |
Hopkins DL, Hegarty RS, Walker PJ, Pethick DW (2006) Relationship between animal age, intramuscular fat, cooking loss, pH, shear force and eating quality of aged meat from sheep. Australian Journal of Experimental Agriculture 46, 879–884.
| Relationship between animal age, intramuscular fat, cooking loss, pH, shear force and eating quality of aged meat from sheep.Crossref | GoogleScholarGoogle Scholar |
Howe P, Meyer B, Record S, Baghurst K (2006) Dietary intake of long-chain omega-3 polyunsaturated fatty acids: contribution of meat sources. Nutrition (Burbank, Los Angeles County, Calif.) 22, 47–53.
| Dietary intake of long-chain omega-3 polyunsaturated fatty acids: contribution of meat sources.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFWiurs%3D&md5=ab70ae1b79493f54a672ad4f8e4dd0c6CAS |
Kitessa S, Liu S, Briegel J, Pethick D, Gardner G, Ferguson M, Allingham P, Nattrass G, McDonagh M, Ponnampalam E, Hopkins D (2010) Effects of intensive or pasture finishing in spring and linseed supplementation in autumn on the omega-3 content of lamb meat and its carcass distribution. Animal Production Science 50, 130–137.
| Effects of intensive or pasture finishing in spring and linseed supplementation in autumn on the omega-3 content of lamb meat and its carcass distribution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhvVGqur4%3D&md5=9ade8ea8253839b971c9b3a4ce630628CAS |
Koohmaraie M (1994) Muscle proteinases and meat aging. Meat Science 36, 93–104.
| Muscle proteinases and meat aging.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXis1ygur0%3D&md5=4f1f51123ff55ce06eedfc528acfb921CAS |
Koohmaraie M, Geesink GH (2006) Contribution of postmortem muscle biochemistry to the delivery of consistent meat quality with particular focus on the calpain system. Meat Science 74, 34–43.
| Contribution of postmortem muscle biochemistry to the delivery of consistent meat quality with particular focus on the calpain system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xms1Grsbk%3D&md5=b8ea603cbcf7f53e165688388e819d21CAS |
Koohmaraie M, Seidemann SC, Schollmeyer JE, Dutson TR, Crouse JD (1987) Effect of post-mortem storage on Ca++-dependent proteases, their inhibitor and myofibril fragmentation. Meat Science 19, 187–196.
| Effect of post-mortem storage on Ca++-dependent proteases, their inhibitor and myofibril fragmentation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXlsFejt7s%3D&md5=1272f84dc80c056dc564520893a124a4CAS |
McDonagh MB, Fernandez C, Oddy VH (1999) Hind-limb protein metabolism and calpain system activity influence post-mortem change in meat quality in lamb. Meat Science 52, 9–18.
| Hind-limb protein metabolism and calpain system activity influence post-mortem change in meat quality in lamb.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXitFGrs78%3D&md5=270f068d2b9af1a626979dd235bb1897CAS |
Meuwissen TH, Hayes BJ, Goddard ME (2001) Prediction of total genetic value using genome-wide dense marker maps. Genetics 157, 1819–1829.
Morris CA, Cullen NG, Hickey SM, Dobbie PM, Veenvliet BA, Manley TR, Pitchford WS, Kruk ZA, Bottema CD, Wilson T (2006) Genotypic effects of calpain 1 and calpastatin on the tenderness of cooked M. longissimus dorsi steaks from Jersey × Limousin, Angus and Hereford-cross cattle. Animal Genetics 37, 411–414.
| Genotypic effects of calpain 1 and calpastatin on the tenderness of cooked M. longissimus dorsi steaks from Jersey × Limousin, Angus and Hereford-cross cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVCmtr%2FI&md5=6cc56137abe9514f248f9d4f51842722CAS |
Mortimer SI, van der Werf JHJ, Jacob RH, Pethick DW, Pearce KL, Warner RD, Geesink GH, Hocking Edwards JE, Gardner GE, Ponnampalam EN, Kitessa SM, Ball AJ, Hopkins DL (2010) Preliminary estimates of genetic parameters for carcass and meat quality traits in Australian sheep. Animal Production Science 50, 1135–1144.
| Preliminary estimates of genetic parameters for carcass and meat quality traits in Australian sheep.Crossref | GoogleScholarGoogle Scholar |
Ouali A, Talmant A (1990) Calpains and calpastatin distribution in bovine, porcine and ovine skeletal muscles. Meat Science 28, 331–348.
| Calpains and calpastatin distribution in bovine, porcine and ovine skeletal muscles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXltFejurg%3D&md5=750e40962af08352b9019bbfce3e072eCAS |
Page BT, Casas E, Quaas RL, Thallman RM, Wheeler TL, Shackelford SD, Koohmaraie M, White SN, Bennett GL, Keele JW, Dikeman ME, Smith TP (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.
Pannier L, Ponnampalam EN, Gardner GE, Hopkins DL, Ball AJ, Jacob RH, Pearce KL, Pethick DW (2010) Prime Australian lamb supplies key nutrients for human health. Animal Production Science 50, 1115–1122.
| Prime Australian lamb supplies key nutrients for human health.Crossref | GoogleScholarGoogle Scholar |
Pawlosky RJ, Hibbeln JR, Novotny JA, Salem N (2001) Physiological compartmental analysis of alpha-linolenic acid metabolism in adult humans. Journal of Lipid Research 42, 1257–1265.
Pethick DW, Warner RD, Banks RG (2006) Genetic improvement of lamb – industry issues and the need for integrated research. Australian Journal of Agricultural Research 57, 591–592.
| Genetic improvement of lamb – industry issues and the need for integrated research.Crossref | GoogleScholarGoogle Scholar |
Rowe JB (2010) The Australian sheep industry – undergoing transformation. Animal Production Science 50, 991–997.
| The Australian sheep industry – undergoing transformation.Crossref | GoogleScholarGoogle Scholar |
Schenkel FS, Miller SP, Jiang Z, Mandell IB, Ye X, Li H, Wilton JW (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.
Shackelford SD, Koohmaraie M, Wheeler TL, Cundiff LV, Dikeman ME (1994) Effect of biological type of cattle on the incidence of the dark, firm, and dry condition in the longissimus muscle. Journal of Animal Science 72, 337–343.
Smith TP, Casas E, Rexroad CE, Kappes SM, Keele JW (2000) Bovine CAPN1 maps to a region of BTA29 containing a quantitative trait locus for meat tenderness. Journal of Animal Science 78, 2589–2594.
Sprecher H, Luthria DL, Mohammed BS, Baykousheva SP (1995) Reevaluation of the pathways for the biosynthesis of polyunsaturated fatty acids. Journal of Lipid Research 36, 2471–2477.
Tanaka T, Shen J, Abecasis GR, Kisialiou A, Ordovas JM, Guralnik JM, Singleton A, Bandinelli S, Cherubini A, Arnett D, Tsai MY, Ferrucci L (2009) Genome-wide association study of plasma polyunsaturated fatty acids in the InCHIANTI study. PLOS Genetics 5, e1000338
| Genome-wide association study of plasma polyunsaturated fatty acids in the InCHIANTI study.Crossref | GoogleScholarGoogle Scholar |
The International Sheep Genomics Consortium Archibald AL, Cockett NE, Dalrymple BP, Faraut T, Kijas JW, Maddox JF, McEwan JC, Hutton Oddy V, Raadsma HW, Wade C, Wang J, Wang W, Xun X (2010) The sheep genome reference sequence: a work in progress. Animal Genetics 41, 449–453.
| The sheep genome reference sequence: a work in progress.Crossref | GoogleScholarGoogle Scholar |
van der Werf JHJ, Kinghorn BP, Banks RG (2010) Design and role of an information nucleus in sheep breeding programs. Animal Production Science 50, 998–1003.
| Design and role of an information nucleus in sheep breeding programs.Crossref | GoogleScholarGoogle Scholar |
Warner RD, Jacob RH, Edwards JEH, McDonagh M, Pearce K, Geesink G, Kearney G, Allingham P, Hopkins DL, Pethick DW (2010) Quality of lamb meat from the Information Nucleus Flock. Animal Production Science 50, 1123–1134.
| Quality of lamb meat from the Information Nucleus Flock.Crossref | GoogleScholarGoogle Scholar |
White SN, Casas E, Wheeler TL, Shackelford SD, Koohmaraie M, Riley DG, Chase CC, Johnson DD, Keele JW, Smith TP (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.
Zhou H, Hickford JG, Fang Q (2007) Single nucleotide polymorphisms of the ovine calpain 3 (CAPN3) gene. Molecular and Cellular Probes 21, 78–79.
| Single nucleotide polymorphisms of the ovine calpain 3 (CAPN3) gene.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht12rtrbE&md5=5c07c813aea3c7645886d7e0ec189f49CAS |
