Skip to main content
Springer Nature Link
Log in

Muscle transcriptomic analyses in Angus cattle with divergent tenderness

  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

Beef tenderness contributes significantly to variation of beef palatability, and is largely influenced by various genetic and environmental factors. To identify candidate genes and pathways related to beef tenderness, we analyzed the longissimus dorsi (LD) muscle of Angus cattle that had different degrees of tenderness, measured by Warner–Bratzler shear force (WBSF). Microarray and RT-PCR analyses identified 53 genes that were differentially expressed in LD samples categorized as either tough or tender, including myosin, heavy chain 3 skeletal muscle embryonic (MYH3), myosin heavy chain 8 skeletal muscle perinatal (MYH8), guanylate binding protein 5 (GBP5), fatty acid binding protein 4 (FABP4), Stearoyl-coenzyme A desaturase (SCD), Fatty acid synthase (FASN), ubiquitin-like with PHD and ring finger domains 1 (UHRF1). Most of these genes are involved in lipid metabolism and skeletal muscle contraction. Employing Gene ontology (GO) and Ingenuity Pathway Analysis (IPA), several GO terms and pathways were found to be related to hydrolase, peptidase and GTPase activity, lipid metabolism, small molecule biochemistry, molecular transport, and tissue development. Overall, this analysis provides insight into the metabolic relationships between muscle biology and beef quality.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Boleman SJ, Boleman SL, Miller RK, Taylor JF, Cross HR, Wheeler TL, Koohmaraie M, Shackelford SD, Miller MF, West RL, Johnson DD, Savell JW (1997) Consumer evaluation of beef of known categories of tenderness. J Anim Sci 75:1521–1524

    PubMed  CAS  Google Scholar 

  2. Goodson KJ, Morgan WW, Reagan JO, Gwartney BL, Courington SM, Wise JW, Savell JW (2002) Beef customer satisfaction: factors affecting consumer evaluations of clod steaks. J Anim Sci 80:401–408

    PubMed  CAS  Google Scholar 

  3. Brady DE (1937) A study of the factors influencing tenderness and texture of beef. J Anim Sci 1937:246–250

    Google Scholar 

  4. Hertzman C, Olsson U, Tornberg E (1993) The influence of high temperature, type of muscle and electrical stimulation on the course of rigor, ageing and tenderness of beef muscles. Meat Sci 35:119–141

    Article  PubMed  CAS  Google Scholar 

  5. Minks D, Stringer WC (1972) The influence of aging beef in vacuum. J Food Sci 37:736–738

    Article  Google Scholar 

  6. Monsón F, Sañudo C, Sierra I (2005) Influence of breed and ageing time on the sensory meat quality and consumer acceptability in intensively reared beef. Meat Sci 71:471–479

    Article  PubMed  Google Scholar 

  7. Neely TR, Lorenzen CL, Miller RK, Tatum JD, Wise JW, Taylor JF, Buyck MJ, Reagan JO, Savell JW (1999) Beef customer satisfaction: cooking method and degree of doneness effects on the top round steak. J Anim Sci 77:653–660

    PubMed  CAS  Google Scholar 

  8. O’Connor SF, Tatum JD, Wulf DM, Green RD, Smith GC (1997) Genetic effects on beef tenderness in Bos indicus composite and Bos taurus cattle. J Anim Sci 75:1822–1830

    PubMed  Google Scholar 

  9. 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 Sci 74:34–43

    Article  PubMed  CAS  Google Scholar 

  10. Nishimura T, Hattori A, Takahashi K (1999) Structural changes in intramuscular connective tissue during the fattening of Japanese Black cattle: effect of marbling on beef tenderization. J Anim Sci 77:93–104

    PubMed  CAS  Google Scholar 

  11. Tornberg E (1996) Biophysical aspects of meat tenderness. Meat Sci 43:175–191

    Article  Google Scholar 

  12. Thompson JM, Perry D, Daly B, Gardner GE, Johnston DJ, Pethick DW (2006) Genetic and environmental effects on the muscle structure response post-mortem. Meat Sci 74:59–65

    Article  PubMed  CAS  Google Scholar 

  13. Huffman KL, Miller MF, Hoover LC, Wu CK, Brittin HC, Ramsey CB (1996) Effect of beef tenderness on consumer satisfaction with steaks consumed in the home and restaurant. J Anim Sci 74:91–97

    PubMed  CAS  Google Scholar 

  14. 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 Genet 9:41

    Article  PubMed  Google Scholar 

  15. Davis GP, Moore SS, Drinkwater RD, Shorthose WR, Loxton ID, Barendse W, Hetzel DJS (2008) QTL for meat tenderness in the M. longissimus lumborum of cattle. Anim Genet 39:40–45

    Article  PubMed  CAS  Google Scholar 

  16. Gao Y, Zhang R, Hu X, Li N (2007) Application of genomic technologies to the improvement of meat quality of farm animals. Meat Sci 77:36–45

    Article  PubMed  Google Scholar 

  17. Hocquette JF, Renard G, Levéziel H, Picard B, Cassar-Malek I (2006) The potential benefits of genetics and genomics to improve beef quality—a review. Anim Sci Pap Rep 24:173–186

    CAS  Google Scholar 

  18. Jennifer G, Stephen B, Caroline MC, John W, Pamela W (2009) Association of selected SNP with carcass and taste panel assessed meat quality traits in a commercial population of Aberdeen Angus-sired beef cattle. Genet Sel Evol 41:36

    Article  Google Scholar 

  19. Morzel M, Terlouw C, Chambon C, Micol D, Picard B (2008) Muscle proteome and meat eating qualities of longissimus thoracis of Blonde d’Aquitaine young bulls: a central role of HSP27 isoforms. Meat Sci 78:297–304

    Article  PubMed  CAS  Google Scholar 

  20. Mullen AM, Stapleton PC, Corcoran D, Hamill RM, White A (2006) Understanding meat quality through the application of genomic and proteomic approaches. Meat Sci 74:3–16

    Article  PubMed  CAS  Google Scholar 

  21. Koohmaraie M, Kent MP, Shackelford SD, Veiseth E, Wheeler TL (2002) Meat tenderness and muscle growth: is there any relationship? Meat Sci 62:345–352

    Article  PubMed  Google Scholar 

  22. Chen FY, Niu H, Wang JQ, Lei CZ, Lan XY, Zhang CL, Li MJ, Hua LS, Wang J, Chen H (2011) Polymorphism of DLK1 and CLPG gene and their association with phenotypic traits in Chinese cattle. Mol Biol Rep 38:243–248

    Article  PubMed  CAS  Google Scholar 

  23. Bernard C, Cassar-Malek I, Le Cunff M, Dubroeucq H, Renand G, Hocquette JF (2007) New indicators of beef sensory quality revealed by expression of specific genes. J Agric Food Chem 55:5229–5237

    Article  PubMed  CAS  Google Scholar 

  24. Iglesias PP, Caffaro ME, Amadio AF, Arias Mañotti A, Poli MA (2011) CAPN1 markers in three Argentinean cattle breeds: report of a new InDel polymorphism within intron 17. Mol Biol Rep 38:1645–1649

    Article  PubMed  CAS  Google Scholar 

  25. Iwanowska A, Grześ B, Mikołajczak B, Iwańska E, Juszczuk-Kubiak E, Rosochacki SJ, Pospiech E (2011) Impact of polymorphism of the regulatory subunit of the -calpain (CAPN1S) on the proteolysis process and meat tenderness of young cattle. Mol Biol Rep 38:1295–1300

    Article  PubMed  CAS  Google Scholar 

  26. Fan YY, Zan LS, Fu CZ, Tian WQ, Wang HB, Liu YY, Xin YP (2011) Three novel SNPs in the coding region of PPAR gene and their associations with meat quality traits in cattle. Mol Biol Rep 38:131–137

    Article  PubMed  CAS  Google Scholar 

  27. Zhang YY, Zan LS, Wang HB (2011) Screening candidate genes related to tenderness trait in Qinchuan cattle by genome array. Mol Biol Rep 38:2007–2014

    Article  PubMed  CAS  Google Scholar 

  28. Zapata I, Zerby HN, Wick M (2009) Functional proteomic analysis predicts beef tenderness and the tenderness differential. J Agric Food Chem 57:4956–4963

    Article  PubMed  CAS  Google Scholar 

  29. Sawdy JC, Kaiser SA, St-Pierre NR, Wick MP (2004) Myofibrillar 1-D fingerprints and myosin heavy chain MS analyses of beef loin at 36 h postmortem correlate with tenderness at 7 days. Meat Sci 67:421–426

    Article  PubMed  CAS  Google Scholar 

  30. Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95:14863

    Article  PubMed  CAS  Google Scholar 

  31. Zheng Q, Wang XJ (2008) GOEAST: a web-based software toolkit for Gene Ontology Enrichment Analysis. Nucleic Acids Res 36:358–363

    Article  Google Scholar 

  32. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408

    Article  PubMed  CAS  Google Scholar 

  33. Wang YH, Reverter A, Tan SH, De Jager N, Wang R, McWilliam SM, Cafe LM, Greenwood PL, Lehnert SA (2009) Gene expression patterns during intramuscular fat development in cattle. J Anim Sci 87:119–130

    Article  PubMed  CAS  Google Scholar 

  34. Perry D, Shorthose WR, Ferguson DM, Thompson JM (2001) Methods used in the CRC program for the determination of carcass yield and beef quality. Aust J Exp Agric 41:953–1040

    Article  Google Scholar 

  35. Hellerstein MK, Christiansen M, Kaempfer S, Kletke C, Wu K, Reid JS, Mulligan K, Hellerstein NS, Shackleton CH (1991) Measurement of de novo hepatic lipogenesis in humans using stable isotopes. J Clin Invest 87:1841

    Article  PubMed  CAS  Google Scholar 

  36. El-Kadi SW, Baldwin RL, Sunny NE, Owens SL, Bequette BJ (2006) Intestinal protein supply alters amino acid, but not glucose, metabolism by the sheep gastrointestinal tract. J Nutr 136:1261

    PubMed  CAS  Google Scholar 

  37. Boleman SJ, Boleman SL, Miller RK, Taylor JF, Cross HR, Wheeler TL, Koohmaraie M, Shackelford SD, Miller MF, West RL (1997) Consumer evaluation of beef of known categories of tenderness. J Anim Sci 75:1521–1524

    PubMed  CAS  Google Scholar 

  38. Behrends JM, Goodson KJ, Koohmaraie M, Shackelford SD, Wheeler TL, Morgan WW, Reagan JO, Gwartney BL, Wise JW, Savell JW (2005) Beef customer satisfaction: USDA quality grade and marination effects on consumer evaluations of top round steaks. J Anim Sci 83:662–670

    PubMed  CAS  Google Scholar 

  39. Wheeler TL, Shackelford SD, Koohmaraie M (1999) Tenderness classification of beef: IV. Effect of USDA quality grade on the palatability of “tender” beef longissimus when cooked well done. J Anim Sci 77:882–888

    PubMed  CAS  Google Scholar 

  40. George MH, Tatum JD, Dolezal HG, Morgan JB, Wise JW, Calkins CR, Gordon T, Reagan JO, Smith GC (1997) Comparison of USDA quality grade with Tendertec for the assessment of beef palatability. J Anim Sci 75:1538–1546

    PubMed  CAS  Google Scholar 

  41. Miller MF, Kerth CR, Wise JW, Lansdell JL, Stowell JE, Ramsey CB (1997) Slaughter plant location, USDA quality grade, external fat thickness, and aging time effects on sensory characteristics of beef loin strip steak. J Anim Sci 75:662–667

    PubMed  CAS  Google Scholar 

  42. Jeremiah LE (1970) Beef quality. I. Marblingas an indicator of palatability. Texas Agricultural Experiment Station Technical Bulletin 22, College Station, TX

  43. DeVol DL, Mckeith FK, Bechtel PJ, Novakofski J, Shanks RD, Carr TR (1988) Variation on composition and palatability traits and relationships between muscle characteristics abd palatability in a random sample of pork carcasses. J Anim Sci 66:385–395

    Google Scholar 

  44. Jeremiah LE (1983) The influence of inherent muscle quality upon the cooking losses from and palatability attributes of pork loin chops. In: Proceedings of Annual Meeting of the Western Section of the American Society of Animal Science, vol 34, pp 109–111

  45. Hoashi S, Hinenoya T, Tanaka A, Ohsaki H, Sasazaki S, Taniguchi M, Oyama K, Mukai F, Mannen H (2008) Association between fatty acid compositions and genotypes of FABP 4 and LXR-alpha in Japanese Black cattle. BMC Genet 9:84

    Article  PubMed  Google Scholar 

  46. Yang A, Larsen TW, Smith SB, Tume RK (1999) 9 desaturase activity in bovine subcutaneous adipose tissue of different fatty acid composition desaturase activity in bovine subcutaneous adipose tissue of different fatty acid composition. Lipids 34:971–978

    Article  PubMed  CAS  Google Scholar 

  47. Zhang L, Ge L, Parimoo S, Stenn K, Prouty SM (1999) Human stearoyl-CoA desaturase: alternative transcripts generated from a single gene by usage of tandem polyadenylation sites. Biochem J 340:255–264

    Article  PubMed  CAS  Google Scholar 

  48. Li J, Ding SF, Habib NA, Fermor BF, Wood CB, Gilmour RS (1994) Partial characterization of a cDNA for human stearoyl CoA desaturase and changes in its mRNA expression in some normal and malignant tissues. Int J Cancer 57:348–352

    Article  PubMed  CAS  Google Scholar 

  49. Jayakumar A, Tai MH, Huang WY, Al-Feel W, Hsu M, Abu-Elheiga L, Chirala SS, Wakil SJ (1995) Human fatty acid synthase: properties and molecular cloning. Proc Natl Acad Sci USA 92:8695–8699

    Article  PubMed  CAS  Google Scholar 

  50. Chakravarty B, Gu Z, Chirala SS, Wakil SJ, Quiocho FA (2004) Human fatty acid synthase: structure and substrate selectivity of the thioesterase domain. Proc Natl Acad Sci USA 101:15567–15572

    Article  PubMed  CAS  Google Scholar 

  51. Mannen H (2011) Identification and utilization of genes associated with beef qualities. Anim Sci J 82:1–7

    Article  PubMed  CAS  Google Scholar 

  52. Roy R, Ordovas L, Zaragoza P, Romero A, Moreno C, Altarriba J, Rodellar C (2006) Association of polymorphisms in the bovine FASN gene with milk-fat content. Anim Genet 37:215–218

    Article  PubMed  CAS  Google Scholar 

  53. Huff-Lonergan E, Baas TJ, Malek M, Dekkers JC, Prusa K, Rothschild MF (2002) Correlations among selected pork quality traits. J Anim Sci 80:617–627

    PubMed  CAS  Google Scholar 

  54. Bouley J, Chambon C, Picard B (2004) Mapping of bovine skeletal muscle proteins using two dimensional gel electrophoresis and mass spectrometry. Proteomics 4:1811–1824

    Article  PubMed  CAS  Google Scholar 

  55. Lubeseder-Martellato C, Guenzi E, Jörg A, Töpolt K, Naschberger E, Kremmer E, Zietz C, Tschachler E, Hutzler P, Schwemmle M (2002) Guanylate-binding protein-1 expression is selectively induced by inflammatory cytokines and is an activation marker of endothelial cells during inflammatory diseases. Am J Pathol 161:1749–1759

    Article  PubMed  CAS  Google Scholar 

  56. Guenzi E, Töpolt K, Lubeseder-Martellato C, Jörg A, Naschberger E, Benelli R, Albini A, Stürzl M (2003) The guanylate binding protein-1 GTPase controls the invasive and angiogenic capability of endothelial cells through inhibition of MMP-1 expression. EMBO J 22:3772–3782

    Article  PubMed  CAS  Google Scholar 

  57. Lu K, Lee MH, Hazard S, Brooks-Wilson A, Hidaka H, Kojima H, Ose L, Stalenhoef AFH, Mietinnen T, Bjorkhem I (2001) Two genes that map to the STSL locus cause sitosterolemia: genomic structure and spectrum of mutations involving sterolin-1 and sterolin-2, encoded by ABCG5 and ABCG8, respectively. Am J Hum Genet 69:278–290

    Article  PubMed  Google Scholar 

  58. Farke C, Meyer HHD, Bruckmaier RM, Albrecht C (2008) Differential expression of ABC transporters and their regulatory genes during lactation and dry period in bovine mammary tissue. J Dairy Res 75:406–414

    Article  PubMed  CAS  Google Scholar 

  59. Viturro E, Farke C, Meyer HHD, Albrecht C (2006) Identification, sequence analysis and mRNA tissue distribution of the bovine sterol transporters ABCG5 and ABCG8. J Dairy Sci 89:553–561

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The work was supported by China Scholarship Council (CSC), Maryland Agricultural Experiment Station (MAES) and Jorgensen Endowment Funds.

Author information

Authors and Affiliations

  1. College of Animal Science and Technology, Northwest A&F University, Yangling, Shaanxi, 712100, China

    Chunping Zhao & Linsen Zan

  2. Department of Animal & Avian Sciences, University of Maryland, College Park, MD, 20742, USA

    Chunping Zhao, Fei Tian, Ying Yu, Juan Luo, Qiong Hu, Brian J. Bequette, M. Scott Updike & Jiuzhou Song

  3. Department of Animal Breeding and Genetics, College of Animal Sciences, China Agricultural University, Beijing, 100193, China

    Ying Yu

  4. Bovine Functional Genomic Laboratory, Animal and Natural Resources Institute, USDA-Agricultural Research Service, Beltsville, MD, 20705, USA

    Ransom L. Baldwin VI & George Liu

Authors
  1. Chunping Zhao
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. Fei Tian
    View author publications

    You can also search for this author inPubMed Google Scholar

  3. Ying Yu
    View author publications

    You can also search for this author inPubMed Google Scholar

  4. Juan Luo
    View author publications

    You can also search for this author inPubMed Google Scholar

  5. Qiong Hu
    View author publications

    You can also search for this author inPubMed Google Scholar

  6. Brian J. Bequette
    View author publications

    You can also search for this author inPubMed Google Scholar

  7. Ransom L. Baldwin VI
    View author publications

    You can also search for this author inPubMed Google Scholar

  8. George Liu
    View author publications

    You can also search for this author inPubMed Google Scholar

  9. Linsen Zan
    View author publications

    You can also search for this author inPubMed Google Scholar

  10. M. Scott Updike
    View author publications

    You can also search for this author inPubMed Google Scholar

  11. Jiuzhou Song
    View author publications

    You can also search for this author inPubMed Google Scholar

Corresponding authors

Correspondence to Linsen Zan or Jiuzhou Song.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 327 kb)

Supplementary material 2 (DOCX 19 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhao, C., Tian, F., Yu, Y. et al. Muscle transcriptomic analyses in Angus cattle with divergent tenderness. Mol Biol Rep 39, 4185–4193 (2012). https://doi.org/10.1007/s11033-011-1203-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-011-1203-6

Keywords