Dissection of beef quality phenotypes using a myogenin network-anchored systems biology approach
A. Reverter A B , E. K. F. Chan A , S. A. Lehnert A , W. Barris A , S. M. McWilliam A , B. P. Dalrymple A and W. Barendse AA Cooperative Research Centre for Beef Genetic Technologies, CSIRO Livestock Industries, Queensland Bioscience Precinct, 306 Carmody Road, St. Lucia, Qld 4067, Australia.
B Corresponding author. Email: Toni.Reverter-Gomez@csiro.au
Australian Journal of Experimental Agriculture 48(8) 1053-1061 https://doi.org/10.1071/EA08052
Submitted: 23 January 2008 Accepted: 5 May 2008 Published: 14 July 2008
Abstract
In order to uncover genes with transcriptional activity linked to various beef quality phenotypes of interest, we designed a systems biology approach. We focussed on traits representing the three major categories of growth and development, fat depots and meat quality phenotypes. We proceeded by linking bovine gene expression data derived from 147 microarray hybridisation experiments and high density marker data from 9260 single nucleotide polymorphisms (SNP) on 189 steers. The individuals in the genotyping study were unrelated to the samples used for expression profiling. The linkage was performed by anchoring these data to a gene network for myogenin (MYOG), a muscle-specific transcription factor essential for the development of skeletal muscle. This approach was able to identify and estimate the strength of the relationship between the statistical association of a SNP to a phenotype of interest with the transcriptional activity of genes in the network. The genes from the MYOG-centred network that were significantly associated with the largest number of meat quality traits were PDLIM3, CALM1 and CRYAB. Among our findings, a novel association between desmin and meat colour points to an alternative biochemical basis for meat colour differences involving costameric structures and their previously reported relationship with tenderness. These newly generated hypotheses can help formulate sound research to further illuminate the genetic architecture of beef quality phenotypes.
Abzhanov A,
Kuo WP,
Hartmann C,
Grant BR,
Grant PR, Tabin CJ
(2006) The calmodulin pathway and evolution of elongated beak morphology in Darwin’s finches. Nature 442, 563–567.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Andersson L, Georges M
(2004) Domestic-animal genomics: deciphering the genetics of complex traits. Nature Reviews. Genetics 5, 202–212.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Barendse W,
Reverter A,
Bunch RJ,
Harrison BE,
Barris W, Thomas MB
(2007a) A validated whole-genome association study of efficient food conversion in cattle. Genetics 176, 1893–1905.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Barendse W,
Harrison BE,
Hawken RJ,
Ferguson DM,
Thompson JM,
Thomas MB, Bunch RJ
(2007b) Epistasis between calpain 1 and its inhibitor calpastatin within breeds of cattle. Genetics 176, 1893–1905.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Bernard C,
Cassar-Malek I,
LeCunff M,
Dubroeucq H,
Renand G, Hocquette JF
(2007) New indicators of beef sensory quality revealed by expression of specific genes. Journal of Agricultural and Food Chemistry 55, 5229–5237.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Blais A,
Tsikitis M,
Acosta-Alvear D,
Sharan R,
Kluger Y, Dynlacht BD
(2005) An initial blueprint for myogenic differentiation. Genes & Development 19, 553–569.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Cao Y,
Kumar RM,
Penn BH,
Berkes CA,
Kooperberg C,
Boyer LA,
Young RA, Tapscott SJ
(2006) Global and gene-specific analyses show dis-tinct roles for Myod and Myog at a common set of promoters. The EMBO Journal 25, 502–511.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Casas E,
White SN,
Wheeler TL,
Shackelford SD,
Koohmaraie M,
Riley DG,
Chase CC,
Johnson DD, Smith TPL
(2006) Effects of calpastatin and µ-calpain markers in beef cattle on tenderness traits. Journal of Animal Science 84, 520–525.
|
CAS |
Crossref |
PubMed |
Cassar-Malek I,
Passelaigue F,
Bernard C,
Leger J, Hocquette JF
(2007) Target genes of myostatin loss-of-function in muscles of late bovine fetuses. BMC Genomics 8, 63.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Chen SL,
Dowhan DH,
Hosking BM, Muscat GE
(2000) The steroid receptor coactivator, GRIP-1, is necessary for MEF-2C-dependent gene expression and skeletal muscle differentiation. Genes & Development 15, 1209–1228.
Ciobanu DC,
Bastiaansen JWM,
Lonergan SM,
Thomsen H,
Dekkers JCM,
Plastow GS, Rothschild MF
(2004) New alleles in calpastatin gene are associated with meat quality traits in pigs. Journal of Animal Science 82, 2829–2839.
|
CAS |
PubMed |
Ferguson DM,
Warner RD,
Walker PJ, Knee B
(2007) Effect of cattle marketing method on beef quality and palatability. Australian Journal of Experimental Agriculture 47, 774–781.
| Crossref | GoogleScholarGoogle Scholar |
Friday BB,
Mitchell PO,
Kegley KM, Pavlath GK
(2003) Calcineurin initiates skeletal muscle differentiation by activating MEF2 and MyoD. Differentiation 71, 217–227.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Georgiadis V,
Stewart HJ,
Pollard HJ,
Tavsanoglu Y,
Prasad R,
Horwood J,
Deltour L,
Goldring K,
Poirier F, Lawrence-Watt DJ
(2007) Lack of galectin-1 results in defects in myoblast fusion and muscle regeneration. Developmental Dynamics 236, 1014–1024.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
González JR,
Armengol LL,
Solé X,
Guinó E,
Mercader JM,
Estivill X, Moreno V
(2007) SNPassoc: an R package to perform whole genome association studies. Bioinformatics (Oxford, England) 23, 654–655.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hardenbol P,
Yu F,
Belmont J,
Mackenzie J, Bruckner C , et al.
(2005) Highly multiplexed molecular inversion probe genotyping: over 10,000 targeted SNPs genotyped in a single tube assay. Genome Research 15, 269–275.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Hasty P,
Bradley A,
Morris H,
Edmondson DJ,
Venuti JM,
Olson EN, Klein WH
(1993) Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene. Nature 364, 501–506.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Hong F, Breitling R
(2008) A comparison of meta-analysis methods for detecting differentially expressed genes in microarray experiments. Bioinformatics (Oxford, England) 24, 374–382.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Johnston DJ,
Reverter A,
Burrow HM,
Oddy VH, Robinson DL
(2003a) Genetic and phenotypic characterization of animal, carcass, and meat quality traits from temperate and tropically adapted beef breeds. 1. Animal measures. Australian Journal of Agricultural Research 54, 107–118.
| Crossref | GoogleScholarGoogle Scholar |
Johnston DJ,
Reverter A,
Ferguson DM,
Thompson JM, Burrow HM
(2003b) Genetic and phenotypic characterization of animal, carcass, and meat quality traits from temperate and tropically adapted beef breeds. 3. Meat quality traits. Australian Journal of Agricultural Research 54, 135–147.
| Crossref | GoogleScholarGoogle Scholar |
Klaavuniemi T,
Kelloniemi A, Ylanne J
(2004) The ZASP-like motif in actinin-associated LIM protein is required for interaction with the alpha-actinin rod and for targeting to the muscle Z-line. The Journal of Biological Chemistry 279, 26402–26410.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Koohmaraie M,
Doumit ME, Wheeler TL
(1996) Meat toughening does not occur when rigor shortening is prevented. Journal of Animal Science 74, 2935–2942.
|
CAS |
PubMed |
Lehnert SA,
Byrne KA, Wang YH
(2004) Development and application of a bovine cDNA microarray for expression profiling of muscle and adipose tissue. Australian Journal of Experimental Agriculture 44, 1127–1133.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Lehnert SA,
Byrne KA,
Reverter A,
Nattrass GS,
Greenwood PL,
Wang YH,
Hudson NJ, Harper GS
(2006) Gene expression profiling of bovine skeletal muscle in response to and during recovery from chronic and severe undernutrition. Journal of Animal Science 84, 3239–3250.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Lehnert SA,
Reverter A,
Byrne KA,
Wang YH,
Nattrass GS,
Hudson NJ, Greenwood PL
(2007) Gene expression studies of developing bovine muscle from two different beef cattle breeds. BMC Developmental Biology 7, 95.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Makambi KH
(2003) Weighted inverse chi-square method for correlated significance tests. Journal of Applied Statistics 30, 225–234.
| Crossref | GoogleScholarGoogle Scholar |
McLachlan GJ,
Bean RW, Peel D
(2002) A mixture model-based approach to clustering of microarray expression data. Bioinformatics (Oxford, England) 18, 413–422.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
McLachlan GJ,
Bean RW, Jones LBT
(2005) Using mixture models to detect differentially expressed genes. Australian Journal of Experimental Agriculture 45, 859–866.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
McLachlan GJ,
Bean RW, Jones LBT
(2006) A simple implementation of a normal mixture approach to differential gene expression in multiclass microarryas. Bioinformatics (Oxford, England) 22, 1608–1615.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Morris CA,
Cullen NG,
Hickey SM,
Dobbie PM,
Veenvliet BA,
Manley TR,
Pitchford WS,
Kruk ZA,
Bottema CDK, 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.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Nabeshima Y,
Hanaoka K,
Hayasaka M,
Esumi E,
Li S,
Nonaka I, Nabeshima Y
(1993) Myogenin gene disruption results in perinatal lethality because of severe muscle defect. Nature 364, 532–535.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
O’Neill A,
Williams MW,
Resneck WG,
Milner DJ,
Capetanaki Y, Block RJ
(2002) Sarcolemmal organisation in skeletal muscle lacking desmin: evidence for cytokeratins associated with the membrane skeleton at costameres. Molecular Biology of the Cell 13, 2347–2359.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Pyne S,
Futher B, Skiena S
(2006) Meta-analysis based on control of false discovery rate: combining yeast ChIP-chip datasets. Bioinformatics (Oxford, England) 22, 2516–2522.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Reverter A,
Johnston DJ,
Perry D,
Goddard ME, Burrow HM
(2003a) Genetic and phenotypic characterization of animal, carcass, and meat quality traits from temperate and tropically adapted beef breeds. 2. Abattoir carcass traits. Australian Journal of Agricultural Research 54, 119–138.
| Crossref | GoogleScholarGoogle Scholar |
Reverter A,
Johnston DJ,
Ferguson DM,
Perry D,
Goddard ME,
Burrow HM,
Oddy VH,
Thompson JM, Bindon BM
(2003b) Genetic and phenotypic characterization of animal, carcass, and meat quality traits from temperate and tropically adapted beef breeds. 2. Abattoir carcass traits. Australian Journal of Agricultural Research 54, 149–158.
| Crossref | GoogleScholarGoogle Scholar |
Reverter A,
Wang YH,
Byrne KA,
Tan SK,
Harper GS, Lehnert SA
(2004) Joint analysis of multiple cDNA microarray studies via multivariate mixed-models applied to genetic improvement of beef cattle. Journal of Animal Science 82, 3430–3439.
|
CAS |
PubMed |
Reverter A,
Hudson NJ,
Wang YH,
Tan SK, Barris W , et al.
(2006) A gene coexpression network for bovine skeletal muscle inferred from microarray data. Physiological Genomics 28, 76–83.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Robinson DL, Oddy VH
(2004) Genetic parameters for feed efficiency, fatness, muscle area and feeding behaviour of feedlot finished beef cattle. Livestock Production Science 90, 255–270.
| Crossref | GoogleScholarGoogle Scholar |
Schadt EE,
Lamb J,
Yang X,
Zhu J, Edwards S , et al.
(2005) An integrative genomics approach to infer causal associations between gene expression and disease. Nature Genetics 37, 710–717.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Sudre K,
Leroux C,
Pietu G,
Cassar-Malek I,
Petit E,
Listrat A,
Auffray B,
Picard B,
Martin P, Hocquette JF
(2003) Transcriptome analysis of two bovine muscles during ontogenesis. Journal of Biochemistry 133, 745–756.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Tan SK,
Reverter A,
Wang YH,
Byrne KA,
McWilliam SM, Lehnert SA
(2006) Gene expression profiling of bovine in vitro adipogenesis using a cDNA microarray. Functional & Integrative Genomics 6, 235–249.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Upton W,
Burrow HM,
Dundon A,
Robinson DL, Farrell EB
(2001) CRC breeding program design, measurements and database: methods that underpin CRC research results. Australian Journal of Experimental Agriculture 41, 943–952.
| Crossref | GoogleScholarGoogle Scholar |
Vicart P,
Caron A,
Guicheney P,
Li Z, Prevost MC , et al.
(1998) A missense mutation in the alphaB-crystallin chaperone gene causes a desmin-related myopathy. Nature Genetics 20, 92–95.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Wang YH,
Byrne KA,
Reverter A,
Harper GS,
Taniguchi M,
McWilliam SM,
Mannen H,
Oyama K, Lehnert SA
(2005a) Transcriptional profiling of skeletal muscle tissue from two breeds of cattle. Mammalian Genome 16, 201–210.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Wang YH,
Reverter A,
Mannen H,
Taniguchi M,
Harper GS,
Oyama K,
Byrne KA,
Oka A,
Tsuji S, Lehnert SA
(2005b) Transcriptional profiling of muscle tissue in growing Japanese Black cattle to identify genes involved with the development of intramuscular fat. Australian Journal of Experimental Agriculture 45, 809–820.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Womack JE
(2005) Advances in livestock genomics: Opening the barn door. Genome Research 15, 1699–1705.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Xu Q,
Yu L,
Liu L,
Cheung CF,
Li X,
Yee SP,
Yang XJ, Wu Z
(2002) p38 mitogen-activated protein kinase-, calcium- calmodulin-dependent protein kinase-, and calcineurin-mediated signaling pathways transcriptionally regulate myogenin expression. Molecular Biology of the Cell 13, 1940–1952.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Zaykin DV,
Zhivotovsky LA,
Westfall PH, Weir BS
(2002) Truncated product method for combining P-values. Genetic Epidemiology 22, 170–185.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Zhu J,
Wiener MC,
Zhang C,
Fridman A,
Minch E,
Lum PY,
Sachs JR, Schadt EE
(2007) Increasing the power to detect causal associations by combining genotypic and expression data in segregating populations. PLoS Computational Biology 3, e69.
| Crossref | GoogleScholarGoogle Scholar | PubMed |