[en] A large number of quantitative trait loci (QTL) for meat quality and carcass traits has been reported in pigs over the past 20 years. However, few QTL have been validated and the biological meaning of the genes associated to these QTL has been underexploited. In this context, a meta-analysis was performed to compare the significant markers with meta-QTL previously reported in literature. Genome association studies were performed for 12 traits, from which 144 SNPs were found out to be significant (P < 0.05). They were validated in the meta-analysis and used to build the Association Weight Matrix, a matrix framework employed to investigate co-association of pairwise SNP across phenotypes enabling to derive a gene network. A total of 45 genes were selected from the Association Weight Matrix analysis, from which 25 significant transcription factors were identified and used to construct the networks associated to meat quality and carcass traits. These networks allowed the identification of key transcription factors, such as SOX5 and NKX2–5, gene–gene interactions (e.g. ATP5A1, JPH1, DPT and NEDD4) and pathways related to the regulation of adipose tissue metabolism and skeletal muscle development. Validated SNPs and knowledge of key genes driving these important industry traits might assist future strategies in pig breeding.
Disciplines :
Animal production & animal husbandry
Author, co-author :
Souza Duarte, Darlene Ana ; Université de Liège - ULiège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Ingénierie des productions animales et nutrition
Salinas Fortes, Marina Rufino
Duarte, Marcio de Souza
Facioni Guimarães, Simone Eliza
Lima Verardo, Lucas
Veroneze, Renata
Frossard Ribeiro, André Mauric
Sávio Lopes, Paulo
Vilela de Resende, Marcos Deon
Fonseca e Silva, Fabyano
Language :
English
Title :
Genome-wide association studies, meta-analyses and derived gene network for meat quality and carcass traits in pigs
Publication date :
March 2017
Journal title :
Animal Production Science
ISSN :
1836-0939
eISSN :
1836-5787
Publisher :
Commonwealth Scientific and Industrial Research Organization Publishing, Clayton, Australia
Arakaki, N., Kita, T., Shibata, H., Higuti, T., Cell-surface H+-ATP synthase as a potential molecular target for anti-obesity drugs (2007) FEBS Letters, 581, pp. 3405-3409
Band, G.O., Guimarães, S.E.F., Lopes, P.S., Schierholt, A.S., Silva, K.M., Pires, A.V., Benevenuto Júnior, A.A., Gomide, L.A.M., Relationship between the Porcine Stress Syndrome gene and pork quality traits of F2 pigs resulting from divergent crosses (2005) Genetics and Molecular Biology, 28, pp. 88-91
Band, G.O., Guimarães, S.E.F., Lopes, P.S., Peixoto, J.O., Faria, D.A., Pires, A.V., Figueiredo, F.C., Gomide, L.A.M., Relationship between the Porcine Stress Syndrome gene and carcass and performance traits in F2 pigs resulting from divergent crosses (2005) Genetics and Molecular Biology, 28, pp. 92-96
Davoli, R., Braglia, S., Molecular approaches in pig breeding to improve meat quality (2007) Briefings in Functional Genomics & Proteomics, 6, pp. 313-321
De Campos, C.F., Lopes, M.S., Silva, F.F., Veroneze, R., Knol, E.F., Lopes, P.S., Gumarães, S.E.F., Genomic selection for boar taint compounds and carcass traits in a commercial pig population (2015) Livestock Science, 174, pp. 10-17
Du, M., Tong, J., Zhao, J., Underwood, K.R., Zhu, M., Ford, S.P., Nathanielsz, P.W., Fetal programming of skeletal muscle development in ruminant animals (2010) Journal of Animal Science, 88, pp. E51-E60
Du, M., Yin, J., Zhu, M.J., Cellular signaling pathways regulating the initial stage of adipogenesis and marbling of skeletal muscle (2010) MeatScience, 86, pp. 103-109
Du, M., Huang, Y., Das, A.K., Yang, Q., Duarte, M.S., Dodson, M.V., Zhu, M.J., Meat science and muscle biology symposium: Manipulating mesenchymal progenitor cell differentiation to optimize performance and carcass value of beef cattle (2013) Journal of Animal Science, 91, pp. 1419-1427
Duarte, M.S., Paulino, P.V., Fonseca, M.A., Diniz, L.L., Cavali, J., Serão, N.V., Gomide, L.A., Cox, R.B., Influence of dental carcass maturity on carcass traits and meat quality of Nellore bulls (2011) Meat Science, 88, pp. 441-446
Duarte, M.S., Paulino, P.V., Das, A.K., Wei, S., Serao, N.V., Fu, X., Harris, S.M., Du, M., Enhancement of adipogenesis and fibrogenesis in skeletal muscle of Wagyu compared with Angus cattle (2013) Journal of Animal Science, 91, pp. 2938-2946
Duarte, M.S., Gionbelli, M.P., Paulino, P.V.R., Serao, N.V.L., Nascimento, C.S., Botelho, M.E., Martins, T.S., Du, M., Maternal overnutrition enhances mRNA expression of adipogenic markers and collagen deposition in skeletal muscle of beef cattle fetuses (2014) Journal of Animal Science, 92, pp. 3846-3854
Evangelou, E., Ioannidis, J.P., Meta-analysis methods for genome-wide association studies and beyond (2013) Nature Reviews Genetics, 14, pp. 379-389
Fortes, M.R.S., Reverter, A., Zhanga, Y., Collisa, E., Nagaraj, S.H., Jonssona, N.N., Prayaga, K.C., Hawkena, R.J., Association weight matrix for the genetic dissection of puberty in beef cattle (2010) Proceedings of the National Academy of Sciences of the United States of America, 107, pp. 13642-13647
Gao, S.Z., Zhao, S.M., Physiology, affecting factors and strategies for control of pig meat intramuscular fat (2009) Recent Patents on Food, Nutrition& Agriculture, 1, pp. 59-74
Große-Brinkhaus, C., Jonas, E., Buschbell, H., Phatsara, C., Tesfaye, D., Jungst, H., Looft, C., Tholen, E., Epistatic QTL pairs associated with meat quality and carcass composition traits in a porcine Duroc x Pietrain population (2010) Genetics, Selection, Evolution, 42, p. 39
Guo, Y., Hou, L., Zhang, X., Huang, M., Mao, H., Chen, H., Ma, J., Huang, L., A meta analysis of genome-wide association studies for limb bone lengths in four pig populations (2015) BMC Genetics, 16, p. 95
Habier, D., Fernando, R.L., Dekkers, J.C.M., Genomic selection using low-density marker panels (2009) Genetics, 182, pp. 343-353
Hidalgo, A.M., Lopes, P.S., Paixão, D.M., Silva, F.F., Bastiaansen, J.W.M., Paiva, S.R., Faria, D.A., Guimarães, S.E.F., Fine mapping and single nucleotide polymorphism effects estimation on pig chromosomes 1, 4, 7, 8, 17 and X (2013) Genetics and Molecular Biology, 36, pp. 511-519
Hocquette, J.F., Gondret, F., Baéza, E., Médale, F., Jurie, C., Pethick, D.W., Intramuscular fat content in meat-producing animals: Development, genetic and nutritional control, and identification of putative markers (2010) Animal, 4, pp. 303-319
Hu, Z.-L., Park, C.A., Wu, X.-L., Reecy, J.M., Animal QTLdb: An improved database tool for livestock animal QTL/association data dissemination in the post-genome era (2013) Nucleic Acids Research, 41, pp. D871-D879
Jennen, D.G.J., Brings, A.D., Liu, G., Jungst, H., Tholen, E., Jonas, E., Tesfaye, D., Phatsara, C., Genetic aspects concerning drip loss and water-holding capacity of porcine meat (2007) Journal of Animal Breeding and Genetics, 124, pp. 2-11
Kaimal, V., Bardes, E.E., Tabar, S.C., Jegga, A.G., Aronow, B.J., ToppCluster: A multiple gene list feature analyzer for comparative enrichment clustering and network-based dissection of biological systems (2010) Nucleic Acids Research, 38, pp. W96-W102
Keller, P., Petrie, J.T., De Rose, P., Gerin, I., Wright, W.S., Chiang, S.H., Nielsen, A.R., MacDougald, O.A., Fat-specific protein 27 regulates storage of triacylglycerol (2008) The Journal of Biological Chemistry, 283, pp. 14355-14365
Kojic, S., Radojkovic, D., Faulkner, G., Muscle ankyrin repeat proteins: Their role in striated muscle function in health and disease (2011) Critical Reviews in Clinical Laboratory Sciences, 48, pp. 269-294
Ma, J., Ren, J., Guo, Y., Duan, Y., Ding, N., Zhou, L., Li, L., Huang, L., Genome-wide identification of quantitative trait loci for carcass composition and meat quality in a largescale White Duroc x Chinese Erhualian resource population (2009) Animal Genetics, 40, pp. 637-647
Ma, G., Wang, H., Li, Y., Cui, L., Cui, Y., Li, Q., Li, K., Zhao, B., Cloning, expression, and bioinformatics analysis of the sheep CARP gene (2013) Molecular and Cellular Biochemistry, 378, pp. 29-37
Mathelier, A., Zhao, X., Zhang, A.W., Parcy, F., Worsley-Hunt, R., Arenillas, D.J., Buchman, S., Wasserman, W.W., JASPAR 2014: An extensively expanded and updated open-access database of transcription factor binding profiles (2014) Nucleic Acids Research, 42, pp. D142-D147
Miar, Y., Plastow, G.S., Moore, S.S., Manafiazar, G., Charagu, P., Kemp, R.A., Van Haandel, B., Wang, Z., Genetic and phenotypic parameters for carcass and meat quality traits in commercial crossbred pigs (2014) Journal of Animal Science, 92, pp. 2869-2884
Mosesson, Y., Chetrit, D., Schley, L., Berghoff, J., Ziv, T., Carvalho, S., Milanezi, F., Yarden, Y., Monoubiquitinylation regulates endosomal localization of Lst2, a negative regulator of EGF receptor signaling (2009) Developmental Cell, 16, pp. 687-698
Nonneman, D.J., Shackelford, S.D., King, D.A., Wheeler, T.L., Wiedmann, R.T., Snelling, W.M., Rohrer, G.A., Genome-wide association of meat quality traits and tenderness in swine (2013) Journal of Animal Science, 91, pp. 4043-4050
Ponsuksili, S., Murani, E., Phatsara, C., Schwerin, M., Schellander, K., Wimmers, K., Porcine muscle sensory attributes associate with major changes in gene networks involving CAPZB, ANKRD1, and CTBP2 (2009) Functional & Integrative Genomics, 9, pp. 455-471
(2013) R: A Language and Environment for Statistical Computing, , http://www.R-project.org/, R Core Team, R Foundation for Statistical Computing, Vienna, Austria, [Verified 21 September 2013]
Ramayo-Caldas, Y., Ballester, M., Fortes, M.R., Esteve-Codina, A., Castelló, A., Noguera, J.L., Fernández, A.I., Folch, J.M., FromSNPco-association toRNAco-expression: Novel insights into gene networks for intramuscular fatty acid composition in porcine (2014) BMC Genomics, 15, p. 232
Ramos, A.M., Crooijmans, R.P., Affara, N.A., Amaral, A.J., Archibald, A.L., Beever, J.E., Bendixen, C., Dehais, P., Design of a high density SNP genotyping assay in the pig using SNPs identified and characterized by next generation sequencing technology (2009) PLoS One, 4, p. e6524
Rescan, P.Y., Ralliere, C., A Sox5 gene is expressed in the myogenic lineage during trout embryonic development (2010) The International Journal of Developmental Biology, 54, pp. 913-918
Reverter, A., Chan, E.K., Combining partial correlation and an information theory approach to the reversed engineering of gene co-expression networks (2008) Bioinformatics, 24, pp. 2491-2497
Riazi, A.M., Lee, H., Hsu, C., Van Arsdell, G., CSX/Nkx2.5 modulates differentiation of skeletal myoblasts and promotes differentiation into neuronal cells in vitro (2005) The Journal of Biological Chemistry, 280, pp. 10716-10720
Safran, M., Dalah, I., Alexander, J., Rosen, N., Stein, T.I., Shmoish, M., Nativ, N., Lancet, D., GeneCards Version 3: The human gene integrator (2010) Database, 2010, p. baq020
Silva, K.M., Bastiaansen, J.W., Knol, E.F., Merks, J.W., Lopes, P.S., Guimaraes, S.E., Van Arendonk, J.A., Meta-analysis of results from quantitative trait loci mapping studies on pig chromosome 4 (2011) Animal Genetics, 42, pp. 280-292
Spittal, M.J., Pirkis, J., Gurrin, L.C., Meta-analysis of incidence rate data in the presence of zero events (2015) BMC Medical Research Methodology, 15, p. 42
Struchalin, M., Aulchenko, Y., MetABEL:meta-analysis of genome-wide SNP association results (2014) R Package Version 0.2-0, , http://CRAN.R-project.org/package=MetABEL, [Verified 21 May 2014]
Strucken, E.M., Schmitt, A.O., Bergfeld, U., Jurke, I., Reissmann, M., Brockmann, G.A., Genomewide study and validation of markers associated with production traits in German Landrace boars (2014) Journal of Animal Science, 92, pp. 1939-1944
Touzet, H., Varré, J.-S., Efficient and accurate P-value computation for Position Weight Matrices (2007) Algorithms for Molecular Biology, 2, p. 15
Uimari, P., Tapio, M., Extent of linkage disequilibrium and effective population size in Finnish Landrace and Finnish Yorkshire pig breeds (2011) Journal of Animal Science, 89, pp. 609-614
Urs, S., Smith, C., Campbell, B., Saxton, A.M., Taylor, J., Zhang, B., Snoddy, J., Moustaid-Moussa, N., Gene expression profiling in human preadipocytes and adipocytes by microarray analysis (2004) The Journal of Nutrition, 134, pp. 762-770
Verardo, L.L., Silva, F.F., Varona, L., Resende, M.D.V., Bastiaansen, J.W.M., Lopes, P.S., Guimarães, S.E.F., Bayesian GWAS and network analysis revealed new candidate genes for number of teats in pigs (2015) Journal of Applied Genetics, 56, pp. 123-132
Veroneze, R., Bastiaansen, J.W.M., Knol, E.F., Guimarães, S.E.F., Harlizius, B., Lopes, M.S., Lopes, O.S., Linkage disequilibrium patterns and persistence of phase in purebred and crossbred pig (Sus scrofa) populations (2014) BMC Genetics 15, 126, pp. 1-9
Zammit, P.S., Relaix, F., Nagata, Y., Ruiz, A.P., Collins, C.A., Partridge, T.A., Beauchamp, J.R., Pax7 and myogenic progression in skeletal muscle satellite cells (2006) Journal of Cell Science, 119, pp. 1824-1832
Zhang, Y., Zan, L., Wang, H., Screening candidate genes related to tenderness trait in Qinchuan cattle by genome array (2011) Molecular Biology Reports, 38, pp. 2007-2014
Zou, Y., Evans, S., Chen, J., Kuo, H.C., Harvey, R.P., Chien, K.R., CARP, a cardiac ankyrin repeat protein, is downstream in the Nkx2-5 homeoboxgene pathway (1997) Development, 124, pp. 793-804