Genome-wide association studies, meta-analyses and derived gene network for meat quality and carcass traits in pigs
Darlene Ana S. Duarte A , Marina Rufino S. Fortes B , Marcio de Souza Duarte A , Simone E. F. Guimarães A , Lucas L. Verardo A , Renata Veroneze A , André Mauric F. Ribeiro A , Paulo Sávio Lopes A , Marcos Deon V. de Resende C and Fabyano Fonseca e Silva A D
+ Author Affiliations
- Author Affiliations
A Department of Animal Science, Universidade Federal de Viçosa (UFV), Viçosa, MG, Brazil.
B School of Chemistry and Molecular Bioscience, University of Queensland, Brisbane, Queensland, Australia.
C Embrapa Florestas/Universidade Federal de Viçosa (UFV), Colombo, PR, Brazil.
D Corresponding author. Email: fabyanofonseca@ufv.br
Animal Production Science 58(6) 1100-1108 https://doi.org/10.1071/AN16018
Submitted: 8 January 2016 Accepted: 15 November 2016 Published: 21 March 2017
Abstract
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.
Additional keywords: biological pathways, post-GWAS, SNP-derived gene networks.
References
Arakaki N, Kita T, Shibata H, Higuti T (2007) Cell-surface H+-ATP synthase as a potential molecular target for anti-obesity drugs. FEBS Letters 581, 3405–3409.| Cell-surface H+-ATP synthase as a potential molecular target for anti-obesity drugs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXnslWgtr8%3D&md5=736a1974494b1144199c7b6c58a822cfCAS |
Band GO, Guimarães SEF, Lopes PS, Schierholt AS, Silva KM, Pires AV, Benevenuto Júnior AA, Gomide LAM (2005a) Relationship between the Porcine Stress Syndrome gene and pork quality traits of F2 pigs resulting from divergent crosses. Genetics and Molecular Biology 28, 88–91.
| Relationship between the Porcine Stress Syndrome gene and pork quality traits of F2 pigs resulting from divergent crosses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXkt1Gis7o%3D&md5=f8ec5ce0354713646e4926cd8a7b349cCAS |
Band GO, Guimarães SEF, Lopes PS, Peixoto JO, Faria DA, Pires AV, Figueiredo FC, Nascimento CS, Gomide LAM (2005b) Relationship between the Porcine Stress Syndrome gene and carcass and performance traits in F2 pigs resulting from divergent crosses. Genetics and Molecular Biology 28, 92–96.
| Relationship between the Porcine Stress Syndrome gene and carcass and performance traits in F2 pigs resulting from divergent crosses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXkt1Gis7g%3D&md5=27d9193bc90bbc0255018cfa731fd8e2CAS |
Davoli R, Braglia S (2007) Molecular approaches in pig breeding to improve meat quality. Briefings in Functional Genomics & Proteomics 6, 313–321.
de Campos CF, Lopes MS, Silva FF, Veroneze R, Knol EF, Lopes PS, Gumarães SEF (2015) Genomic selection for boar taint compounds and carcass traits in a commercial pig population. Livestock Science 174, 10–17.
| Genomic selection for boar taint compounds and carcass traits in a commercial pig population.Crossref | GoogleScholarGoogle Scholar |
Du M, Tong J, Zhao J, Underwood KR, Zhu M, Ford SP, Nathanielsz PW (2010a) Fetal programming of skeletal muscle development in ruminant animals. Journal of Animal Science 88, E51–E60.
| Fetal programming of skeletal muscle development in ruminant animals.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3c3pslOisw%3D%3D&md5=441ff97fb240fff66aa9025ee20cb0bcCAS |
Du M, Yin J, Zhu MJ (2010b) Cellular signaling pathways regulating the initial stage of adipogenesis and marbling of skeletal muscle. Meat Science 86, 103–109.
| Cellular signaling pathways regulating the initial stage of adipogenesis and marbling of skeletal muscle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXos1CnsLo%3D&md5=2ef694b1b685364c4b7057616b4f6a46CAS |
Du M, Huang Y, Das AK, Yang Q, Duarte MS, Dodson MV, Zhu MJ (2013) Meat science and muscle biology symposium: manipulating mesenchymal progenitor cell differentiation to optimize performance and carcass value of beef cattle. Journal of Animal Science 91, 1419–1427.
| Meat science and muscle biology symposium: manipulating mesenchymal progenitor cell differentiation to optimize performance and carcass value of beef cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmsFKnu7o%3D&md5=aff0b403a2aae302459ab59b7ca1c7eeCAS |
Duarte MS, Paulino PV, Fonseca MA, Diniz LL, Cavali J, Serão NV, Gomide LA, Reis SF, Cox RB (2011) Influence of dental carcass maturity on carcass traits and meat quality of Nellore bulls. Meat Science 88, 441–446.
| Influence of dental carcass maturity on carcass traits and meat quality of Nellore bulls.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M3psVSkuw%3D%3D&md5=a55ffd9e8091e707ba6f98e505bb9007CAS |
Duarte MS, Paulino PV, Das AK, Wei S, Serao NV, Fu X, Harris SM, Dodson MV, Du M (2013) Enhancement of adipogenesis and fibrogenesis in skeletal muscle of Wagyu compared with Angus cattle. Journal of Animal Science 91, 2938–2946.
| Enhancement of adipogenesis and fibrogenesis in skeletal muscle of Wagyu compared with Angus cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXpvFCru70%3D&md5=6af0fa12b4e9c5e18c51f5e9b4fdd821CAS |
Duarte MS, Gionbelli MP, Paulino PVR, Serao NVL, Nascimento CS, Botelho ME, Martins TS, Filho SCV, Dodson MV, Guimaraes SEF, Du M (2014) Maternal overnutrition enhances mRNA expression of adipogenic markers and collagen deposition in skeletal muscle of beef cattle fetuses. Journal of Animal Science 92, 3846–3854.
| Maternal overnutrition enhances mRNA expression of adipogenic markers and collagen deposition in skeletal muscle of beef cattle fetuses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhslamurzE&md5=5fa0846a13d91d2281575a518172e160CAS |
Evangelou E, Ioannidis JP (2013) Meta-analysis methods for genome-wide association studies and beyond. Nature Reviews Genetics 14, 379–389.
Fortes MRS, Reverter A, Zhanga Y, Collisa E, Nagaraj SH, Jonssona NN, Prayaga KC, Barrisa W, Hawkena RJ (2010) Association weight matrix for the genetic dissection of puberty in beef cattle. Proceedings of the National Academy of Sciences of the United States of America 107, 13642–13647.
| Association weight matrix for the genetic dissection of puberty in beef cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVWmtrjE&md5=75c566a197cedf7340b1994f9a4731e1CAS |
Gao SZ, Zhao SM (2009) Physiology, affecting factors and strategies for control of pig meat intramuscular fat. Recent Patents on Food, Nutrition & Agriculture 1, 59–74.
| Physiology, affecting factors and strategies for control of pig meat intramuscular fat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjtVyju7g%3D&md5=bcb7f5be84e4b8dfb2e0fbf3b6e2724bCAS |
Große-Brinkhaus C, Jonas E, Buschbell H, Phatsara C, Tesfaye D, Jungst H, Looft C, Schellander K, Tholen E (2010) Epistatic QTL pairs associated with meat quality and carcass composition traits in a porcine Duroc x Pietrain population. Genetics, Selection, Evolution. 42, 39
| Epistatic QTL pairs associated with meat quality and carcass composition traits in a porcine Duroc x Pietrain population.Crossref | GoogleScholarGoogle Scholar |
Guo Y, Hou L, Zhang X, Huang M, Mao H, Chen H, Ma J, Chen C, Ai H, Ren J, Huang L (2015) A meta analysis of genome-wide association studies for limb bone lengths in four pig populations. BMC Genetics 16, 95
Habier D, Fernando RL, Dekkers JCM (2009) Genomic selection using low-density marker panels. Genetics 182, 343–353.
| Genomic selection using low-density marker panels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlvFCmt7c%3D&md5=337c2e64577eb55b24f39d33cd6bda1cCAS |
Hidalgo AM, Lopes PS, Paixão DM, Silva FF, Bastiaansen JWM, Paiva SR, Faria DA, Guimarães SEF (2013) Fine mapping and single nucleotide polymorphism effects estimation on pig chromosomes 1, 4, 7, 8, 17 and X. Genetics and Molecular Biology 36, 511–519.
| Fine mapping and single nucleotide polymorphism effects estimation on pig chromosomes 1, 4, 7, 8, 17 and X.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXit12htb0%3D&md5=d85fe4c9a0d711bd852bf4043cf2fc53CAS |
Hocquette JF, Gondret F, Baéza E, Médale F, Jurie C, Pethick DW (2010) Intramuscular fat content in meat-producing animals: development, genetic and nutritional control, and identification of putative markers. Animal 4, 303–319.
| Intramuscular fat content in meat-producing animals: development, genetic and nutritional control, and identification of putative markers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1Sls7rM&md5=db5d9c3d146a29e4fffd5b294706de95CAS |
Hu Z-L, Park CA, Wu X-L, Reecy JM (2013) Animal QTLdb: an improved database tool for livestock animal QTL/association data dissemination in the post-genome era. Nucleic Acids Research 41, D871–D879.
Jennen DGJ, Brings AD, Liu G, Jungst H, Tholen E, Jonas E, Tesfaye D, Schellander K, Phatsara C (2007) Genetic aspects concerning drip loss and water-holding capacity of porcine meat. Journal of Animal Breeding and Genetics 124, 2–11.
| Genetic aspects concerning drip loss and water-holding capacity of porcine meat.Crossref | GoogleScholarGoogle Scholar |
Kaimal V, Bardes EE, Tabar SC, Jegga AG, Aronow BJ (2010) ToppCluster: a multiple gene list feature analyzer for comparative enrichment clustering and network-based dissection of biological systems. Nucleic Acids Research 38, W96–W102.
Keller P, Petrie JT, De Rose P, Gerin I, Wright WS, Chiang SH, Nielsen AR, Fischer CP, Pedersen BK, MacDougald OA (2008) Fat-specific protein 27 regulates storage of triacylglycerol. The Journal of Biological Chemistry 283, 14355–14365.
| Fat-specific protein 27 regulates storage of triacylglycerol.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlvFyjsrk%3D&md5=d50d651e1e1c11e0f94caf19e40bbc7dCAS |
Kojic S, Radojkovic D, Faulkner G (2011) Muscle ankyrin repeat proteins: their role in striated muscle function in health and disease. Critical Reviews in Clinical Laboratory Sciences 48, 269–294.
| Muscle ankyrin repeat proteins: their role in striated muscle function in health and disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1KrsbbK&md5=ab0aef2e02c11a4b847294c5f775e5f6CAS |
Leroy MC, Perroud J, Darbellay B, Bernheim L, Konig S (2013) Epidermal growth factor receptor down-regulation triggers human myoblast differentiation. PLoS One 8, e71770
| Epidermal growth factor receptor down-regulation triggers human myoblast differentiation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtlCkt7zM&md5=3d284970dd7bbda33a79d630540f4538CAS |
Li JJ, Ferry RJ, Diao S, Xue B, Bahouth SW, Liao FF (2015) Nedd4 haploinsufficient mice display moderate insulin resistance, enhanced lipolysis, and protection against high-fat diet-induced obesity. Endocrinology 156, 1283–1291.
| Nedd4 haploinsufficient mice display moderate insulin resistance, enhanced lipolysis, and protection against high-fat diet-induced obesity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXls1KmtLo%3D&md5=c22e8e2e8ec66d7f18c830c90435e483CAS |
Ma J, Ren J, Guo Y, Duan Y, Ding N, Zhou L, Li L, Yan X, Yang K, Huang L, Song Y, Xie J, Milan D, Huang L (2009) Genome-wide identification of quantitative trait loci for carcass composition and meat quality in a large-scale White Duroc x Chinese Erhualian resource population. Animal Genetics 40, 637–647.
| Genome-wide identification of quantitative trait loci for carcass composition and meat quality in a large-scale White Duroc x Chinese Erhualian resource population.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1Mnksl2hsQ%3D%3D&md5=660f705cc5803757663170f8539cf8c4CAS |
Ma G, Wang H, Li Y, Cui L, Cui Y, Li Q, Li K, Zhao B (2013) Cloning, expression, and bioinformatics analysis of the sheep CARP gene. Molecular and Cellular Biochemistry 378, 29–37.
| Cloning, expression, and bioinformatics analysis of the sheep CARP gene.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjvFeisrg%3D&md5=9b0b1f20381d81fea2969f5520c27fc0CAS |
Mathelier A, Zhao X, Zhang AW, Parcy F, Worsley-Hunt R, Arenillas DJ, Buchman S, Chen C, Chou A, Ienasescu H, Lim J, Shyr C, Tan G, Zhou M, Lenhard B, Sandelin A, Wasserman WW (2014) JASPAR 2014: an extensively expanded and updated open-access database of transcription factor binding profiles. Nucleic Acids Research 42, D142–D147.
| JASPAR 2014: an extensively expanded and updated open-access database of transcription factor binding profiles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXoslak&md5=26946ce2c7e4fae58ef530768d45809eCAS |
Miar Y, Plastow GS, Moore SS, Manafiazar G, Charagu P, Kemp RA, Van Haandel B, Huisman AE, Zhang CY, McKay RM, Bruce HL, Wang Z (2014) Genetic and phenotypic parameters for carcass and meat quality traits in commercial crossbred pigs. Journal of Animal Science 92, 2869–2884.
| Genetic and phenotypic parameters for carcass and meat quality traits in commercial crossbred pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtFyrt77L&md5=35f49b17b5d425ee8c3b978cc3046965CAS |
Mosesson Y, Chetrit D, Schley L, Berghoff J, Ziv T, Carvalho S, Milanezi F, Admon A, Schmitt F, Ehrlich M, Yarden Y (2009) Monoubiquitinylation regulates endosomal localization of Lst2, a negative regulator of EGF receptor signaling. Developmental Cell 16, 687–698.
| Monoubiquitinylation regulates endosomal localization of Lst2, a negative regulator of EGF receptor signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXps1ymsL0%3D&md5=8e5f3a7d12fd184d63b4fab1eda4ec43CAS |
Nonneman DJ, Shackelford SD, King DA, Wheeler TL, Wiedmann RT, Snelling WM, Rohrer GA (2013) Genome-wide association of meat quality traits and tenderness in swine. Journal of Animal Science 91, 4043–4050.
| Genome-wide association of meat quality traits and tenderness in swine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsVOlsbzE&md5=ddc075871d0f20c6c44e1c058e135e09CAS |
Ponsuksili S, Murani E, Phatsara C, Schwerin M, Schellander K, Wimmers K (2009) Porcine muscle sensory attributes associate with major changes in gene networks involving CAPZB, ANKRD1, and CTBP2. Functional & Integrative Genomics 9, 455–471.
| Porcine muscle sensory attributes associate with major changes in gene networks involving CAPZB, ANKRD1, and CTBP2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1CmtrzO&md5=8127d065a1b205b91504119007b1518aCAS |
R Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at http://www.R-project.org/ [Verified 21 September 2013]
Ramayo-Caldas Y, Ballester M, Fortes MR, Esteve-Codina A, Castelló A, Noguera JL, Fernández AI, Pérez-Enciso M, Reverter A, Folch JM (2014) From SNP co-association to RNA co-expression: Novel insights into gene networks for intramuscular fatty acid composition in porcine. BMC Genomics 15, 232
| From SNP co-association to RNA co-expression: Novel insights into gene networks for intramuscular fatty acid composition in porcine.Crossref | GoogleScholarGoogle Scholar |
Ramos AM, Crooijmans RP, Affara NA, Amaral AJ, Archibald AL, Beever JE, Bendixen C, Churcher C, Clark R, Dehais P (2009) Design of a high density SNP genotyping assay in the pig using SNPs identified and characterized by next generation sequencing technology. PLoS One 4, e6524
| Design of a high density SNP genotyping assay in the pig using SNPs identified and characterized by next generation sequencing technology.Crossref | GoogleScholarGoogle Scholar |
Rescan PY, Ralliere C (2010) A Sox5 gene is expressed in the myogenic lineage during trout embryonic development. The International Journal of Developmental Biology 54, 913–918.
| A Sox5 gene is expressed in the myogenic lineage during trout embryonic development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpsFWjtLk%3D&md5=732aea637ce7fe35760c14550d95a2b6CAS |
Reverter A, Chan EK (2008) Combining partial correlation and an information theory approach to the reversed engineering of gene co-expression networks. Bioinformatics 24, 2491–2497.
| Combining partial correlation and an information theory approach to the reversed engineering of gene co-expression networks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht12gtbvF&md5=b220f5d3299751c3e8f7e3a67072aa13CAS |
Riazi AM, Lee H, Hsu C, Van Arsdell G (2005) CSX/Nkx2.5 modulates differentiation of skeletal myoblasts and promotes differentiation into neuronal cells in vitro. The Journal of Biological Chemistry 280, 10716–10720.
| CSX/Nkx2.5 modulates differentiation of skeletal myoblasts and promotes differentiation into neuronal cells in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXit1ertrk%3D&md5=008a61f2f61cf6261b80e8e2f273b1dfCAS |
Safran M, Dalah I, Alexander J, Rosen N, Stein TI, Shmoish M, Nativ N, Bahir I, Doniger T, Krug H, Sirota-Madi A, Olender T, Golan Y, Stelzer G, Harel A, Lancet D (2010) GeneCards Version 3: the human gene integrator. Database 2010, baq020
| GeneCards Version 3: the human gene integrator.Crossref | GoogleScholarGoogle Scholar |
Silva KM, Bastiaansen JW, Knol EF, Merks JW, Lopes PS, Guimaraes SE, van Arendonk JA (2011) Meta-analysis of results from quantitative trait loci mapping studies on pig chromosome 4. Animal Genetics 42, 280–292.
| Meta-analysis of results from quantitative trait loci mapping studies on pig chromosome 4.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MvpsVCqug%3D%3D&md5=2ffc07e8ebc84739949134b850dabd15CAS |
Spittal MJ, Pirkis J, Gurrin LC (2015) Meta-analysis of incidence rate data in the presence of zero events. BMC Medical Research Methodology 15, 42
| Meta-analysis of incidence rate data in the presence of zero events.Crossref | GoogleScholarGoogle Scholar |
Struchalin M, Aulchenko Y (2014) MetABEL: meta-analysis of genome-wide SNP association results. R package version 0.2–0. Available at http://CRAN.R-project.org/package=MetABEL [Verified 21 May 2014]
Strucken EM, Schmitt AO, Bergfeld U, Jurke I, Reissmann M, Brockmann GA (2014) Genomewide study and validation of markers associated with production traits in German Landrace boars. Journal of Animal Science 92, 1939–1944.
| Genomewide study and validation of markers associated with production traits in German Landrace boars.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXot12isbc%3D&md5=14574f71306fd36a9a24009b59b86714CAS |
Touzet H, Varré J-S (2007) Efficient and accurate P-value computation for Position Weight Matrices. Algorithms for Molecular Biology 2, 15
| Efficient and accurate P-value computation for Position Weight Matrices.Crossref | GoogleScholarGoogle Scholar |
Uimari P, Tapio M (2011) Extent of linkage disequilibrium and effective population size in Finnish Landrace and Finnish Yorkshire pig breeds. Journal of Animal Science 89, 609–614.
| Extent of linkage disequilibrium and effective population size in Finnish Landrace and Finnish Yorkshire pig breeds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjtlSmtr4%3D&md5=6e53190b081f4a976ea2d3769ace7146CAS |
Urs S, Smith C, Campbell B, Saxton AM, Taylor J, Zhang B, Snoddy J, Jones Voy B, Moustaid-Moussa N (2004) Gene expression profiling in human preadipocytes and adipocytes by microarray analysis. The Journal of Nutrition 134, 762–770.
Verardo LL, Silva FF, Varona L, Resende MDV, Bastiaansen JWM, Lopes PS, Guimarães SEF (2015) Bayesian GWAS and network analysis revealed new candidate genes for number of teats in pigs. Journal of Applied Genetics 56, 123–132.
| Bayesian GWAS and network analysis revealed new candidate genes for number of teats in pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtlarsLbI&md5=53236b2f509604e512be1fdb7a1aaac4CAS |
Veroneze R, Bastiaansen JWM, Knol EF, Guimarães SEF, Harlizius B, Lopes MS, Lopes OS (2014) Linkage disequilibrium patterns and persistence of phase in purebred and crossbred pig (Sus scrofa) populations. BMC Genetics 15, 126, 1–9
| Linkage disequilibrium patterns and persistence of phase in purebred and crossbred pig (Sus scrofa) populations.Crossref | GoogleScholarGoogle Scholar |
Zammit PS, Relaix F, Nagata Y, Ruiz AP, Collins CA, Partridge TA, Beauchamp JR (2006) Pax7 and myogenic progression in skeletal muscle satellite cells. Journal of Cell Science 119, 1824–1832.
| Pax7 and myogenic progression in skeletal muscle satellite cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XlsVOmsrk%3D&md5=99fac2b728a5722e74d7bc59aa1c3873CAS |
Zhang Y, Zan L, Wang H (2011) Screening candidate genes related to tenderness trait in Qinchuan cattle by genome array. Molecular Biology Reports 38, 2007–2014.
| Screening candidate genes related to tenderness trait in Qinchuan cattle by genome array.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlenu7g%3D&md5=d33cdc94ad00ba2283b45d15f36eef25CAS |
Zou Y, Evans S, Chen J, Kuo HC, Harvey RP, Chien KR (1997) CARP, a cardiac ankyrin repeat protein, is downstream in the Nkx2–5 homeobox gene pathway. Development 124, 793–804.
