Dynamic transcriptomic analysis in hircine longissimus dorsi muscle from fetal to neonatal development stages

Zhan, Siyuan; Zhao, Wei; Song, Tianzeng; Dong, Yao; Guo, Jiazhong; Cao, Jiaxue; Zhong, Tao; Wang, Linjie; Li, Li; Zhang, Hongping

doi:10.1007/s10142-017-0573-9

Original Article
Published: 09 October 2017

Dynamic transcriptomic analysis in hircine longissimus dorsi muscle from fetal to neonatal development stages

Siyuan Zhan ORCID: orcid.org/0000-0003-1244-2722¹^na1,
Wei Zhao¹^na1,
Tianzeng Song²,
Yao Dong¹,
Jiazhong Guo¹,
Jiaxue Cao¹,
Tao Zhong¹,
Linjie Wang¹,
Li Li¹ &
Hongping Zhang¹

Functional & Integrative Genomics volume 18, pages 43–54 (2018)Cite this article

743 Accesses
10 Citations
1 Altmetric
Metrics details

Abstract

Muscle growth and development from fetal to neonatal stages consist of a series of delicately regulated and orchestrated changes in expression of genes. In this study, we performed whole transcriptome profiling based on RNA-Seq of caprine longissimus dorsi muscle tissue obtained from prenatal stages (days 45, 60, and 105 of gestation) and neonatal stage (the 3-day-old newborn) to identify genes that are differentially expressed and investigate their temporal expression profiles. A total of 3276 differentially expressed genes (DEGs) were identified (Q value < 0.01). Time-series expression profile clustering analysis indicated that DEGs were significantly clustered into eight clusters which can be divided into two classes (Q value < 0.05), class I profiles with downregulated patterns and class II profiles with upregulated patterns. Based on cluster analysis, GO enrichment analysis found that 75, 25, and 8 terms to be significantly enriched in biological process (BP), cellular component (CC), and molecular function (MF) categories in class I profiles, while 35, 21, and 8 terms to be significantly enriched in BP, CC, and MF in class II profiles. KEGG pathway analysis revealed that DEGs from class I profiles were significantly enriched in 22 pathways and the most enriched pathway was Rap1 signaling pathway. DEGs from class II profiles were significantly enriched in 17 pathways and the mainly enriched pathway was AMPK signaling pathway. Finally, six selected DEGs from our sequencing results were confirmed by qPCR. Our study provides a comprehensive understanding of the molecular mechanisms during goat skeletal muscle development from fetal to neonatal stages and valuable information for future studies of muscle development in goats.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

References

Abe S, Soejima M, Iwanuma O, Saka H, Matsunaga S, Sakiyama K, Ide Y (2009) Expression of myostatin and follistatin in Mdx mice, an animal model for muscular dystrophy. Zool Sci 26:315–320. https://doi.org/10.2108/zsj.26.315
CAS Article PubMed Google Scholar
Apponi LH, Corbett AH, Pavlath GK (2011) RNA-binding proteins and gene regulation in myogenesis. Trends Pharmacol Sci 32:652–658. https://doi.org/10.1016/j.tips.2011.06.004
CAS Article PubMed PubMed Central Google Scholar
Bar-Joseph Z, Gitter A, Simon I (2012) Studying and modelling dynamic biological processes using time-series gene expression data. Nat Rev Genet 13:552–564. https://doi.org/10.1038/nrg3244
CAS Article PubMed Google Scholar
Bentzinger CF, Wang YX, Rudnicki MA (2012) Building muscle: molecular regulation of myogenesis. Cold Spring Harb Perspect Biol 4(2):a008342. https://doi.org/10.1101/cshperspect.a008342
Berkes CA, Tapscott SJ (2005) MyoD and the transcriptional control of myogenesis. Semin Cell Dev Biol 16:585–595. https://doi.org/10.1016/j.semcdb.2005.07.006
CAS Article PubMed Google Scholar
Boettner B, Van Aelst L (2009) Control of cell adhesion dynamics by Rap1 signaling. Curr Opin Cell Biol 21:684–693. https://doi.org/10.1016/j.ceb.2009.06.004
CAS Article PubMed PubMed Central Google Scholar
Braun T, Gautel M (2011) Transcriptional mechanisms regulating skeletal muscle differentiation, growth and homeostasis. Nat Rev Mol Cell Biol 12:349–361. https://doi.org/10.1038/nrm3118
CAS Article PubMed Google Scholar
Buckingham M, Rigby PW (2014) Gene regulatory networks and transcriptional mechanisms that control myogenesis. Dev Cell 28:225–238. https://doi.org/10.1016/j.devcel.2013.12.020
CAS Article PubMed Google Scholar
Cagnazzo M, te Pas MF, Priem J, de Wit AA, Pool MH, Davoli R, Russo V (2006) Comparison of prenatal muscle tissue expression profiles of two pig breeds differing in muscle characteristics. J Anim Sci 84:1–10. https://doi.org/10.2527/2006.8411
CAS Article PubMed Google Scholar
Dodson MV, Hausman GJ, Guan L, Du M, Rasmussen TP, Poulos SP, Mir P, Bergen WG, Fernyhough ME, McFarland DC, Rhoads RP, Soret B, Reecy JM, Velleman SG, Jiang Z (2010) Skeletal muscle stem cells from animals I. Basic cell biology. Int J Biol Sci 6:465–474. https://doi.org/10.7150/ijbs.6.465
Article PubMed PubMed Central Google Scholar
Dong Y, Xie M, Jiang Y, Xiao N, Du X, Zhang W, Tosser-Klopp G, Wang J, Yang S, Liang J, Chen W, Chen J, Zeng P, Hou Y, Bian C, Pan S, Li Y, Liu X, Wang W, Servin B, Sayre B, Zhu B, Sweeney D, Moore R, Nie W, Shen Y, Zhao R, Zhang G, Li J, Faraut T, Womack J, Zhang Y, Kijas J, Cockett N, Xu X, Zhao S, Wang J, Wang W (2013) Sequencing and automated whole-genome optical mapping of the genome of a domestic goat (Capra hircus). Nat Biotechnol 31:135–141. https://doi.org/10.1038/nbt.2478
CAS Article PubMed Google 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. J Anim Sci 88:E51–E60. https://doi.org/10.2527/jas.2009-2311
CAS Article PubMed Google Scholar
Du M, Yan X, Tong JF, Zhao J, Zhu MJ (2010b) Maternal obesity, inflammation, and fetal skeletal muscle development. Biol Reprod 82:4–12. https://doi.org/10.1095/biolreprod.109.077099
CAS Article PubMed Google Scholar
Duan C, Ren H, Gao S (2010) Insulin-like growth factors (IGFs), IGF receptors, and IGF-binding proteins: roles in skeletal muscle growth and differentiation. Gen Comp Endocrinol 167:344–351. https://doi.org/10.1016/j.ygcen.2010.04.009
CAS Article PubMed Google Scholar
Egerman MA, Glass DJ (2014) Signaling pathways controlling skeletal muscle mass. Crit Rev Biochem Mol Biol 49:59–68. https://doi.org/10.3109/10409238.2013.857291
CAS Article PubMed Google Scholar
Eng D, Ma H-Y, Gross MK, Kioussi C (2013) Gene networks during skeletal myogenesis. ISRN Dev Biol 2013:1–8. https://doi.org/10.1155/2013/348704
Article Google Scholar
Ernst J, Bar-Joseph Z (2006) STEM: a tool for the analysis of short time series gene expression data. BMC Bioinformatics 7:191. https://doi.org/10.1186/1471-2105-7-191
Article PubMed PubMed Central Google Scholar
Ernst J, Nau GJ, Bar-Joseph Z (2005) Clustering short time series gene expression data. Bioinformatics 21(Suppl 1):i159–i168. https://doi.org/10.1093/bioinformatics/bti1022
CAS Article PubMed Google Scholar
Estrella NL, Desjardins CA, Nocco SE, Clark AL, Maksimenko Y, Naya FJ (2015) MEF2 transcription factors regulate distinct gene programs in mammalian skeletal muscle differentiation. J Biol Chem 290:1256–1268. https://doi.org/10.1074/jbc.M114.589838
CAS Article PubMed Google Scholar
Feve B (2005) Adipogenesis: cellular and molecular aspects. Best Pract Res Clin Endocrinol Metab 19:483–499. https://doi.org/10.1016/j.beem.2005.07.007
CAS Article PubMed Google Scholar
Fu X, Zhao JX, Zhu MJ, Foretz M, Viollet B, Dodson MV, Du M (2013) AMP-activated protein kinase alpha1 but not alpha2 catalytic subunit potentiates myogenin expression and myogenesis. Mol Cell Biol 33:4517–4525. https://doi.org/10.1128/MCB.01078-13
CAS Article PubMed PubMed Central Google Scholar
Gnanalingham MG, Mostyn A, Symonds ME, Stephenson T (2005) Ontogeny and nutritional programming of adiposity in sheep: potential role of glucocorticoid action and uncoupling protein-2. Am J Physiol Regul Integr Comp Physiol 289:R1407–R1415. https://doi.org/10.1152/ajpregu.00375.2005
CAS Article PubMed Google Scholar
Jiang BH, Zheng JZ, Vogt PK (1998) An essential role of phosphatidylinositol 3-kinase in myogenic differentiation. Proc Natl Acad Sci U S A 95:14179–14183. https://doi.org/10.1073/pnas.95.24.14179
CAS Article PubMed PubMed Central Google Scholar
Jiang BH, Aoki M, Zheng JZ, Li J, Vogt PK (1999) Myogenic signaling of phosphatidylinositol 3-kinase requires the serine-threonine kinase Akt/protein kinase B. Proc Natl Acad Sci U S A 96:2077–2081. https://doi.org/10.1073/pnas.96.5.2077
CAS Article PubMed PubMed Central Google Scholar
Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14:R36. https://doi.org/10.1186/gb-2013-14-4-r36
Article PubMed PubMed Central Google Scholar
Kooistra MR, Dube N, Bos JL (2007) Rap1: a key regulator in cell-cell junction formation. J Cell Sci 120:17–22. https://doi.org/10.1242/jcs.03306
CAS Article PubMed Google Scholar
Langley B, Thomas M, Bishop A, Sharma M, Gilmour S, Kambadur R (2002) Myostatin inhibits myoblast differentiation by down-regulating MyoD expression. J Biol Chem 277:49831–49840. https://doi.org/10.1074/jbc.M204291200
CAS Article PubMed Google Scholar
Langmead B, Salzberg SL (2012) Fast gapped-read alignment with bowtie 2. Nat Methods 9:357–359. https://doi.org/10.1038/nmeth.1923
CAS Article PubMed PubMed Central Google Scholar
Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25. https://doi.org/10.1186/gb-2009-10-3-r25
Article PubMed PubMed Central Google Scholar
Lehnert SA, Reverter A, Byrne KA, Wang Y, Nattrass GS, Hudson NJ, Greenwood PL (2007) Gene expression studies of developing bovine longissimus muscle from two different beef cattle breeds. BMC Dev Biol 7:95. https://doi.org/10.1186/1471-213X-7-95
Article PubMed PubMed Central Google Scholar
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
CAS Article PubMed Google Scholar
Logan CY, Nusse R (2004) The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 20:781–810. https://doi.org/10.1146/annurev.cellbio.20.010403.113126
CAS Article PubMed Google Scholar
Lynch GS, Ryall JG (2008) Role of beta-adrenoceptor signaling in skeletal muscle: implications for muscle wasting and disease. Physiol Rev 88:729–767. https://doi.org/10.1152/physrev.00028.2007
CAS Article PubMed Google Scholar
Maere S, Heymans K, Kuiper M (2005) BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21:3448–3449. https://doi.org/10.1093/bioinformatics/bti551
CAS Article PubMed Google Scholar
Mavalli MD, DiGirolamo DJ, Fan Y, Riddle RC, Campbell KS, van Groen T, Frank SJ, Sperling MA, Esser KA, Bamman MM, Clemens TL (2010) Distinct growth hormone receptor signaling modes regulate skeletal muscle development and insulin sensitivity in mice. J Clin Invest 120:4007–4020. https://doi.org/10.1172/JCI42447
CAS Article PubMed PubMed Central Google Scholar
Moncaut N, Rigby PW, Carvajal JJ (2013) Dial M(RF) for myogenesis. FEBS J 280:3980–3990. https://doi.org/10.1111/febs.12379
CAS Article PubMed Google Scholar
Musi N, Goodyear LJ (2003) AMP-activated protein kinase and muscle glucose uptake. Acta Physiol Scand 178:337–345. https://doi.org/10.1046/j.1365-201X.2003.01168.x
CAS Article PubMed Google Scholar
Naya FJ, Olson E (1999) MEF2: a transcriptional target for signaling pathways controlling skeletal muscle growth and differentiation. Curr Opin Cell Biol 11:683–688. https://doi.org/10.1016/S0955-0674(99)00036-8
CAS Article PubMed Google Scholar
O'Neill HM (2013) AMPK and exercise: glucose uptake and insulin sensitivity. Diabetes Metab J 37:1–21. https://doi.org/10.4093/dmj.2013.37.1.1
Article PubMed PubMed Central Google Scholar
Otto A, Schmidt C, Luke G, Allen S, Valasek P, Muntoni F, Lawrence-Watt D, Patel K (2008) Canonical Wnt signalling induces satellite-cell proliferation during adult skeletal muscle regeneration. J Cell Sci 121:2939–2950. https://doi.org/10.1242/jcs.026534
CAS Article PubMed Google Scholar
Pauly M, Daussin F, Burelle Y, Li T, Godin R, Fauconnier J, Koechlin-Ramonatxo C, Hugon G, Lacampagne A, Coisy-Quivy M, Liang F, Hussain S, Matecki S, Petrof BJ (2012) AMPK activation stimulates autophagy and ameliorates muscular dystrophy in the mdx mouse diaphragm. Am J Pathol 181:583–592. https://doi.org/10.1016/j.ajpath.2012.04.004
CAS Article PubMed Google Scholar
Pizon V, Cifuentes-Diaz C, Mege RM, Baldacci G, Rieger F (1996) Expression and localization of RAP1 proteins during myogenic differentiation. Eur J Cell Biol 69:224–235
CAS PubMed Google Scholar
Ploner A (2015) Heatplus: Heatmaps with row and/or column covariates and colored clusters. R package version 2.18.0
Ren Y, Wu H, Ma Y, Yuan J, Liang H, Liu D (2014) Potential of adipose-derived mesenchymal stem cells and skeletal muscle-derived satellite cells for somatic cell nuclear transfer mediated transgenesis in Arbas Cashmere goats. PLoS One 9:e93583. https://doi.org/10.1371/journal.pone.0093583
Article PubMed PubMed Central Google Scholar
Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140. https://doi.org/10.1093/bioinformatics/btp616
CAS Article PubMed Google Scholar
Sanchez AM, Candau RB, Csibi A, Pagano AF, Raibon A, Bernardi H (2012) The role of AMP-activated protein kinase in the coordination of skeletal muscle turnover and energy homeostasis. Am J Physiol Cell Physiol 303:C475–C485. https://doi.org/10.1152/ajpcell.00125.2012
CAS Article PubMed Google Scholar
Schiaffino S, Dyar KA, Ciciliot S, Blaauw B, Sandri M (2013) Mechanisms regulating skeletal muscle growth and atrophy. FEBS J 280:4294–4314. https://doi.org/10.1111/febs.12253
CAS Article PubMed Google Scholar
Shin SC, Chung ER (2016) Identification of differentially expressed genes between high and low marbling score grades of the longissimus lumborum muscle in Hanwoo (Korean cattle). Meat Sci 121:114–118. https://doi.org/10.1016/j.meatsci.2016.05.018
CAS Article PubMed Google Scholar
Sun X, Li M, Sun Y, Cai H, Li R, Wei X, Lan X, Huang Y, Lei C, Chen H (2015) The developmental transcriptome landscape of bovine skeletal muscle defined by Ribo-Zero ribonucleic acid sequencing. J Anim Sci 93:5648–5658. https://doi.org/10.2527/jas.2015-9562
CAS Article PubMed Google Scholar
Sun L, Bai M, Xiang L, Zhang G, Ma W, Jiang H (2016) Comparative transcriptome profiling of longissimus muscle tissues from Qianhua Mutton Merino and Small Tail Han sheep. Sci Rep 6:33586. https://doi.org/10.1038/srep33586
CAS Article PubMed PubMed Central Google Scholar
Tang Z, Yang Y, Wang Z, Zhao S, Mu Y, Li K (2015) Integrated analysis of miRNA and mRNA paired expression profiling of prenatal skeletal muscle development in three genotype pigs. Sci Rep 5:15544. https://doi.org/10.1038/srep15544
CAS Article PubMed PubMed Central Google Scholar
Tong J, Zhu MJ, Underwood KR, Hess BW, Ford SP, Du M (2008) AMP-activated protein kinase and adipogenesis in sheep fetal skeletal muscle and 3T3-L1 cells. J Anim Sci 86:1296–1305. https://doi.org/10.2527/jas.2007-0794
CAS Article PubMed Google Scholar
Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511–515. https://doi.org/10.1038/nbt.1621
CAS Article PubMed PubMed Central Google Scholar
Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and cufflinks. Nat Protoc 7:562–578. https://doi.org/10.1038/nprot.2012.016
CAS Article PubMed PubMed Central Google Scholar
Tripathi AK, Patel AK, Shah RK, Patel AB, Shah TM, Bhatt VD, Joshi CG (2014) Transcriptomic dissection of myogenic differentiation signature in caprine by RNA-Seq. Mech Dev 132:79–92. https://doi.org/10.1016/j.mod.2014.01.001
CAS Article PubMed Google Scholar
Tureckova J, Wilson EM, Cappalonga JL, Rotwein P (2001) Insulin-like growth factor-mediated muscle differentiation: collaboration between phosphatidylinositol 3-kinase-Akt-signaling pathways and myogenin. J Biol Chem 276:39264–39270. https://doi.org/10.1074/jbc.M104991200
CAS Article PubMed Google Scholar
van Amerongen R, Berns A (2006) Knockout mouse models to study Wnt signal transduction. Trends Genet 22:678–689. https://doi.org/10.1016/j.tig.2006.10.001
Article PubMed Google Scholar
Wang YH, Zhang CL, Plath M, Fang XT, Lan XY, Zhou Y, Chen H (2015) Global transcriptional profiling of longissimus thoracis muscle tissue in fetal and juvenile domestic goat using RNA sequencing. Anim Genet 46:655–665. https://doi.org/10.1111/age.12338
CAS Article PubMed Google Scholar
Wenping H, Yuan Z, Jie S, Lijun Z, Zhezhi W (2011) De novo transcriptome sequencing in Salvia miltiorrhiza to identify genes involved in the biosynthesis of active ingredients. Genomics 98:272–279. https://doi.org/10.1016/j.ygeno.2011.03.012
Article PubMed Google Scholar
Xie C, Mao X, Huang J, Ding Y, Wu J, Dong S, Kong L, Gao G, Li CY, Wei L (2011) KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Res 39:W316–W322. https://doi.org/10.1093/nar/gkr483
CAS Article PubMed PubMed Central Google Scholar
Yan X, Zhu MJ, Dodson MV, Du M (2013) Developmental programming of fetal skeletal muscle and adipose tissue development. J Genomics 1:29–38. https://doi.org/10.7150/jgen.3930
Article PubMed PubMed Central Google Scholar
Zhao Y, Li J, Liu H, Xi Y, Xue M, Liu W, Zhuang Z, Lei M (2015) Dynamic transcriptome profiles of skeletal muscle tissue across 11 developmental stages for both Tongcheng and Yorkshire pigs. BMC Genomics 16:377. https://doi.org/10.1186/s12864-015-1580-7
Article PubMed PubMed Central Google Scholar

Download references

Acknowledgements

We thank all contributors of the present study. We also thank Mr. Cheng Zufu and his colleagues at Gene Denovo Ltd., Co (Guangzhou, China) for assistance in data processing.

Funding

This work was supported by the National Natural Science Foundation of China (31672402), Sichuan Province Science and Technology Support Program (2016NYZ0045), and the Tibet Autonomous Region Science and Technology Major Project (Z2016B01N04-06).

Author information

Siyuan Zhan and Wei Zhao contributed equally to this work.

Affiliations

Farm Animal Genetic Resources Exploration and Innovation Key Laboratory of Sichuan Province, Sichuan Agricultural University, Chengdu, 611130, People’s Republic of China
Siyuan Zhan, Wei Zhao, Yao Dong, Jiazhong Guo, Jiaxue Cao, Tao Zhong, Linjie Wang, Li Li & Hongping Zhang
Tibet Academy of Agricultural & Animal Husbandry Science, Institute of Animal Science, Lhasa, 850000, People’s Republic of China
Tianzeng Song

Authors

Siyuan Zhan
View author publications
You can also search for this author in PubMed Google Scholar
Wei Zhao
View author publications
You can also search for this author in PubMed Google Scholar
Tianzeng Song
View author publications
You can also search for this author in PubMed Google Scholar
Yao Dong
View author publications
You can also search for this author in PubMed Google Scholar
Jiazhong Guo
View author publications
You can also search for this author in PubMed Google Scholar
Jiaxue Cao
View author publications
You can also search for this author in PubMed Google Scholar
Tao Zhong
View author publications
You can also search for this author in PubMed Google Scholar
Linjie Wang
View author publications
You can also search for this author in PubMed Google Scholar
Li Li
View author publications
You can also search for this author in PubMed Google Scholar
Hongping Zhang
View author publications
You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Li Li or Hongping Zhang.

Ethics declarations

Availability of data

The raw data we obtained from RNA-Seq are available in the National Center for Biotechnology Information (NCBI) Sequence Read Archive (SRA) (accession number: SRR3567144).

Electronic supplementary material

Table S1

Summary of RNA-seq data and reads mapped to the Capra hircus reference genome. (XLSX 13 kb)

Table S2

List of identified DEGs from pairwise comparisons. (XLSX 553 kb)

Table S3

Significantly enriched GO terms for ClassIprofiles (profiles 9, 3, 0, and 12) with down-regulated patterns. (XLSX 54 kb)

Table S4

Significantly enriched GO terms for ClassIIprofiles (profiles 16, 25, 13, and 24) with up-regulated patterns. (XLSX 22 kb)

Table S5

Significantly enriched KEGG pathways for ClassIprofiles (profiles 9, 3, 0, and 12) with down-regulated patterns. (XLSX 13 kb)

Table S6

Significantly enriched KEGG pathways for ClassIIprofiles (profiles 16, 25, 13, and 24) with up-regulated patterns. (XLSX 11 kb)

Table S7

Primers used in the qPCR analysis. (XLSX 9 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Zhan, S., Zhao, W., Song, T. et al. Dynamic transcriptomic analysis in hircine longissimus dorsi muscle from fetal to neonatal development stages. Funct Integr Genomics 18, 43–54 (2018). https://doi.org/10.1007/s10142-017-0573-9

Download citation

Received: 11 August 2017
Accepted: 11 September 2017
Published: 09 October 2017
Issue Date: January 2018
DOI: https://doi.org/10.1007/s10142-017-0573-9

Keywords

Muscle development
RNA-Seq
Differential expression
Goat