Skip to main content
Log in

Characterisation of Single Nucleotide Polymorphisms and Haplotypes of MSTN Associated with Growth Traits in European Sea Bass (Dicentrarchus labrax)

  • Research
  • Published:
Marine Biotechnology Aims and scope Submit manuscript

Abstract

The myostatin (MSTN) gene, known as growth differentiation factor-8 (GDF-8), is a member of the transforming growth factor-β (TGF-β) superfamily and plays a specific inhibitory role during the critical phases of skeletal muscle mass development in vertebrates. This study was conducted to investigate MSTN polymorphisms in harvest size European sea bass reared in Turkey. Nine single nucleotide polymorphisms (SNPs) and two indels were identified in exons 1–3 of MSTN in the European sea bass population The associations between the g.16612A indel located in intron 1 and standard length were significant. The MSTN g.15252 T > A locus in intron 2 was significantly related to the total weight, fillet weight and standard length (P < 0.05). The relationship between the g.14873C > T locus in exon 3 of MSTN and standard height, head length, body length, pre-anal length, abdominal length, post-anal length and head width was significant (P < 0.05). According to the results of the haplotype analysis, two haplogroup and eight haplotype combinations were detected in the population. The haplogroup 2 had significant associations with all measured growth traits (P < 0.05). Thus, SNPs and haplotypes identified in this study could be useful for European sea bass breeding and marker-assisted selection.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Data Availability

The data analyzed in this study are presented in this article and the supplementary information file. The raw data supporting the conclusion can be shared by request.

References

  • Agnihotry S, Pathak RK, Singh DB, Tiwari A, Hussain I (2022) Protein structure prediction. Editor(s): Dev Bukhsh Singh, Rajesh Kumar Pathak, Bioinformatics. Academic Press 177–188. https://doi.org/10.1016/B978-0-323-89775-4.00023-7

  • Ahad WA, Andrabi M, Beigh SA, Bhat RA, Shah RA (2017) Applications of myostatin (MSTN) gene in the livestock animals and humans: a review. Int J Curr Microbiol App Sci 6:1807–1811

    Article  Google Scholar 

  • Barrett JC, Fry B, Maller J, Daly MJ (2005) Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21:263–265

    Article  PubMed  CAS  Google Scholar 

  • Bertotto D, Poltronieri C, Negrato E, Richard J, Pascoli F, Simontacchi C, Radaelli G (2011) Whole body cortisol and expression of HSP70, IGF-I and MSTN in early development of sea bass subjected to heat shock. Gen Comp Endocrinol 174:44–50

    Article  PubMed  CAS  Google Scholar 

  • Bignell CW, Malau-Aduli AEO, Nichols PD, McCulloch R, Kijas JW (2010) East Friesian sheep carry a Myostatin allele known to cause muscle hypertrophy in other breeds. Anim Genet 41:445–446

    Article  PubMed  CAS  Google Scholar 

  • Boman IA, Våge DI (2009) An insertion in the coding region of the myostatin (MSTN) gene affects carcass conformation and fatness in the Norwegian Spælsau (Ovis aries). BMC Res Not 2:1–5

    Google Scholar 

  • Cheng L, Sun YH (2015) Polymorphisms in a myostatin gene and associations with growth in a hybrid of Culter alburnus and Ancherythroculter nigrocauda. Genet Mol Res 14:5615–5620

    Article  ADS  PubMed  CAS  Google Scholar 

  • Chung S, Perry RP (1989) Importance of introns for expression of mouse ribosomal protein gene rpL32. Mol Cell Biol 9:2075–2082

    PubMed  PubMed Central  CAS  Google Scholar 

  • Clop A, Marcq F, Takeda H, Pirottin D, Tordoir X, Bibe´ B, Bouix J, Caiment, F, Elsen JM, Eychenne F et al (2006) A mutation creating a potential illegitimate microRNA target site in the myostatin gene affects muscularity in sheep. Nat Genet 38:813–818

  • De-Santis C, Evans BS, Smith-Keune C, Jerry DR (2008) Molecular characterization, tissue expression and sequence variability of the barramundi (Lates calcarifer) myostatin gene. BMC Genom 9:1–15

    Article  Google Scholar 

  • Elkatatny NA, Elbialy ZI, El-Nahas AF, Mahmoud S (2016) Characterization of myostatin gene in Nile Tilapia (Oreochromis niloticus), the possible association of BsmI-exon 2 polymorphism with its growth. Am J Life Sci 4:82–86

    Article  CAS  Google Scholar 

  • FAO (2022) Food and Agriculture Organization. Fisheries and Aquaculture Department. https://www.fao.org/fishery/en/statistics/software/fishstatj/en. Accessed 30 Nov 2022

  • Feng X, Yu X, Tong J (2014) Novel single nucleotide polymorphisms of the insulin-like growth factor-I gene and their associations with growth traits in common carp (Cyprinus carpio L.). Int J Mol Sci 15:22471–22482

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gabriel SB, Schaffner SF, Nguyen H, Moore JM, Roy J, Blumenstiel B, Higgins J, Defelice M, Lochner A, Faggart M, Liu-Cordero SN, Rotimi C, Adeyemo A, Cooper R, Ward R, Lander ES, Daly MJ, Altshuler D (2002) The structure of haplotype blocks in the human genome. Science 296:2225–2229

    Article  ADS  PubMed  CAS  Google Scholar 

  • Gao Y, Dai Z, Shi C, Zhai G, Jin X, He J, Lou Q, Yin Z (2016) Depletion of myostatin b promotes somatic growth and lipid metabolism in zebrafish. Front Endocrinol 7:88

    Article  Google Scholar 

  • Garikipati DK, Gahr SA, Roalson EH, Rodgers BD (2007) Characterization of rainbow trout myostatin-2 genes (rtMSTN-2a and-2b): genomic organization, differential expression, and pseudogenization. Endocrinology 148:2106–2115

    Article  PubMed  CAS  Google Scholar 

  • Garcia de Leon FJ, Chikhi L, Bonhomme F (1997) Microsatellite polymorphism and population subdivision in natural populations of European sea bass Dicentrarchus labrax (Linnaeus, 1758). Molecular Ecol 6:51–62

    Article  Google Scholar 

  • Garikipati DK, Gahr SA, Rodgers BD (2006) Identification, characterization, and quantitative expression analysis of rainbow trout myostatin-1a and myostatin-1b genes. J Endocrinol 190:879–888

    Article  PubMed  CAS  Google Scholar 

  • Gökçek EÖ, Işık R, Karahan B, Gamsız K (2020) Genetic variation of insulin-like growth factor II (IGF-II) gene and its associations with growth traits in European sea bass (Dicentrarchus labrax). Turkish J Fish Aquat Sci 20:541–548

    Google Scholar 

  • Grobet L, Martin LJR, Poncelet D, Pirrotin D, Brouwers B, Riquet J et al (1997) A deletion in the bovine myostatin gene causes the double-muscled phenotype in cattle. Nat Genet 17:4

    Article  Google Scholar 

  • Guo L, Li L, Zhang S, Guo X, Zhang G (2011) Novel polymorphisms in the myostatin gene and their association with growth traits in a variety of bay scallop. Argopecten Irradians Anim Genet 42:339–340

    Article  PubMed  CAS  Google Scholar 

  • Hall T, Biosciences I, Carlsbad CJGBB (2011) BioEdit: an important software for molecular biology. GERF Bull Biosci 2:60–61

    Google Scholar 

  • Işık R, Özdil F, Meral S (2022) Evaluation of variation on Myostatin (MSTN) gene of Turkish donkey populations in Thrace Region of Turkey. Tekirdağ Ziraat Fak Der 19:426–434

    Article  Google Scholar 

  • Janssen K, Chavanne H, Berentsen P, Komen H (2017) Impact of selective breeding on European aquaculture. Aquaculture 472:8–16

    Article  Google Scholar 

  • Kishimoto K, Washio Y, Yoshiura Y, Toyoda A, Ueno T, Fukuyama H, Kato K, Kinoshita M (2018) Production of a breed of red sea bream Pagrus major with an increase of skeletal muscle mass and reduced body length by genome editing with CRISPR/Cas9. Aquaculture 495:415–427

    Article  CAS  Google Scholar 

  • Komar AA (2007) Silent SNPs: impact on gene function and phenotype. Pharmacogenomics 8:1075–1080

    Article  PubMed  CAS  Google Scholar 

  • Kong S, Zhou Z, Zhou T, Zhao J, Chen L, Lin H, Pu F, Ke P, Bai H, Xu P (2020) Genome-wide association study of body shape-related traits in large yellow croaker (Larimichthys crocea). Mari Biotechnol 22:631–643

    Article  CAS  Google Scholar 

  • Lei M, Luo C, Peng X, Fang M, Nie Q, Zhang D, Yang G, Zhang X (2007) Polymorphism of growth-correlated genes associated with fatness and muscle fiber traits in chickens. Poult Sci 86:835–842

    Article  PubMed  CAS  Google Scholar 

  • Li H, Fan J, Liu S, Yang Q, MuG HC (2012) Characterization of a myostatin gene (MSTN1) from spotted halibut (Verasper variegatus) and association between its promoter polymorphism and individual growth performance. Comp Biochem Physiol B, Biochem Mol Biol 161:315–322

    Article  PubMed  CAS  Google Scholar 

  • Li S, Zhou Z, Dong Y, Sun H, Gao S, Chen Z, Yang A, Liu W, Wang Q (2016) Molecular characterization, expression analysis of the myostatin gene and its association with growth traits in sea cucumber (Apostichopus japonicus). Comp Biochem Physiol. B, Biochem Mol Biol 201:12–20

    Article  CAS  Google Scholar 

  • Liu L, Yu X, Tong J (2012) Molecular characterization of myostatin (MSTN) gene and association analysis with growth traits in the bighead carp (Aristichthys nobilis). Mol Biol Rep 39:9211–9221

    Article  PubMed  CAS  Google Scholar 

  • Louro B, Kuhl H, Tine M, de Koning DJ, Batargias C, Volckaert FA, Reinhardt R, Canario VMA, Power MD (2016) Characterization and refinement of growth related quantitative trait loci in European sea bass (Dicentrarchus labrax) using a comparative approach. Aquaculture 455:8–21

    Article  CAS  Google Scholar 

  • Maccatrozzo L, Bargelloni L, Radaelli G, Mascarello F, Patarnello T (2001) Characterization of the myostatin gene in the gilthead seabream (Sparus aurata): sequence, genomic structure, and expression pattern. Mar Biotechnol 3:224–230

    Article  CAS  Google Scholar 

  • Man Y, Yin R, Cai K, Qin C, Wang J, Yan H, Li M (2019) Primary amino acids affect the distribution of methylmercury rather than inorganic mercury among tissues of two farmed-raised fish species. Chemosphere 225:320–328

    Article  ADS  PubMed  CAS  Google Scholar 

  • Massault C, Hellemans B, Louro B, Batargias C, Van Houdt JKJ, Canario A, Volckaert FAM, Bovehuis H, Haley C, De Koning DJ (2010) QTL for body weight, morphometric traits and stress response in European sea bass Dicentrarchus labrax. Anim Genet 41:337–345

    Article  PubMed  CAS  Google Scholar 

  • McPherron AC, Lawler AM, Lee SJ (1997) Regulation of skeletal muscle mass in mice by a new TGF-b superfamily member. Nature 387:83–90

    Article  ADS  PubMed  CAS  Google Scholar 

  • McPherron AC, Lee SJ (1997) Double muscling in cattle due to mutations in the myostatin gene. PNAS 94:12457–12461

    Article  ADS  PubMed  PubMed Central  CAS  Google Scholar 

  • Miar Y, Salehi A, Kolbehdari D, Aleyasin SA (2014) Application of myostatin in sheep breeding programs: a review. Mol Biol Res Commun 3(1):33. eISSN 2345–2005

  • Mohammadabadi M, Bordbar F, Jensen J, Du M, Guo W (2021) Key genes regulating skeletal muscle development and growth in farm animals. Animals 11:835

    Article  PubMed  PubMed Central  Google Scholar 

  • Montera M, Piaggio F, Marchese C, Gismondi V, Stella A, Resta N, Varesco L, Guanti G, Marenia CA (2001) A silent mutation in exon 14 of the APC gene is associated with exon skipping in a FAP family. Mol Biol Res Commun 38:863–867

    CAS  Google Scholar 

  • Nazari S, Jafari V, Pourkazemi M, Miandare HK, Abdolhay HA (2016) Association between myostatin gene (MSTN-1) polymorphism and growth traits in domesticated rainbow trout (Oncorhynchus mykiss). Agri Gene 1:109–115

    Article  Google Scholar 

  • NCBI (2022) National Center for Biotechnology Information. https://www.ncbi.nlm.nih.gov/. Accessed 30 July 2022

  • Østbye TKK, Wetten OF, Tooming-Klunderud A, Jakobsen KS, Yafe A, Etzioni S, ... & Andersen Ø (2007) Myostatin (MSTN) gene duplications in Atlantic salmon (Salmo salar): evidence for different selective pressure on teleost MSTN-1 and-2. Gene 403:159–169. https://doi.org/10.1016/j.gene.2007.08.008

  • Özcan Gökçek E, Işık R (2020) Associations between genetic variants of the insulin-like growth factor I (IGF-I) gene and growth traits in European sea bass (Dicentrarchus labrax, L.). Fish Physiol Biochem 46:1131–1138

  • Palaiokostas C, Bekaert M, Taggart JB, Gharbi K, McAndrew BJ, Chatain B, Penman DJ, Vandeputte M (2015) A new SNP-based vision of the genetics of sex determination in European sea bass (Dicentrarchus labrax). Genet Sel Evol 47:1–10

    Article  Google Scholar 

  • Peñaloza C, Hamilton A, Guy DR, Bishop SC, Houston RD (2013) A SNP in the 5′ flanking region of the myostatin-1b gene is associated with harvest traits in Atlantic salmon (Salmo salar). BMC Genet 14:112

    Article  PubMed  PubMed Central  Google Scholar 

  • Piferrer F, Blázquez M, Navarro L, González A (2005) Genetic, endocrine, and environmental components of sex determination and differentiation in the European sea bass (Dicentrarchus labrax L.). Gen Comp Endocrinol 142:102–110

    Article  PubMed  CAS  Google Scholar 

  • Radaelli G, Rowlerson A, Mascarello F, Patruno M, & Funkenstein B (2003) Myostatin precursor is present in several tissues in teleost fish: a comparative immunolocalization study. Cell Tissue Res 311:239–250. https://doi.org/10.1007/s00441-002-0668-y

  • Quéré N, Guinand B, Kuhl H, Reinhardt R, Bonhomme F, Desmarais E (2010) Genomic sequences and genetic differentiation at associated tandem repeat markers in growth hormone, somatolactin and insulin-like growth factor-1 genes of the sea bass. Dicentrarchus Labrax Aquat Living Resour 23:285–296

    Article  Google Scholar 

  • Sánchez-Ramos I, Cross I, Mácha J, Martínez-Rodríguez G, Krylov V, Rebordinos L (2012) Assessment of tools for marker-assisted selection in a marine commercial species: significant association between MSTN-1 gene polymorphism and growth traits. Sci World J 2012

  • Sawayama E (2020) Polymorphisms and haplotypes of the myostatin gene associated with growth in juvenile red sea bream Pagrus major. Aquac Res 51:4238–4244

    Article  CAS  Google Scholar 

  • Shahi N, Mallik SK, Sarma D (2022) Muscle growth in targeted knockout common carp (Cyprinus carpio) mstn gene with low off-target effects. Aquaculture 547:737423

    Article  CAS  Google Scholar 

  • Sun Y, Li Q, Wang G, Zhu D, Chen J, Li P, Tong J (2017) Polymorphisms in the Myostatin-1 gene and their association with growth traits in Ancherythroculter nigrocauda. Chin J Oceanol Limnol 35:597–602

    Article  CAS  Google Scholar 

  • Sun Y, Yu X, Tong J (2012) Polymorphisms in myostatin gene and associations with growth traits in the common carp (Cyprinus carpio L.). Int J Mol Sci 13:14956–14961

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tao WJ, Boulding EG (2003) Associations between single nucleotide polymorphisms in candidate genes and growth rate in Arctic charr (Salvelinus alpinus L.). Heredity 91:60–69

    Article  PubMed  CAS  Google Scholar 

  • TEAM R Core et al (2013) R: a language and environment for statistical computing

  • Terova G, Bernardini G, Binelli G, Gornati R, Saroglia M (2006) cDNA encoding sequence for myostatin and FGF6 in sea bass (Dicentrarchus labrax L.) and the effect of fasting and refeeding on their abundance levels. Domest Anim Endocrinol 30:304–319

    Article  PubMed  CAS  Google Scholar 

  • Terova G, Rimoldi S, Bernardini G, Saroglia M (2013) Inhibition of myostatin gene expression in skeletal muscle of fish by in vivo electrically mediated dsRNA and shRNAi. Delivery Mol Biotechnol 54:673

    Article  PubMed  CAS  Google Scholar 

  • Tran TTH, Nguyen HT, Le BTN, Tran PH, Van Nguyen S, Kim OTP (2021) Characterization of single nucleotide polymorphism in IGF1 and IGF1R genes associated with growth traits in striped catfish (Pangasianodon hypophthalmus Sauvage, 1878). Aquaculture 538:736542

    Article  CAS  Google Scholar 

  • Tsai HY, Hamilton A, Guy DR, Houston RD (2014) Single nucleotide polymorphisms in the insulin-like growth factor 1 (IGF 1) gene are associated with growth-related traits in farmed Atlantic salmon. Anim Genet 45:709–715

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vandeputte M, Gagnaire PA, Allal F (2019) The European Sea bass: a key marine fish model in the wild and in aquaculture. Anim Genet 50:195–206

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vandeputte M, Quillet E, Chatain B (2012) Are sex ratios in wild European sea bass (Dicentrarchus labrax) populations biased? Aquat Living Resour 25:77–81

    Article  Google Scholar 

  • Wang Y, Lang Z, Huang D, Chen J (2008) Effects of pre-mRNA introns on regulation of eukaryotic gene expression. Biotechnol J 18:1–91

    Google Scholar 

  • Wang Y, Wang X, Meng X, Wang H, Jiang Z, Qiu X (2014) Identification of two SNPs in myostatin (MSTN) gene of Takifugu rubripes and their association with growth traits. Mol Cell Probes 28:200–203

    Article  PubMed  CAS  Google Scholar 

  • Whitehead PJP, Bauchot ML, Hureau JC, Nielsen J, Tortonese E (1986) Fish of the North-eastern Atlantic and Mediterranean, Vol.2. UNESCO

  • Yan M, Li B, Wang J, Bai Y, Ke Q, Zhou T, Xu P (2022) Disruption of mstn Gene by CRISPR/Cas9 in large yellow croaker (Larimichthys crocea). Mar Biotechnol 24:681–689

    Article  CAS  Google Scholar 

  • Yang J, Zhang Y (2015) I-TASSER server: new development for protein structure and function predictions. Nucleic Acids Res 43:W174–W181

    Article  ADS  PubMed  PubMed Central  CAS  Google Scholar 

  • Yang Y, Lan Z, Shu H, Zhou H, Jiang X, Hou L, Gu P (2018) Association between expression levels and growth trait-related SNPs located in promoters of the MC4R and MSTN genes in Spinibarbus hollandi. Genes and Genomics 40:1119–1125

    Article  PubMed  CAS  Google Scholar 

  • Yeh YC, Kinoshita M, Ng TH, Chang YH, Maekawa S, Chiang YA, Aoki T, Wang HC (2017) Using CRISPR/Cas9-mediated gene editing to further explore growth and trade-off effects in myostatin-mutated F4 medaka (Oryzias latipes). Sci Rep 7:1–13

    Article  ADS  Google Scholar 

  • Zhang C, McFarlane C, Lokireddy S, Bonala S, Ge X, Masuda S, Sharma M, Kambadur R (2011) Myostatin-deficient mice exhibit reduced insulin resistance through activating the AMP-activated protein kinase signalling pathway. Diabetologia 54:1491–1501

    Article  PubMed  CAS  Google Scholar 

  • Zhou Z, Wang M, Yang J, Liu B, Li L, Shi Y, Pu F, Xu P (2021) Genome-wide association analysis reveals genetic variations and candidate genes associated with growth-related traits and condition factor in Takifugu bimaculatus. Reproduction and Breeding 1:89–99

    Article  Google Scholar 

  • Zuo A, Zhou Y, Li Y, Zhang Y, Yi Z, Xiao Y, Zou M, Cao S, Qu F, Tang J, Liu Z (2022) Molecular characterization of LKB1 of Triploid Crucian Carp and its regulation on muscle growth and quality. Animals 12:2474

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We are grateful to Ege University Planning and Monitoring Coordination of Organizational Development and Directorate of Library and Documentation for their support in editing and proofreading service of this study.

Funding

This work was supported by the Scientific Research Projects Coordination Unit of Ege University (Project No: FKP-2020–21912).

Author information

Authors and Affiliations

Authors

Contributions

E.Ö.G. and R.I. developed the research topic and acted as study principal investigator (PI). E.Ö.G., B.K. and K.G. collected phenotypic data and sampling. E.Ö.G. obtained and analyzed genetic data. E.Ö.G. and R.I. performed statistical analysis and wrote the manuscript. All authors reviewed the manuscript.

Corresponding author

Correspondence to Emel Özcan Gökçek.

Ethics declarations

Ethics Approval

All experiments in this study were conducted according to national and institutional guidelines (Ege University Animal Experiments Ethics Committee).

Conflict of Interest

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 84 KB)

Supplementary file2 (PDF 99 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Özcan Gökçek, E., Işık, R., Karahan, B. et al. Characterisation of Single Nucleotide Polymorphisms and Haplotypes of MSTN Associated with Growth Traits in European Sea Bass (Dicentrarchus labrax). Mar Biotechnol 25, 347–357 (2023). https://doi.org/10.1007/s10126-023-10211-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-023-10211-w

Keywords

Navigation