A SNP in the 5′ flanking region of the myostatin-1b gene is associated with harvest traits in Atlantic salmon (Salmo salar)

BMC Genetics

Ross D Houston¹  Stephen C Bishop¹  Derrick R Guy²  Alastair Hamilton²  Carolina Peñaloza¹ 

[1]Division of Genetics and Genomics, The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh, Midlothian EH25 9RG, UK

[2]Landcatch Natural Selection Ltd, 15 Beta Centre, Stirling University Innovation Park, Stirling FK9 4NF, UK

关键词: Marker-assisted selection;    Aquaculture;    Myostatin;    Atlantic salmon;    Association analysis;   

Others  :  1086318
DOI  :  10.1186/1471-2156-14-112

 received in 2013-05-16, accepted in 2013-11-11,  发布年份 2013

【 摘 要 】

Background

Myostatin (MSTN) belongs to the transforming growth factor-β superfamily and is a potent negative regulator of skeletal muscle development and growth in mammals. Most teleost fish possess two MSTN paralogues. However, as a consequence of a recent whole genome-duplication event, salmonids have four: MSTN-1 (−1a and -1b) and MSTN-2 (−2a and -2b). Evidence suggests that teleost MSTN plays a role in the regulation of muscle growth. In the current study, the MSTN-1b gene was re-sequenced and screened for SNP markers in a commercial population of Atlantic salmon. After genotyping 4,800 progeny for the discovered SNPs, we investigated their association with eight harvest traits - four body-weight traits, two ratios of weight traits, flesh colour and fat percentage - using a mixed model association analysis.

Results

Three novel SNPs were discovered in the MSTN-1b gene of Atlantic salmon. One of the SNPs, located within the 5′ flanking region (g.1086C > T), had a significant association with harvest traits (p < 0.05), specifically for: Harvest Weight (kg), Gutted Weight (kg), Deheaded Weight (kg) and Fillet Weight (kg). The haplotype-based association analysis was consistent with this result because the two haplotypes that showed a significant association with body-weight traits, hap4 and hap5 (p < 0.05 and p < 0.01, respectively), differ by a single substitution at the g.1086C > T locus. The alleles at g.1086C > T act in an additive manner and explain a small percentage of the genetic variation of these phenotypes.

Conclusions

The association analysis revealed that g.1086C > T had a significant association with all body-weight traits under study. Although the SNP explains a small percentage of the variance, our results indicate that a variation in the 5′ flanking region of the myostatin gene is associated with the genetic regulation of growth in Atlantic salmon.

【 授权许可】

   
2013 Peñaloza et al.; licensee BioMed Central Ltd.

【 参考文献 】

• [1]Lee SJ, McPherron AC: Myostatin and the control of skeletal muscle mass. Curr Opin Genet Dev 1999, 9:604-607.
• [2]McPherron AC, Lee SJ: Double muscling in cattle due to mutations in the myostatin gene. Proc Natl Acad Sci U S A 1997, 94:12457-12461.
• [3]Kambadur R, Sharma M, Smith TPL, Bass JJ: Mutations in myostatin (GDF8) in double-muscled Belgian blue and piedmontese cattle. Genome Res 1997, 7:910-915.
• [4]Clop A, Marcq F, Takeda H, Pirottin D, Tordoir X, Bibé B, Bouix J, Caiment F, Elsen J-M, Eychenne F, Eychenne F, Larzul C, Laville E, Meish F, Milenkovic D, Tobin J, Charlier C, Georges M: A mutation creating a potential illegitimate microRNA target site in the myostatin gene affects muscularity in sheep. Nat Genet 2006, 38:813-818.
• [5]Grobet L, Martin L, Poncelet D, Pirottin D, Brouwers B, Riquet J, Schoeberlein A, Dunner S, Ménissier F, Massabanda J, Fries R, Hanset R, Georges M: A deletion in the bovine myostatin gene causes the double-muscled phenotype in cattle. Nat Genet 1997, 17:71-74.
• [6]Hu X, Guo H, He Y, Wang S, Zhang L, Huang X, Roy SW, Lu W, Hu J, Bao Z: Molecular characterization of myostatin gene from zhikong scallop Chlamys farreri (Jones et preston 1904). Genes Genet Syst 2010, 85:207-218.
• [7]Liu L, Yu X, Tong J: Molecular characterization of myostatin (MSTN) gene and association analysis with growth traits in the bighead carp (Aristichthys nobilis). Mol Biol Rep 2012, 39:9211-9221.
• [8]De Santis C, Evans B, Smith-Keune C, Jerry D: Molecular characterization, tissue expression and sequence variability of the barramundi (Lates calcarifer) myostatin gene. BMC Genomics 2008, 9:82. BioMed Central Full Text
• [9]De Santis C, Wade NM, Jerry DR, Preston NP, Glencross BD, Sellars MJ: Growing backwards: an inverted role for the shrimp ortholog of vertebrate myostatin and GDF11. J Exp Biol 2011, 214:2671-2677.
• [10]Xing F, Tan X, Zhang PJ, Ma J, Zhang Y, Xu P, Xu Y: Characterization of amphioxus GDF8/11 gene, an archetype of vertebrate MSTN and GDF11. Dev Genes Evol 2007, 217:549-554.
• [11]Amores A, Force A, Yan Y-L, Joly L, Amemiya C, Fritz A, Ho RK, Langeland J, Prince V, Wang Y-L, Westerfield M, Ekker M, Postlethwait JH: Zebrafish hox Clusters and Vertebrate Genome Evolution. Science 1998, 282:1711-1714.
• [12]Postlethwait JH, Yan Y-L, Gates MA, Horne S, Amores A, Brownlie A, Donovan A, Egan ES, Force A, Gong Z, Goutel C, Fritz A, Kelsh R, Knapik E, Liao E, Paw B, Ransom D, Singer A, Thomson M, Abduljabbar TS, Yelick P, Beier D, Joly J-S, Larhammar D, Rosa F, Westerfield M, Zon LI, Johnson SL, Talbot WS: Vertebrate genome evolution and the zebrafish gene map. Nat Genet 1998, 18:345-349.
• [13]Kerr T, Roalson EH, Rodgers BD: Phylogenetic analysis of the myostatin gene sub-family and the differential expression of a novel member in zebrafish. Evol Dev 2005, 7:390-400.
• [14]Allendorf FW, Thorgaard GH: Tetraploidy and the Evolution of Salmonid Fishes. In Evolutionary Genetics of Fishes. Edited by Turner BJ. New York: Plenum Press; 1984:1-53.
• [15]Gabillard J-C, Biga PR, Rescan P-Y, Seiliez I: Revisiting the paradigm of myostatin in vertebrates: insights from fishes. Gen Comp Endocrinol 2013, 194:45-54.
• [16]McPherron AC, Lawler AM, Lee SJ: Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature 1997, 387:83-90.
• [17]Garikipati D, Gahr S, Rodgers B: Identification, characterization, and quantitative expression analysis of rainbow trout myostatin-1a and myostatin-1b genes. J Endocrinol 2006, 190:879-888.
• [18]Ostbye T-K, Wetten O, Tooming-Klunderud A, Jakobsen K, Yafe A, Etzioni S, Moen T, Andersen O: Myostatin (MSTN) gene duplications in Atlantic salmon (Salmo salar): evidence for different selective pressure on teleost MSTN-1 and −2. Gene 2007, 403:159-169.
• [19]Maccatrozzo L, Bargelloni L, Cardazzo B, Rizzo G, Patarnello T: A novel second myostatin gene is present in teleost fish. FEBS Lett 2001, 509:36-40.
• [20]Lee CY, Hu SY, Gong HY, Chen MH, Lu JK, Wu JL: Suppression of myostatin with vector-based RNA interference causes a double-muscle effect in transgenic zebrafish. Biochem Biophys Res Commun 2009, 387:766-771.
• [21]Sawatari E, Seki R, Adachi T, Hashimoto H, Uji S, Wakamatsu Y, Nakata T, Kinoshita M: Overexpression of the dominant-negative form of myostatin results in doubling of muscle-fiber number in transgenic medaka (Oryzias latipes). Comp Biochem Physiol A Mol Integr Physiol 2010, 155:183-189.
• [22]Medeiros E, Phelps M, Fuentes F, Bradley T: Overexpression of follistatin in trout stimulates increased muscling. Am J Physiol Regul Integr Comp Physiol 2009, 297:42.
• [23]FAO: The State of the World Fisheries and Aquaculture. Rome: FAO; 2010.
• [24]Fjalestad K, Moen T, Gomez-Raya L: Prospects for genetic technology in salmon breeding programmes. Aquac Res 2003, 34:397-406.
• [25]Davidson WS, Koop BF, Jones SJ, Iturra P, Vidal R, Maass A, Jonassen I, Lien S, Omholt SW: Sequencing the genome of the Atlantic salmon (Salmo salar). Genome Biol 2010, 11:403.
• [26]Baranski M, Moen T, Våge D: Mapping of quantitative trait loci for flesh colour and growth traits in Atlantic salmon (Salmo salar). Genet Sel Evol 2010, 42:17. BioMed Central Full Text
• [27]Reid D, Szanto A, Glebe B, Danzmann R, Ferguson M: QTL for body weight and condition factor in Atlantic salmon (Salmo salar): comparative analysis with rainbow trout (Oncorhynchus mykiss) and Arctic charr (Salvelinus alpinus). Heredity 2005, 94:166-172.
• [28]Boulding E, Culling M, Glebe B, Berg P, Lien S, Moen T: Conservation genomics of Atlantic salmon: SNPs associated with QTLs for adaptive traits in parr from four trans-Atlantic backcrosses. Heredity 2008, 101:381-391.
• [29]Houston R, Bishop S, Hamilton A, Guy D, Tinch A, Taggart J, Derayat A, McAndrew B, Haley C: Detection of QTL affecting harvest traits in a commercial Atlantic salmon population. Anim Genet 2009, 40:753-755.
• [30]Gutierrez A, Lubieniecki K, Davidson E, Lien S, Kent M, Fukui S, Withler R, Swift B, Davidson W: Genetic mapping of quantitative trait loci (QTL) for body-weight in Atlantic salmon (Salmo salar) using a 6.5 K SNP array. Aquaculture 2012, 358–359:61-70.
• [31]Zhu YY, Liang HW, Li Z, Luo XZ, Li L, Zhang ZW, Zou GW: Polymorphism of MSTN gene and its association with growth traits in yellow catfish (Pelteobagruse fulvidraco). Yi Chuan 2012, 34:72-78.
• [32]Li H, Fan J, Liu S, Yang Q, Mu G, He C: 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 2012, 161:315-322.
• [33]Sun Y, Yu X, Tong J: Polymorphisms in myostatin gene and associations with growth traits in the common carp (Cyprinus carpio L.). Int J Mol Sci 2012, 13:14956-14961.
• [34]Guo L, Li L, Zhang S, Guo X, Zhang G: Novel polymorphisms in the myostatin gene and their association with growth traits in a variety of bay scallop, Argopecten irradians. Anim Genet 2011, 42:339-340.
• [35]Sanchez-Ramos I, Cross I, Macha J, Martinez-Rodriguez G, Krylov V, Rebordinos L: 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, 2012:369802.
• [36]Lee SB, Kim YS, Oh M-Y, Jeong I-h, Seong K-B, Jin H-J: Improving rainbow trout (Oncorhynchus mykiss) growth by treatment with a fish (Paralichthys olivaceus) myostatin prodomain expressed in soluble forms in E. coli. Aquaculture 2010, 302:270-278.
• [37]Carpio Y, Acosta J, Morales R, Santisteban Y, Sanchéz A, Estrada M: Regulation of body mass growth through activin type IIB receptor in teleost fish. Gen Comp Endocrinol 2009, 160:158-167.
• [38]Kim Y-S, Fox B, Kim KH, Lee SB, Jin HJ, Tamaru CS: Immersion bath treatment of tilapia fry with myostatin-1 prodomain does not affect tilapia growth at market size. Aquac Res 2012, 44:1643-1648.
• [39]Stinckens A, Georges M, Buys N: Mutations in the myostatin gene leading to hypermuscularity in mammals: indications for a similar mechanism in fish? Anim Genet 2011, 42:229-234.
• [40]Goddard M, Hayes B: Mapping genes for complex traits in domestic animals and their use in breeding programmes. Nat Rev Genet 2009, 10:381-391.
• [41]Hall TA: BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 1999, 41:95-98.
• [42]Powell J, White I, Guy D, Brotherstone S: Genetic parameters of production traits in Atlantic salmon (Salmo salar). Aquaculture 2008, 274:225-231.
• [43]Barrett JC, Fry B, Maller J, Daly MJ: Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 2005, 21:263-265.
• [44]Stephens M, Donnelly P: A comparison of bayesian methods for haplotype reconstruction from population genotype data. Am J Hum Genet 2003, 73:1162-1169.
• [45]Stephens M, Smith N, Donnelly P: A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 2001, 68:978-989.
• [46]Gilmour AR, Gogel BJ, Cullis BR, Welham SJ, Thompson R: ASREML User Guide Release 3.0. VSN International Ltd: Hemel Hempstead, UK; 2009.
• [47]Falconer DS, Mackay TFC: Introduction to Quantitative Genetics. 4th edition. Longmans Green: Harlow, Essex, UK; 1996.