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Correlation analysis of mandarin fish (Siniperca chuatsi) growth hormone gene polymorphisms and growth traits

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Abstract

Screening of trait-associated molecular markers can be used to enhance the efficiency of selective breeding. Previously, we produced the first high-density genetic linkage map for the mandarin fish (Siniperca chuatsi) and identified 11 quantitative-trait loci significantly associated with growth, of which one is located within the growth hormone (GH) gene. To investigate the GH gene polymorphisms and their correlation with growth, the complete sequence was cloned and 32 single-nucleotide polymorphisms (SNPs) and one simple-sequence repeat (SSR) were identified. Of which, eight SNPs (G1–G8) and the SSR (GH-AG) were selected for genotyping and correlation analysis with growth traits in a random population. The results showed that the four novel polymorphic loci (G1, G2, G3 and GH-AG) were significantly correlated with growth traits of mandarin fish (\(P<~0.05\)). Of these, G1, G3 and GH-AG showed highly significant correlations with multiple growth traits (\(P <~0.01\)) and the combined SNP analysis showed that G1–G3 formed four effective diplotypes (D1–D4), among which D1 was highly significantly greater than D4 (\(P<~0.01\)) for some important growth traits. In conclusion, our results show that the four polymorphic loci G1–G3 and GH-AG within the mandarin fish GH gene are significantly correlated with growth traits and could be used as candidate molecular markers for selective breeding of superior varieties of mandarin fish.

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References

  • Almuly R., Skopal T. and Funkenstein B. 2008 Regulatory regions in the promoter and first intron of Sparus aurata growth hormone gene: repression of gene activity by a polymorphic minisatellite. Comp. Biochem. Physiol. Part D. Genom. Proteom.  3, 43–50.

    Google Scholar 

  • Ardlie K. G., Kruglyak L. and Seielstad M. 2002 Patterns of linkage disequilibrium in the human genome. Nat. Rev. Genet.  3, 299–309.

    Article  CAS  Google Scholar 

  • Bachl J., Olsson C., Chitkara N. and Wabl M. 1998 The Ig mutator is dependent on the presence, position, and orientation of the large intron enhancer. Proc. Natl. Acad. Sci. USA  95, 2396–2399.

    Article  CAS  Google Scholar 

  • Brem G., Brenig B., Hörstgen-Schwark G. and Winnacker E. L. 1988 Gene transfer in tilapia (Oreochromis niloticus). Aquaculture  68, 209–219.

    Article  CAS  Google Scholar 

  • Brinster R. L., Allen J. M., Behringer R. R., Gelinas R. E. and Palmiter R. D. 1988 Introns increase transcriptional efficiency in transgenic mice. Proc. Natl. Acad. Sci. USA  85, 836–840.

    Article  CAS  Google Scholar 

  • Carlson C. S., Eberle M. A., Rieder M. J., Yi Q., Kruglyak L. and Nickerson D. A. 2004 Selecting a maximally informative set of single-nucleotide polymorphisms for association analyses using linkage disequilibrium. Am. J. Hum. Genet.  74, 106–120.

    Article  CAS  Google Scholar 

  • Cavari B., Funkenstei B., Chen T. T., Gonzalez-Villasenor L. I. and Schartl M. 1993 Effect of growth hormone on the growth rate of the gilthead seabream (Sparus aurata), and use of different constructs for the production of transgenic fish. Aquaculture  111, 189–197.

    Article  CAS  Google Scholar 

  • Chang K. C. 2000 Critical regulatory domains in intron 2 of a porcine sarcomeric myosin heavy chain gene. J. Muscle Res. Cell Motil.  21, 451–461.

    Article  CAS  Google Scholar 

  • Chatakondi N., Lovell R. T., Duncan P. L., Hayat M., Chen T. T., Powers D. A. et al. 1995 Body composition of transgenic common carp, Cyprinus carpio, containing rainbow trout growth hormone gene. Aquaculture  138, 99–109.

    Article  CAS  Google Scholar 

  • Cheng Y., Liu S., Su D., Lu C., Zhang X., Wu Q. et al. 2016 Distribution and linkage disequilibrium analysis of polymorphisms of GH-1 gene in different populations of pigs associated with body size. J. Genet.  95, 79–87.

    Article  CAS  Google Scholar 

  • Cogan J. D., Prince M. A., Lekhakula S., Bundey S., Futrakul A., McCarthy E. M. et al. III 1997 A novel mechanism of aberrant pre-mRNA splicing in humans. Hum. Mol. Genet.  6, 909–912.

  • Fletcher G. L., Shears M. A., Yaskowiak E. S., King M. J. and Goddard S. V. 2005 Gene transfer: potential to enhance the genome of atlantic salmon for aquaculture. Aust. J. Exp. Agric.  44, 1095–1100.

    Article  Google Scholar 

  • Fofanova O. V., Evgrafov O. V., Polyakov A. V., Poltaraus A. B., Peterkova V. A. and Dedov II. 2003 A novel IVS2-2A\(>\)T splicing mutation in the GH-1 gene in familial isolated growth hormone deficiency type ii in the spectrum of other splicing mutations in the Russian population. J. Clin. Endocr. Metab.  88, 820–826.

    Google Scholar 

  • Forsyth I. A. and Wallis M. 2002 Growth hormone and prolactin-molecular and functional evolution. J. Mammary Gland Biol. Neoplasia  7, 291–312.

    Article  Google Scholar 

  • Hua G., Chen S., Yu J., Cai K., Wu C., Li Q. et al. 2009 Polymorphism of the growth hormone gene and its association with growth traits in Boer goat bucks. Meat Sci.  81, 391–395.

    Article  CAS  Google Scholar 

  • Jaser S. K. K., Dias M. A. D., Lago A. D. A., Neto R. V. R. and Hilsdorf A. W. S. 2017 Single nucleotide polymorphisms in the growth hormone gene of Oreochromis niloticus and their association with growth performance. Aquac. Res.  48, 5835–5845.

    Article  CAS  Google Scholar 

  • Kamijo T., Hayashi Y., Shimatsu A., Kinoshita E., Yoshimoto M., Ogawa M. et al. 1999 Mutations in intron 3 of GH-1 gene associated with isolated GH deficiency type II in three Japanese families. Clin. Endocrinol.  51, 355–360.

    Article  CAS  Google Scholar 

  • Li M., Liu W., Luo W., Luo W., Zhang X., Zhu W. et al. 2016 Polymorphisms and their association with growth traits in the growth hormone gene of yellow catfish, Pelteobagrus fulvidraco. Aquaculture  469, 117–123.

    Article  Google Scholar 

  • Liu F., Lu S., Liu Z., Xie X., Tang J. and Kuang G. 2009 The GH gene diversity among three Siniperca fish species. Oceanologia et Limnologia Sinica  40, 470–478.

    Google Scholar 

  • Liu X., Liang H., Liang Y., Li Z., Qin X., Zhang T. et al. 2017 Significant associations of polymorphisms in the growth hormone gene with growth traits in common carp (Cyprinus carpio). Meta Gene  14, 38–41.

    Article  Google Scholar 

  • Ma D., Han L., Bai J., Li S., Fan J., Yu L. et al. 2014 A 66-bp deletion in growth hormone releasing hormone gene 5\(^\prime \)-flanking region with largemouth bass recessive embryonic lethal. Anim. Genet.  45, 421–426.

    Google Scholar 

  • Nott A., Meislin S. H. and Moore M. J. 2003 A quantitative analysis of intron effects on mammalian gene expression. RNA  9, 607–617.

    Article  CAS  Google Scholar 

  • Ogura Y., Kou I., Miura S., Takahashi A., Xu L., Takeda K. et al. 2015 A functional SNP in BNC2 is associated with adolescent idiopathic scoliosis. Am. J. Hum. Genet.  97, 337–342.

    Article  CAS  Google Scholar 

  • Oscarson M., Hidestrand M., Johansson I. and Ingelman-Sundberg M. 1997 A combination of mutations in the CYP2D6*17 (CYP2D6Z) allele causes alterations in enzyme function. Mol. Pharmacol.  52, 1034–1040.

    Article  CAS  Google Scholar 

  • Oztetik E., Kockar F., Alper M. and Iscan M. 2015 Molecular characterization of zeta class glutathione S-transferases from Pinus brutia Ten. J. Genet.  94, 417–423.

    Article  CAS  Google Scholar 

  • Pagani F. and Baralle F. E. 2004 Genomic variants in exons and introns: identifying the splicing spoilers. Nat. Rev. Genet.  5, 389–396.

    Article  CAS  Google Scholar 

  • Phillips J. A., Cogan J. D., Millendavis S., Milner R. D. G., Sakati N., Schenkman S. S. et al. 1993 Molecular-basis of autosomal recessive and autosomal-dominant inheritance of familial GH deficiency. Am. J. Hum. Genet.  53, 6–6.

    Google Scholar 

  • Reinecke M., Björnsson B. T., Dickhoff W. W., McCormick S. D., Navarro I., Power D. M. et al. 2005 Growth hormone and insulin-like growth factors in fish: where we are and where to go. Gen. Comp. Endocrinol.  142, 20–24.

    Article  CAS  Google Scholar 

  • Stephens M., Smith N. J. and Donnelly P. 2001 A new statistical method for haplotype reconstruction from population data. Am. J. Hum. Genet.  68, 978–989.

    Article  CAS  Google Scholar 

  • Sun C., Ye X., Tian Y. and Dong J. 2015a Simple sequence repeat-based analysis of the genetic diversity and population genetic structure of populations of Siniperca chuatsi. Genet. Mol. Res.  14, 9343–9352.

    Article  CAS  Google Scholar 

  • Sun J., He S., Liang X., Li L., Wen Z., Zhu T. et al. 2015b Identification of SNPs in NPY and LEP and the association with food habit domestication traits in mandarin fish. J. Genet.  94, 118–112.

  • Sun C., Niu Y., Ye X., Dong J., Hu W., Zeng Q. et al. 2017 Construction of a high-density linkage map and mapping of sex determination and growth-related loci in the mandarin fish (Siniperca chuatsi). BMC Genom.  18, 446.

    Article  Google Scholar 

  • Sweeney G. 2002 Leptin signaling Cell Signa  14, 655–663.

    Article  CAS  Google Scholar 

  • Tan X., Yu X. and Tong J. 2009 Correlation study of bighead carp (Aristichthys nobilis) GH gene single nucleotide polymorphisms and growth traits. Acad. Annu. Meet. Chin. Soc. Fish. 1, 81.

    Google Scholar 

  • Tian C., Yang M., Lv L., Yuan Y., Liang X., Guo W. et al. 2014 Single nucleotide polymorphisms in growth hormone gene and their association with growth traits in Siniperca chuatsi (basilewsky). Int. J. Mol. Sci.  15, 7029–7036.

    Article  Google Scholar 

  • Tsai H. J., Kuo J. C., Lou S. W. and Kuo T. T. 1994 Growth enhancement of juvenile striped mullet by feeding recombinant yeasts containing fish growth hormone. Prog. Fish-Cult.  56, 7–12.

    Article  Google Scholar 

  • Waltz E. 2017 First genetically engineered salmon sold in Canada. Nature  548, 148–148.

    Article  CAS  Google Scholar 

  • Wang D., Guo Y., Wrighton S. A., Cooke G. E. and Sadee W. 2011 Intronic polymorphism in CYP3A4 affects hepatic expression and response to statin drugs. Pharmacogenom. J.  11, 274–286.

    Article  Google Scholar 

  • Wang H., Sun J., Wang P., Lu X., Xu P., Gu Y. et al. 2016 Polymorphism in Growth hormone gene and its association with growth traits in Siniperca chuatsi. Isr. J. Aquacult-Bamid.  68, 1–8

    Google Scholar 

  • Wu Y., Pan A. L., Pi J. S., Pu Y. J., Du J. P., Liang Z. H. et al. 2012 One novel SNP of growth hormone gene and its associations with growth and carcass traits in ducks. Mol. Biol. Rep.  39, 8027–8033.

    Article  CAS  Google Scholar 

  • Yong Y. and Lin H. E. 2005 SHEsis, a powerful software platform for analyses of linkage disequilibrium, haplotype construction, and genetic association at polymorphism loci. Cell Res.  15, 97–98.

    Article  Google Scholar 

  • Yu L., Bai J., Fan J., Li X. and Ye X. 2010 SNPs detection in largemouth bass Myostatin gene and its association with growth traits. J. Fish. China  34, 665–671.

    Article  CAS  Google Scholar 

  • Zeng Y., Zhang L., Hu Z., Yang Q., Ma M., Liu B. et al. 2016 Association of protein Z and factor VII gene polymorphisms with risk of cerebral hemorrhage: a case-control and a family-based association study in a Chinese Han population. J. Genet.  95, 383–388.

    Article  Google Scholar 

  • Zhang P., Hayat M., Joyce C., Gonzalez-Villaseñor L. I., Lin C. M., Dunham R. A. et al. 1990 Gene transfer, expression and inheritance of PRSV-rainbow trout-GH cDNA in the common carp, cyprinus carpio (linnaeus). Mol. Reprod. Dev.  25, 3–13.

    Article  CAS  Google Scholar 

  • Zhang S., Zhong L., Qin Q., Wang M., Pan J., Chen X. et al. 2016 Three SNPs polymorphism of growth hormone-releasing hormone gene (GHRH) and association analysis with growth traits in channel catfish. Acta Hydrobiol. Sin.  40, 886–893.

    Google Scholar 

  • Zhao J., He F., Wen H., Li J. and Si Y. 2014 Correlation between the polymorphism of GH gene of male half-smooth tongue sole and their growth traits and hormone content. Period. Ocean Univ. China  44, 35–40.

    CAS  Google Scholar 

  • Zhu Z., Li G., He L. and Chen S. 1985 Novel gene transfer into the fertilized eggs of gold fish (Carassius auratus L. 1758). J. Appl. Ichthyol.  1, 31–34.

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by grants from the China Agriculture Research System (CARS-46), Provincial Special Project for Promoting Economic Development (YueYu 2018-06), Central Public-interest Scientific Institution Basal Research Fund CAFS (no. 2017HY-ZC0402), Ocean Fisheries Science and Technology Promotion Project of Guangdong province (no. A201601A06) and the Science and Technology Project of Guangdong province (no. 2015A020209034). We appreciate all the famers who had cultured and fed our fishes in the Yushun Animal Husbandry and Fishery Science and Technology Service.

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  1. Cheng-Fei Sun and Hai-Lin Sun contributed equally to this work.

Authors and Affiliations

  1. Key Laboratory of Tropical and Subtropical Fishery Resource Application and Cultivation, Ministry of Agriculture, Pearl River Fisheries Research Institute, Chinese Academy of Fishery Science, Guangzhou, 510380, People’s Republic of China

    Cheng-Fei Sun, Hai-Lin Sun, Jun-Jian Dong, Yuan-Yuan Tian, Jie Hu & Xing Ye

  2. College of Fisheries and Life Science, Shanghai Ocean University, Shanghai, 201306, People’s Republic of China

    Cheng-Fei Sun, Hai-Lin Sun & Xing Ye

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  1. Cheng-Fei Sun
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Correspondence to Xing Ye.

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Corresponding editor: H. A. Ranganath

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Sun, CF., Sun, HL., Dong, JJ. et al. Correlation analysis of mandarin fish (Siniperca chuatsi) growth hormone gene polymorphisms and growth traits. J Genet 98, 58 (2019). https://doi.org/10.1007/s12041-019-1100-7

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