Advertisement

Journal of Genetics

, 98:58 | Cite as

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

  • Cheng-Fei Sun
  • Hai-Lin Sun
  • Jun-Jian Dong
  • Yuan-Yuan Tian
  • Jie Hu
  • Xing YeEmail author
RESEARCH ARTICLE
  • 51 Downloads

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.

Keywords

growth hormone polymorphism growth trait Siniperca chuatsi 

Notes

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.

Supplementary material

12041_2019_1100_MOESM1_ESM.docx (19 kb)
Supplementary material 1 (docx 18 KB)

References

  1. 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
  2. Ardlie K. G., Kruglyak L. and Seielstad M. 2002 Patterns of linkage disequilibrium in the human genome. Nat. Rev. Genet.  3, 299–309.CrossRefGoogle Scholar
  3. 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.CrossRefGoogle Scholar
  4. Brem G., Brenig B., Hörstgen-Schwark G. and Winnacker E. L. 1988 Gene transfer in tilapia (Oreochromis niloticus). Aquaculture  68, 209–219.CrossRefGoogle Scholar
  5. 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.CrossRefGoogle Scholar
  6. 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.CrossRefGoogle Scholar
  7. 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.CrossRefGoogle Scholar
  8. 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.CrossRefGoogle Scholar
  9. 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.CrossRefGoogle Scholar
  10. 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.CrossRefGoogle Scholar
  11. 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.Google Scholar
  12. 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.CrossRefGoogle Scholar
  13. 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
  14. Forsyth I. A. and Wallis M. 2002 Growth hormone and prolactin-molecular and functional evolution. J. Mammary Gland Biol. Neoplasia  7, 291–312.CrossRefGoogle Scholar
  15. 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.CrossRefGoogle Scholar
  16. 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.CrossRefGoogle Scholar
  17. 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.CrossRefGoogle Scholar
  18. 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.CrossRefGoogle Scholar
  19. 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
  20. 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.CrossRefGoogle Scholar
  21. 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
  22. Nott A., Meislin S. H. and Moore M. J. 2003 A quantitative analysis of intron effects on mammalian gene expression. RNA  9, 607–617.CrossRefGoogle Scholar
  23. 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.CrossRefGoogle Scholar
  24. 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.CrossRefGoogle Scholar
  25. 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.CrossRefGoogle Scholar
  26. Pagani F. and Baralle F. E. 2004 Genomic variants in exons and introns: identifying the splicing spoilers. Nat. Rev. Genet.  5, 389–396.CrossRefGoogle Scholar
  27. 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
  28. 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.CrossRefGoogle Scholar
  29. 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.CrossRefGoogle Scholar
  30. 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.CrossRefGoogle Scholar
  31. 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.Google Scholar
  32. 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.CrossRefGoogle Scholar
  33. Sweeney G. 2002 Leptin signaling Cell Signa  14, 655–663.CrossRefGoogle Scholar
  34. 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
  35. 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.CrossRefGoogle Scholar
  36. 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.CrossRefGoogle Scholar
  37. Waltz E. 2017 First genetically engineered salmon sold in Canada. Nature  548, 148–148.CrossRefGoogle Scholar
  38. 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.CrossRefGoogle Scholar
  39. 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, 1–8Google Scholar
  40. 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.CrossRefGoogle Scholar
  41. 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.CrossRefGoogle Scholar
  42. 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.CrossRefGoogle Scholar
  43. 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.CrossRefGoogle Scholar
  44. 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.CrossRefGoogle Scholar
  45. 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
  46. 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.Google Scholar
  47. 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.CrossRefGoogle Scholar

Copyright information

© Indian Academy of Sciences 2019

Authors and Affiliations

  • Cheng-Fei Sun
    • 1
    • 2
  • Hai-Lin Sun
    • 1
    • 2
  • Jun-Jian Dong
    • 1
  • Yuan-Yuan Tian
    • 1
  • Jie Hu
    • 1
  • Xing Ye
    • 1
    • 2
    Email author
  1. 1.Key Laboratory of Tropical and Subtropical Fishery Resource Application and Cultivation, Ministry of Agriculture, Pearl River Fisheries Research InstituteChinese Academy of Fishery ScienceGuangzhouPeople’s Republic of China
  2. 2.College of Fisheries and Life ScienceShanghai Ocean UniversityShanghaiPeople’s Republic of China

Personalised recommendations