Skip to main content
Log in

Molecular cloning, characterization, and mRNA expression of gonadotropins during larval development in turbot (Scophthalmus maximus)

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

Gonadotropins (GtHs) play a pivotal role in regulating the reproductive axis and puberty. In this study, full-length sequences coding for common glycoprotein α subunit (CGα) and luteinizing hormone β (LHβ) were isolated from female turbot (Scophthalmus maximus) pituitary by homology cloning and a strategy based on rapid amplification of cDNA end-polymerase chain reaction. Results showed that the two cDNAs consisted of 669 and 660 nucleotides encoding 129 and 139 amino acids, respectively. CGα and LHβ manifested typical characteristics of glycoprotein hormones, high homologies with the corresponding sequences of available teleosts, and high homology with that of Hippoglossus hippoglossus. CGα, FSHβ, and LHβ mRNAs were abundant in the pituitary, but less expressed in extra-pituitary tissues. The cgα, fshβ, and lhβ were detected at 1-day post-hatching (dph) and peaked simultaneously at early-metamorphosis (22 dph). cgα and fshβ mRNA levels were significantly increased at pre-metamorphosis, peaked in early metamorphosis, and then gradually decreased until metamorphosis was completed. Conversely, lhβ mRNA levels gradually decreased at pre-metamorphosis, dramatically peaked at early metamorphosis, and then decreased during metamorphosis. In addition, the mRNA levels of cgα were significantly higher than those of fshβ and lhβ during turbot larval metamorphic development, whereas no significant difference was found between fshβ and lhβ. These results suggested (i) an early activation of the GtHs system after hatching, which was the highest expression at early metamorphosis, and (ii) FSHβ and LHβ were together involved in the establishment of the reproductive axis during larval development in turbot. These findings contribute to further understanding the potential roles of GtHs during fish larval development.

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
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Arey BJ, Stevis PE, Deecher DC, Shen ES, Frail DE, Negro-Vilar A, Lopez FJ (1997) Induction of promiscuous G protein coupling of the follicle-stimulating hormone (FSH) receptor: a novel mechanism for transducing pleiotropic actions of FSH isoforms. Mol Endocrinol 11:517–526

    Article  CAS  Google Scholar 

  • Chen W, Ge W (2012) Ontogenic expression profiles of gonadotropins (fshb and lhb) and growth hormone (gh) during sexual differentiation and puberty onset in female zebrafish. Biol Reprod 86(73):1–11

    CAS  Google Scholar 

  • Fan HG, Wang DS, Kobayashi T, Senthilkumaran B, Sudhakumari CC, Yoshikuni M, Nagahama Y (2003) Molecular cloning of the three gonadotropin subunits and early expression of FSHβ during sex differentiation in the Nile tilapia, Oreochromis niloticus. Fish Physiol Biochem 28:143–144

    Article  CAS  Google Scholar 

  • FAO (2012) Fisheries department, fishery information, data and statistics unit. Fishstat plus: universal software for fishery statistical time series. Version. 2.3 2000:FAO Aquaculture Production (Quantities and values) 1950-2010 (Release date: April 2010)

  • García-Ayala A, Villaplana M, García-Hernández MP, Chaves-Pozo E, Agulleiro B (2003) FSH-, LH-, and TSH-expressing cells during development of Sparus aurata L. (Teleostei): an immunocytochemical study. Gen Comp Endocrinol 134:72–79

    Article  Google Scholar 

  • Gen K, Okuzawa K, Senthilkumaran B, Tanaka H, Moriyama S, Kagawa H (2000) Unique expression of gonadotropin-I and -II subunit genes in male and female red seabream (Pagrus major) during sexual maturation. Biol Reprod 63:308–319

    Article  CAS  Google Scholar 

  • Gomez JM, Weil C, Ollitrault M, Le Bail PY, Breton B, Le Gac F (1999) Growth hormone (GH) and gonadotropin subunit gene expression and pituitary and plasma changes during spermatogenesis and oogenesis in rainbow trout (Oncorhynchus mykiss). Gen Comp Endocrinol 113:413–428

    Article  CAS  Google Scholar 

  • Guzmán JM, Bayarri MJ, Ramos J, Zohar Y, Sarasquete C, Mañanós EL (2009) Follicle stimulating hormone (FSH) and luteinizing hormone (LH) gene expression during larval development in Senegalese sole (Solea senegalensis). Comp Biochem Physiol A 154:37–43

    Article  Google Scholar 

  • Jia YD, Meng Z, Liu XF, Lei JL (2014a) Biochemical composition and quality of turbot (Scophthalmus maximus) eggs throughout the reproductive season. Fish Physiol Biochem 40:1093–1104

    Article  CAS  Google Scholar 

  • Jia YD, Meng Z, Niu HX, Hu P, Lei JL (2014b) Molecular cloning, characterization, and expression analysis of luteinizing hormone receptor gene in turbot (Scophthalmus maximus). Fish Physiol Biochem 40:1639–1650

    Article  CAS  Google Scholar 

  • Jia YD, Sun A, Meng Z, Liu BL, Lei JL (2016) Molecular characterization and quantification of the follicle-stimulating hormone receptor in turbot (Scophthalmus maximus). Fish Physiol Biochem 42:179–191

    Article  CAS  Google Scholar 

  • Kanda S, Okubo K, Oka Y (2011) Differential regulation of the luteinizing hormone genes in teleosts and tetrapods due to their distinct genomic environments-insights into gonadotropin beta subunit evolution. Gen Comp Endocrinol 173:253–258

    Article  CAS  Google Scholar 

  • Kim HK, Kim JH, Baek HJ, Kwon JY (2016) Gene expression of aromatases, steroid receptor, GnRH and GTHs in the brain during the formation of ovarian cavity in red spotted grouper, Epinephelus akaara. Dev Rep 20:367–377

    Article  Google Scholar 

  • Levavi-Sivan B, Bogerd J, Mañanós EL, Gómez A, Lareyre JJ (2010) Perspectives on fish gonadotropins and their receptors. Gen Comp Endocrinol 165:412–437

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real time quantitative PCR and the 2-∆∆CT method. Methods 25:402–408

    Article  CAS  Google Scholar 

  • Meiri I, Knibb WR, Zohar Y, Elizur A (2004) Temporal profile of beta follicle-stimulating hormone, beta luteinizing hormone, and growth hormone gene expression in the protandrous hermaphrodite, gilthead seabream, Sparus aurata. Gen Comp Endocrinol 137:288–299

    Article  CAS  Google Scholar 

  • Meng Z, Hu P, Lei JL, Jia YD (2016) Expression of insulin-like growth factors at mRNA levels during the metamorphic development of turbot (Scophthalmus maximus). Gen Comp Endocrinol 235:11–17

    Article  CAS  Google Scholar 

  • Miranda LA, Strüssmann CA, Somoza GM (2001) Immunocytochemical identification of GtH1 and GtH2 cells during the temperature-sensitive period for sex determination in pejerrey, Odontesthes bonariensis. Gen Comp Endocrinol 124:45–52

    Article  CAS  Google Scholar 

  • Nocillado JN, Elizur A (2010) Neuroendocrine regulation of puberty in fish: insights from the grey mullet (Mugil cephalus) model. Mol Reprod Dev 75:355–361

    Article  Google Scholar 

  • Nozaki M, Naito N, Swanson P, Miyata K, Nakai Y, Oota Y, Suzuki K, Kawauchi H (1990) Salmonid pituitary gonadotropins I. distinct cellular distributions of two gonadotropins, GtH I and GtH II. Gen Comp Endocrinol 77:348–357

    Article  CAS  Google Scholar 

  • Pandolfi M, Lo Nostro F, Shimizu A, Pozzi AG, Meijide FJ, Vazquez GR, Maggese MC (2006) Identification of immunoreactive FSH and LH cells in the cichlid fish Cichlasoma dimerus during the ontogeny and sexual differentiation. Anat Embryol 211:355–365

    Article  Google Scholar 

  • Parhar IS, Soga T, Ogawa S, Sakuma Y (2003) FSH and LH-beta subunits in the preoptic nucleus: ontogenic expression in teleost. Gen Comp Endocrinol 132:369–378

    Article  CAS  Google Scholar 

  • Piñuela C, Rendón C, Ml GDC, Sarasquete C (2004) Development of the Senegal sole, Solea senegalensis forebrain. Eur J Histochem 48:377

    PubMed  Google Scholar 

  • Planas JV, Athos J, Goetz FW, Swanson P (2000) Regulation of ovarian steroidogenesis in vitro by follicle-stimulating hormone and luteinizing hormone during sexual maturation in salmonid Fish1. Biol Reprod 62:1262–1269

    Article  CAS  Google Scholar 

  • Saga T, Oota Y, Nozaki M, Swanson P (1993) Salmonid pituitary gonadotrophs, III. Chronological appearance of GTH I and other adenohypophysial hormones in the pituitary of the developing rainbow trout (Oncorhynchus mykiss irideus). Gen Comp Endocrinol 92:233–241

    Article  CAS  Google Scholar 

  • Schulz RW, Zandbergen MA, Peute J, Bogerd J, van Dijk W, Goos HJ (1997) Pituitary gonadotrophs are strongly activated at the beginning of spermatogenesis in African catfish, Clarias gariepinus. Biol Reprod 57:139–147

    Article  CAS  Google Scholar 

  • Schulz RW, de França LR, Lareyre J, LeGac F, Chiarini-Garcia H, Nobrega RH, Miura T (2010) Spermatogenesis in fish. Gen Comp Endocrinol 165:390–411

    Article  CAS  Google Scholar 

  • Scobell SK, MacKenzie DS (2011) Reproductive endocrinology of Syngnathidae. J Fish Biol 78:1662–1680

    Article  CAS  Google Scholar 

  • So WK, Kwok HF, Ge W (2005) Zebrafish gonadotropins and their receptors: II. Cloning and characterization of zebrafish follicle-stimulating hormone and luteinizing hormone subunits—their spatial-temporal expression patterns and receptor specificity1. Biol Reprod 72:1382–1396

    Article  CAS  Google Scholar 

  • Swanson P, Dickey JT, Campbell B (2003) Biochemistry and physiology of fish gonadotropins. Fish Physiol Biochem 28:53–59

    Article  CAS  Google Scholar 

  • Tobet SA, Nozaki M, Youson JH, Sower SA (1995) Distribution of lamprey gonadotropin-releasing hormone-III (GnRH-III) in brains of larval lampreys (Petromyzon marinus). Cell Tissue Res 279:261–270

    Article  CAS  Google Scholar 

  • Weltzien FA, Kobayashi T, Andersson E, Norberg B, Andersen Ø (2003) Molecular characterization and expression of FSHβ, LHβ, and common α-subunit in male Atlantic halibut (Hippoglossus hippoglossus). Gen Comp Endocrinol 131:87–96

    Article  CAS  Google Scholar 

  • Weltzien FA, Hildahl J, Hodne K, Okubo K, Haug TM (2014) Embryonic development of gonadotrope cells and gonadotropic hormones-lessons from model fish. Mol Cell Endocrinol 385:18–27

    Article  CAS  Google Scholar 

  • Wong TT, Zohar Y (2004) Novel expression of gonadotropin subunit genes in oocytes of the gilthead seabream (Sparus aurata). Endocrinology 145:5210–5220

    Article  CAS  Google Scholar 

  • Yaron Z (1995) Endocrine control of gametogenesis and spawning induction in the carp. Aquaculture 129:49–73

    Article  CAS  Google Scholar 

  • Yaron Z, Gur G, Melamed P, Rosenfeld H, Elizur A, Levavisivan B (2003) Regulation of fish gonadotropins. Int Rev Cytol 225:131–185

    Article  CAS  Google Scholar 

Download references

Funding

This study was supported by the National Natural Science Foundation of China (31302205), China Agriculture Research System (CARS-47-G24), and Shandong Major Science and Technology Innovation Projects (2018YFJH0703).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yudong Jia.

Additional information

Publisher’s note

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

Electronic supplementary material

ESM 1

(DOCX 1445 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gao, Y., Jing, Q., Huang, B. et al. Molecular cloning, characterization, and mRNA expression of gonadotropins during larval development in turbot (Scophthalmus maximus). Fish Physiol Biochem 45, 1697–1707 (2019). https://doi.org/10.1007/s10695-019-00656-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-019-00656-z

Keywords

Navigation