Skip to main content
SpringerLink
Log in

The sbGnRH–GTH system in the female short mackerel, Rastrelliger brachysoma (Bleeker, 1851), during breeding season: implications for low gamete production in captive broodstock

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

Abstract

The short mackerel (Rastrelliger brachysoma) is one of the most economically important fish in Thailand; it is also a prime candidate for mariculture but unfortunately is plagued by reproductive problems that cause low production of gametes in captivity. An understanding of how the brain, pituitary, and gonad axis (BPG) from the neuroendocrine system are involved in the reproductive activity of wild and captive R. brachysoma should help clarify the situation. In this study, we investigated changes in the sea bream gonadotropin-releasing hormone (sbGnRH)–gonadotropin (GTH) system in the female short mackerel, Rastrelliger brachysoma (Bleeker, 1851), during breeding season. sbGnRH-immunoreactive (ir) cell bodies were detected in the nucleus preopticus-periventricularis including nucleus periventricularis (NPT), nucleus preopticus (Np), and nucleus lateralis tuberis (NLT). Additionally, the sbGnRH-ir fibers protruded into the proximal par distalis (PPD) where GTH (FSH and LH) cells were detected. The number of sbGnRH-ir cell bodies and GTH cells and level of LH mRNA were significantly higher in the breeding season than those in the non-breeding season. Moreover, the number of sbGnRH-ir cell bodies and GTH cells and levels of sbGnRH and GTH (FSH and LH) mRNA were significantly higher in the wild fish than those in the cultured broodstock. It is suggested that the wild fish tended to have better reproductive system than hatchery fishes. This could be related to the endocrinological dysfunction and the reproductive failure in the hatchery condition. Moreover, the changes of all of the hormonal level could potentially be applied to R. brachysoma aquaculture.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Amano M, Oka Y, Yamanome T, Okuzawa K, Yamamori K (2002) Three GnRH systems in the brain and pituitary of a pleuronectiform fish, the barfin flounder Verasper moseri. Cell Tissue Res 309:323–329

    Article  CAS  PubMed  Google Scholar 

  • Amano M, Okubo K, Yamanome T, Yamada H, Aida K, Yamamori K (2004) Changes in brain GnRH mRNA and pituitary GnRH peptide during testicular maturation in barfin flounder. Comp Biochem Physiol B 138:435–443

    Article  CAS  PubMed  Google Scholar 

  • Amaral J, de Melo R, Honji R, Moreira R (2007) Effects of migration impediment of Salminus hilarii (Teleost: Characidae) on the pituitary–gonad axis. Comp Biochem Physiol A Mol Integr Physiol 148:S44

    Article  Google Scholar 

  • Bancroft JD, Gamble M (2008) Theory and practice of histological techniques, 6th ed. Churchill Livingstone/Elsevier, Philadelphia

  • Becker D, Galili N, Degani G (1992) Gcns- identified steroids and steroids goucoronides in gonads and holding water in gonads and holding water of trichogaster tricopterus (anabantidea, pallas 1770). Comp Biochem Physiol 103B:15–19

    CAS  Google Scholar 

  • Blazer V (2002) Histopathological assessment of gonadal tissue in wild fishes. Fish Physiol Biochem 26:85–101

    Article  CAS  Google Scholar 

  • Degani G (1993) The effect of sexual behavior on oocyte development and steroid changes in trichogaster trichopterus. Copeia 4:1091–1096

    Article  Google Scholar 

  • Degani G (2001) Blue gourami (Trichogaster trichopterus) model for labyrinth fish. Laser Pages Publishing, Israel, pp 1–134

    Google Scholar 

  • Degani G (2016) Oogenesis control in multi-spawning blue gourami (trichogaster trichopterus) as a model for the anabantidae family internal. J Sci Res 5:179–184

    Google Scholar 

  • Dietrich D, Kriegerp HO (2009) Chapter 8: evaluation of effects in fish gonads. In: Histological analysis of endocrine disruptive effects in small laboratory fish. Willey & Sons Inc, p 254–269

  • Fernald RD, White RB (1999) Gonadotropin-releasing hormone genes: phylogeny, structure, and functions. Front Neuroendocrinol 20:224–240

    Article  CAS  PubMed  Google Scholar 

  • Forniés M, Carrillo M, Mañanós E, Sorbera LA, Zohar Y, Zanuy S (2003) Relative potency of the forms of GnRH and their analogs on LH release in sea bass. J Fish Biol 63:73–89

    Article  CAS  Google Scholar 

  • González-Martínez D, Madigou T, Zmora N, Anglade I, Zanuy S, Zohar Y, Elizur A, Muñoz-Cueto JA, Kah O (2001) Differential expression of three different prepro-GnRH (gonadotrophin-releasing hormone) messengers in the brain of the european sea bass (Dicentrarchus labrax). J Comp Neurol 429:144–155

    Article  PubMed  Google Scholar 

  • González-Martínez D, Zmora N, Mañanos E, Saligaut D, Zanuy S, Zohar Y, Elizur A, Kah O, Muñoz-Cueto JA (2002) Immunohistochemical localization of three different prepro-GnRHs in the brain and pituitary of the European sea bass (Dicentrarchus labrax) using antibodies to the corresponding GnRH-associated peptides. J Comp Neurol 446:95–113

    Article  CAS  PubMed  Google Scholar 

  • Gothilf Y, Meiri I, Elizur A, Zohar Y (1997) Preovulatory changes in the levels of three gonadotropin-releasing hormone-encoding messenger ribonucleic acids (mRNAs), gonadotropin beta-subunit mRNAs, plasma gonadotropin, and steroids in the female gilthead seabream, Sparus aurata. Biol Reprod 57:1145–1154

    Article  CAS  PubMed  Google Scholar 

  • Guilgur LG, Moncaut NP, Canário AV, Somoza GM (2006) Evolution of GnRH ligands and receptors in gnathostomata. Comp Biochem Physiol A Mol Integr Physiol 144:272–283

    Article  CAS  PubMed  Google Scholar 

  • Guzmán JM, Rubio M, Ortiz-Delgado JB, Klenke U, Kight K, Cross I, Sánchez-Ramos I, Riaza A, Rebordinos L, Sarasquete C (2009) Comparative gene expression of gonadotropins (FSH and LH) and peptide levels of gonadotropin-releasing hormones (GnRHs) in the pituitary of wild and cultured Senegalese sole (Solea senegalensis) broodstocks. Comp Biochem Physiol A Mol Integr Physiol 153:266–277

    Article  CAS  PubMed  Google Scholar 

  • Hernández MPG, Ayala AG, Zandbergen MA, Agulleiro B (2002) Investigation into the duality of gonadotropic cells of Mediterranean yellowtail (Seriola dumerilii, Risso 1810): immunocytochemical and ultrastructural studies. Gen Comp Endocrinol 128:25–35

    Article  CAS  Google Scholar 

  • Honji R, Narcizo A, Borella M, Romagosa E, Moreira R (2009) Patterns of oocyte development in natural habitat and captive Salminus hilarii Valenciennes, 1850 (Teleostei: Characidae). Fish Physiol Biochem 35:109–123

    Article  CAS  PubMed  Google Scholar 

  • Honji RM, Mello PH, Araújo BC, Rodrigues-Filho JA, Hilsdorf AW, Moreira RG (2011) Influence of spawning procedure on gametes fertilization success in Salminus hilarii Valenciennes, 1850 (Teleostei: Characidae): implications for the conservation of this species. Neotrop Ichthy 9:363–370

    Article  Google Scholar 

  • Humason GL (1979) Animal Tissue Techniques. 4th. Freeman, San Francisco

    Google Scholar 

  • Imanaga Y, Nyuji M, Amano M, Takahashi A, Kitano H, Yamaguchi A, Matsuyama M (2014) Characterization of gonadotropin-releasing hormone and gonadotropin in jack mackerel (Trachurus japonicus): comparative gene expression analysis with respect to reproductive dysfunction in captive and wild fish. Aquaculture 428:226–235

    Article  CAS  Google Scholar 

  • Jackson K, Abraham M, Degani G (1994) Oocyte maturation triggered by the male in a tropical fish trichogaster trichopterus. J Morphol 220:1–9

    Article  PubMed  Google Scholar 

  • Kagawa H, Tanaka H, Okuzawa K, Kobayashi M (1998) GTH II but not GTH I induces final maturation and the development of maturational competence of oocytes of red seabream in vitro. Gen Comp Endocrinol 112:80–88

    Article  CAS  PubMed  Google Scholar 

  • Kah O, Anglade I, Leprêtre E, Dubourg P, de Monbrison D (1993) The reproductive brain in fish. Fish Physiol Biochem 11:85–98

    Article  CAS  PubMed  Google Scholar 

  • Kah O, Lethimonier C, Somoza G, Guilgur L, Vaillant C, Lareyre JJ (2007) GnRH and GnRH receptors in metazoa: a historical, comparative, and evolutive perspective. Gen Comp Endocrinol 153:346–364

    Article  CAS  PubMed  Google Scholar 

  • Kauffman AS, Rissman EF (2004) A critical role for the evolutionarily conserved gonadotropin-releasing hormone II: mediation of energy status and female sexual behavior. Endocrinology 145:3639–3646

    Article  CAS  PubMed  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 

  • Levy G, Degani G (2011) Evidence for a reproduction-related function of pituitary adenylate cyclase-activating polypeptide-related peptide (prp) in an anabantidae fish. J Mol Endocrinol 46:1–11

    Article  CAS  Google Scholar 

  • Levy G, Degani G (2012) Involvement of gnrh, pacap and prp in the reproduction of blue gourami females (trichogaster trichopterus). J Mol Neurosci 48:9730–9738

    Article  CAS  Google Scholar 

  • Levy G, David D, Degani G (2011) Effect of environmental temperature on growth- and reproduction-related hormone gene expression in the female blue gourami (trichogaster trichopterus). Comp Biochem Physiol A 160:381–389

    Article  CAS  Google Scholar 

  • Miranda LA, Strüssm 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  PubMed  Google Scholar 

  • Mousa HA, Mousa MA (1999) Immunocytochemical and histological studies on the hypophyseal‐gonadal system in the freshwater Nile Tilapia, Oreochromis niloticus (L.), during sexual maturation and spawning in different habitats. J Exp Zool 284:343–354

  • Naito N, Hyodo S, Okumoto N, Urano A, Nakai Y (1991) Differential production and regulation of gonadotropins (GTH I and GTH II) in the pituitary gland of rainbow trout, Oncorhynchus mykiss, during ovarian development. Cell Tissue Res 266:457–467

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Nyuji M, Shiraishi T, Selvaraj S, Van In V, Kitano H, Yamaguchi A, Okamoto K, Onoue S, Shimizu A, Matsuyama M (2011) Immunoreactive changes in pituitary FSH and LH cells during seasonal reproductive and spawning cycles of female chub mackerel Scomber japonicus. Fish Sci 77:731–739

    Article  CAS  Google Scholar 

  • Nyuji M, Shiraishi T, Kitano H, Irie S, Yamaguchi A, Matsuyama M (2012) Induction of final oocyte maturation and ovulation in jack mackerel, Trachurus japonicus, temporarily reared in captivity. J Fac Agric Kyushu Univ 57:427–430

    Google Scholar 

  • Oakley AE, Clifton DK, Steiner RA (2009) Kisspeptin signaling in the brain. Endocrinol Rev Esp Herp 30:713–743

    Article  CAS  Google Scholar 

  • Okuzawa K, Granneman J, Bogerd J, Goos HT, Zohar Y, Kagawa H (1997) Distinct expression of GnRH genes in the red seabream brain. Fish Physiol Biochem 17:71–79

    Article  CAS  Google Scholar 

  • Palevitch O, Abraham E, Borodovsky N, Levkowitz G, Zohar Y, Gothilf Y (2009) Nasal embryonic LHRH factor plays a role in the developmental migration and projection of gonadotropin-releasing hormone 3 neurons in zebrafish. Dev Dyn 238:66–75

    Article  CAS  PubMed  Google Scholar 

  • Palmieri G, Acone F, Desantis S, Corriero A, Ventriglia G, Addis P, Genovese S, Aprea A, Spedicato D, Losurdo M (2008) Brain morphology and immunohistochemical localization of the gonadotropin-releasing hormone in the bluefin tuna, Thunnus thynnus. Eur J Histochem 52:19

    Article  CAS  PubMed  Google Scholar 

  • Peter R, Crim L, Billard R (1991) A stereotaxic atlas and implantation technique for nuclei of the diencephalon of Atlantic salmon (Salmo salar) parr. Reprod Nutr Dev 31:167–186

    Article  CAS  PubMed  Google Scholar 

  • Pham KX, Amano M, Kurita Y, Shimizu A, Fujinami Y, Amiya N, Yamamori K (2008) Changes in the immunostaining intensities of follicle-stimulating hormone and luteinizing hormone during ovarian maturation in the female Japanese flounder. Fish Physiol Biochem 34:357–365

    Article  CAS  PubMed  Google Scholar 

  • Planas JV, Swanson P, Dickhoff WW (1993) Regulation of testicular steroid production in vitro by gonadotropins (GTH I and GTH II) and cyclic AMP in coho salmon (Oncorhynchus kisutch). Gen Comp Endocrinol 91:8–24

    Article  CAS  PubMed  Google Scholar 

  • Powell J, Zohar Y, Elizur A, Park M, Fischer W, Craig A, Rivier J, Lovejoy D, Sherwood N (1994) Three forms of gonadotropin-releasing hormone characterized from brains of one species. Proc Natl Acad Sci 91:12081–12085

  • Quérat B, Tonnerre-Doncarli C, Géniès F, Salmon C (2001) Duality of gonadotropins in gnathostomes. Gen Comp Endocrinol 124:308–314

    Article  CAS  PubMed  Google Scholar 

  • Rosenfeld H, Meiri I, Elizur A (2007) Gonadotropic regulation of oocyte development. In: Patrick J, Cerdà, BJ, Lubzens E (eds) The fish oocyte: from basic studies to biotechnological applications. Springer, Dordrecht, p 175–20

  • Selvaraj S, Kitano H, Fujinaga Y, Amano M, Takahashi A, Shimizu A, Yoneda M, Yamaguchi A, Matsuyama M (2009) Immunological characterization and distribution of three GnRH forms in the brain and pituitary gland of chub mackerel (Scomber japonicus). Zool Sci 26:828–839

    Article  CAS  PubMed  Google Scholar 

  • Selvaraj S, Kitano H, Amano M, Nyuji M, Kaneko K, Yamaguchi A, Matsuyama M (2012) Molecular characterization and expression profiles of three GnRH forms in the brain and pituitary of adult chub mackerel (Scomber japonicus) maintained in captivity. Aquaculture 356:200–210

    Article  CAS  Google Scholar 

  • Senarat S, Kettretad J, Jiraungkoorskul W (2017) Ovarian histology and reproductive health of short mackerel, Rastrelliger brachysoma (Bleeker, 1851), as threatened marine fish in Thailand. Songklanakarin. J Sci Technol 39:225–235

    Google Scholar 

  • Sherwood NM, Adams BA (2005) Gonadotropin-releasing hormone in fish: evolution, expression and regulation of the GnRH gene. Hormones and their receptors in fish reprod 4: 1–39

  • Shimizu A, Tanaka H, Kagawa H (2003) Immunocytochemical applications of specific antisera raised against synthetic fragment peptides of mummichog GtH subunits: examining seasonal variations of gonadotrophs (FSH cells and LH cells) in the mummichog and applications to other acanthopterygian fishes. Gen Comp Endocrinol 132:35–45

    Article  CAS  PubMed  Google Scholar 

  • Shiraishi T, Ohta K, Yamaguchi A, Yoda M, Chuda H, Matsuyama M (2005) Reproducti.ve parameters of the chub mackerel Scomber japonicus estimated from human chorionic gonadotropin-induced final oocyte maturation and ovulation in captivity. Fish Sci 71:531–542

    Article  CAS  Google Scholar 

  • Temple JL, Millar RP, Rissman EF (2003) An evolutionarily conserved form of gonadotropin-releasing hormone coordinates energy and reproductive behavior. Endocrinology 144:13–19

    Article  CAS  PubMed  Google Scholar 

  • Tyler C, Sumpter J, Kawauchi H, Swanson P (1991) Involvement of gonadotropin in the uptake of vitellogenin into vitellogenic oocytes of the rainbow trout, Oncorhynchus mykiss. Gen Comp Endocrinol 84:291–299

    Article  CAS  PubMed  Google Scholar 

  • Wilson JM, Bunte RM, Carty AJ (2009) Evaluation of rapid cooling and tricaine methanesulfonate (MS222) as methods of euthanasia in zebrafish (Danio rerio). J Am Assoc Lab Anim Sci 48:785–789

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Z, Chen YF (2004) Induced ovulation in obscure puffer Takifugu obscurus by injections of LHRH-a. Aquacult Int 12:215–223

    Article  CAS  Google Scholar 

  • Zohar Y, Muñoz-Cueto J, Elizur A, Kah O (2010) Neuroendocrinology of reproduction in teleost fish. Gen Comp Endocrinol 165:438–455

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors are especially thankful to Ms. Piyakorn Boonyoung, Mr. Kanda Tongmitr, and the members of the Aquatic toxicology Unit, Department of Pathobiology, Faculty of Science, Mahidol University, for their technical support in laboratory.

Funding

This research was financially supported by The 100th Anniversary Chulalongkorn University Fund for Doctoral Scholarship.

Author information

Authors and Affiliations

  1. Department of Marine Science, Faculty of Science, Chulalongkorn University, Bangkok, 10330, Thailand

    Sinlapachai Senarat, Jes Kettratad & F. Gerald Plumley

  2. Department of Pathobiology, Faculty of Science, Mahidol University, Bangkok, 10400, Thailand

    Niwat Kangwanrangsan & Wannee Jiraungkoorskul

  3. School of Marine Biosciences, Kitasato University, Sagamihara, Kanagawa, 252-0373, Japan

    Masafumi Amano

  4. National Research Institute of Fisheries Science, Fukuura 2-12-4, Kanazawa, Yokohama, 236-8648, Japan

    Akio Shimizu

  5. Samut Songkhram Marine Fisheries Research and Development Station, Department of Fisheries, Samut Songkhram, 75000, Thailand

    Sasipong Tipdomrongpong

Authors
  1. Sinlapachai Senarat
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jes Kettratad
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Niwat Kangwanrangsan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Wannee Jiraungkoorskul
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Masafumi Amano
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Akio Shimizu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. F. Gerald Plumley
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Sasipong Tipdomrongpong
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jes Kettratad.

Additional information

The original version of this article was revised due to outdated Figures 1 to 7. The updated Figures were loaded in this version.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Senarat, S., Kettratad, J., Kangwanrangsan, N. et al. The sbGnRH–GTH system in the female short mackerel, Rastrelliger brachysoma (Bleeker, 1851), during breeding season: implications for low gamete production in captive broodstock. Fish Physiol Biochem 45, 1–18 (2019). https://doi.org/10.1007/s10695-018-0509-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-018-0509-x

Keywords

Search

Navigation