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Changes of melatonin and its receptors in synchronizing turbot (Scophthalmus maximus) seasonal reproduction and maturation rhythm

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  • Marine Biology
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Abstract

In most fish, reproduction is seasonal or periodic under the suitable conditions. In turbot (Scophthalmus maximus) farms, one of the most economically important marine flatfish species, changes in daylength could cause changes in the spawning time. In this study, to characterize the regulation of reproductive physiology following light signals, three melatonin receptors (Mtnr) investigated in turbot were named smMtnr1, smMtnr2, and smMtnr1c. Distinct expression profiles demonstrated that Mtnr mRNAs were concentrated in the brain (as detected in the hypothalamus (Hy) and mesencephalon (Me)), gonad and eye. The most abundant Mtnr1 and Mtnr2 mRNA expression levels were detected in the central nervous system at the beginning of the breeding season, suggesting that Mtnr1 and Mtnr2 may play vital roles in the regulation of turbot gonadal development. In addition, the melatonin profiles gradually increased and reached to the highest level at the spawning stage, indicating that melatonin is a potent hormone in the regulation of fish oocyte growth and maturation. The results of this study suggested that melatonin is the primary factor that transduces the light signal and regulates the physiological functions of turbot seasonal reproduction. Moreover, the results of this study may establish a foundation for further research seeking to identify fish melatonin receptors involved in the gonadal development and gamete maturation.

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References

  • Alvariño J M R, Rebollar P G, Olmedo M, et al. 2001. Effects of melatonin implants on reproduction and growth of turbot broodstock. Aquaculture International, 9(6): 477–487

    Article  Google Scholar 

  • Boeuf G, Le Bail P Y. 1999. Does light have an influence on fish growth?. Aquaculture, 177(1–4): 129–152

    Article  Google Scholar 

  • Carnevali O, Gioacchini G, Piccinetti C C, et al. 2010. Melatonin control of oogenesis and metabolic resources in Zebrafish. Journal of Applied Ichthyology, 26(5): 826–830

    Article  Google Scholar 

  • Chai Ke, Liu Xiaochun, Zhang Yong, et al. 2013. Day-night and reproductive cycle profiles of melatonin receptor, kiss, and gnrh expression in orange-spotted grouper (Epinephelus coioides). Molecular Reproduction and Development, 80(7): 535–548

    Article  Google Scholar 

  • Chattoraj A, Seth M, Basu A, et al. 2009. Temporal relationship between the circulating profiles of melatonin and ovarian steroids under natural photo-thermal conditions in an annual reproductive cycle in carp Catla catla. Biological Rhythm Research, 40(4): 347–359

    Article  Google Scholar 

  • Choi C Y, Shin H S, Kim N N, et al. 2015. Time-related effects of various LED light spectra on reproductive hormones in the brain of the goldfish Carassius auratus. Biological Rhythm Research, 46(5): 671–682

    Article  Google Scholar 

  • Ciani E, Fontaine R, Maugars G, et al. 2019. Melatonin receptors in Atlantic salmon stimulate cAMP levels in heterologous cell lines and show season-dependent daily variations in pituitary expression levels. Journal of Pineal Research, 67(3): e12590

    Article  Google Scholar 

  • Confente F, Rendón M C, Besseau L, et al. 2010. Melatonin receptors in a pleuronectiform species, Solea senegalensis: Cloning, tissue expression, day-night and seasonal variations. General and Comparative Endocrinology, 167(2): 202–214

    Article  Google Scholar 

  • Coon S L, Klein D C. 2006. Evolution of arylalkylamine N-acetyltransferase: emergence and divergence. Molecular and Cellular Endocrinology, 252(1–2): 2–10

    Article  Google Scholar 

  • Danilova N, Krupnik V E, Sugden D, et al. 2004. Melatonin stimulates cell proliferation in zebrafish embryo and accelerates its development. The FASEB Journal, 18(6): 751–753

    Article  Google Scholar 

  • Davies B, Hannah L T, Randall C F, et al. 1994. Central melatonin binding sites in rainbow trout (Onchorhynchus mykiss). General and Comparative Endocrinology, 96(1): 19–26

    Article  Google Scholar 

  • Elakkanai P, Francis T, Ahilan B, et al. 2015. Role of GnRH, HCG and Kisspeptin on reproduction of fishes. Indian Journal of Science and Technology, 8(17): 65166

    Article  Google Scholar 

  • Falcón J, Besseau L, Sauzet S, et al. 2007. Melatonin effects on the hypothalamo-pituitary axis in fish. Trends in Endocrinology & Metabolism, 18(2): 81–88

    Article  Google Scholar 

  • Falcón J, Migaud H, Munoz-Cueto J A, et al. 2010. Current knowledge on the melatonin system in teleost fish. General and Comparative Endocrinology, 165(3): 469–482

    Article  Google Scholar 

  • Forés R, Iglesias J, Olmedo M, et al. 1990. Induction of spawning in turbot (scophthalmus maximus L.) by a sudden change in the photoperiod. Aquacultural Engineering, 9(5): 357–366

    Article  Google Scholar 

  • Forsell J, Holmqvist B O, Helvik J V, et al. 1997. Role of the pineal organ in the photoregulated hatching of the Atlantic halibut. International Journal of Developmental Biology, 41(4): 591–595

    Google Scholar 

  • Gaeta L M, Tozzi G, Pastore A, et al. 2002. Determination of superoxide dismutase and glutathione peroxidase activities in blood of healthy pediatric subjects. Clinica Chimica Acta, 322(1–2): 117–120

    Article  Google Scholar 

  • Galano A, Tan D X, Reiter R J. 2013. On the free radical scavenging activities of melatonin’s metabolites, AFMK and AMK. Journal of Pineal Research, 54(3): 245–257

    Article  Google Scholar 

  • Gopurappilly R, Ogawa S, Parhar I S. 2013. Functional significance of GnRH and kisspeptin, and their cognate receptors in teleost reproduction. Frontiers in Endocrinology, 4: 24

    Article  Google Scholar 

  • Hastings M H, Walker A P, Herbert J. 1987. Effect of asymmetrical reductions of photoperiod on pineal melatonin, locomotor activity and gonadal condition of male syrian hamsters. Journal of Endocrinology, 114(2): 221–229

    Article  Google Scholar 

  • Hong Luyan, Hong Wanshu, Zhu Wenbo, et al. 2014. Cloning and expression of melatonin receptors in the mudskipper Boleophthalmus pectinirostris: their role in synchronizing its semilunar spawning rhythm. General and Comparative Endocrinology, 195: 138–150

    Article  Google Scholar 

  • Ikegami T, Azuma K, Nakamura M, et al. 2009. Diurnal expressions of four subtypes of melatonin receptor genes in the optic tectum and retina of goldfish. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 152(2): 219–224

    Article  Google Scholar 

  • Ikegami K, Yoshimura T. 2016. Comparative analysis reveals the underlying mechanism of vertebrate seasonal reproduction. General and Comparative Endocrinology, 227: 64–68

    Article  Google Scholar 

  • Imsland A K, Gunnarsson S, Roth B, et al. 2013. Long-term effect of photoperiod manipulation on growth, maturation and flesh quality in turbot. Aquaculture, 416–417: 152–160

    Article  Google Scholar 

  • Kim B H, Hur S P, Hyeon J Y, et al. 2020. Annual patterns of ocular melatonin level in the female grass puffer, Takifugu alboplumbeus: possible involvement in seasonal reproductive response. Fish Physiology and Biochemistry, 46(3): 787–801

    Article  Google Scholar 

  • Kim J H, Park J W, Kwon J Y. 2018. Effects of exogenous melatonin on the reproductive activities of Nile tilapia, Oreochromis niloticus. Biological Rhythm Research, 49(3): 392–404

    Article  Google Scholar 

  • Kochman K. 2012. Evolution of gonadotropin-releasing hormone (GnRH) structure and its receptor. Journal of Animal and Feed Sciences, 21(1): 3–30

    Article  Google Scholar 

  • Kulczykowska E, Kalamarz H, Warne J M, et al. 2006. Day-night specific binding of 2-[125I] iodomelatonin and melatonin content in gill, small intestine and kidney of three fish species. Journal of Comparative Physiology B, 176(4): 277–285

    Article  Google Scholar 

  • Lan-Chow-Wing O, Confente F, Herrera-Pérez P, et al. 2014. Distinct expression profiles of three melatonin receptors during early development and metamorphosis in the flatfish Solea senegalensis. International Journal of Molecular Sciences, 15(11): 20789–20799

    Article  Google Scholar 

  • Maitra S K, Chattoraj A, Mukherjee S, et al. 2013. Melatonin: A potent candidate in the regulation of fish oocyte growth and maturation. General and Comparative Endocrinology, 181: 215–222

    Article  Google Scholar 

  • Maitra S K, Hasan K N. 2016. The role of melatonin as a hormone and an antioxidant in the control of fish reproduction. Frontiers in Endocrinology, 7: 38

    Article  Google Scholar 

  • Mazurais D, Brierley I, Anglade I, et al. 1999. Central melatonin receptors in the rainbow trout: Comparative distribution of lig- and binding and gene expression. Journal of Comparative Neurology, 409(2): 313–324

    Article  Google Scholar 

  • Moniruzzaman M, Hasan K N, Maitra S K. 2016. Melatonin actions on ovaprim (synthetic GnRH and domperidone)—induced oocyte maturation in carp. Reproduction, 151(4): 285–296

    Article  Google Scholar 

  • Moniruzzaman M, Maitra S K. 2012. Influence of altered photoperiods on serum melatonin and its receptors (MT1 and MT2) in the brain, retina, and ovary in carp Catla catla. Chronobiology International, 29(2): 175–188

    Article  Google Scholar 

  • Nishiwaki-Ohkawa T, Yoshimura T. 2016. Molecular basis for regulating seasonal reproduction in vertebrates. Journal of Endocrinology, 229(3): R117–R127

    Article  Google Scholar 

  • Park Y J, Park J G, Hiyakawa N, et al. 2007a. Diurnal and circadian regulation of a melatonin receptor, MT1, in the golden rabbit-fish, Siganus guttatus. General and Comparative Endocrinology, 150(2): 253–262

    Article  Google Scholar 

  • Park Y J, Park J G, Jeong H B, et al. 2007b. Expression of the melatonin receptor Mel1c in neural tissues of the reef fish Siganus guttatus. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 147(1): 103–111

    Article  Google Scholar 

  • Park Y J, Park J G, Kim S J, et al. 2006. Melatonin receptor of a reef fish with lunar-related rhythmicity: cloning and daily variations. Journal of Pineal Research, 41(2): 166–174

    Article  Google Scholar 

  • Patiño M A L, Alonso-Gómez A L, Guijarro A, et al. 2008. Melatonin receptors in brain areas and ocular tissues of the teleost Tinca tinca: Characterization and effect of temperature. General and Comparative Endocrinology, 155(3): 847–856

    Article  Google Scholar 

  • Peleteiro-Alonso J B, Rodríguez-Ojea G, Iglesias-Estévez J. 1995. Spawning control in different turbot (Scophthalmus maximus L.) broodstock groups under artificial and natural photoperiods. In: ICES Marine Science Symposium 201. Copenhagen: ICES, 202–203

    Google Scholar 

  • Plant T M. 2015. 60 Years of neuroendocrinology: the hypothalamopituitary-gonadal axis. Journal of Endocrinology, 226(2): T41–T54

    Article  Google Scholar 

  • Power D M, Llewellyn L, Faustino M, et al. 2001. Thyroid hormones in growth and development of fish. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 130(4): 447–459

    Google Scholar 

  • Rad F, Bozaoglu S, Gözükara S E, et al. 2006. Effects of different long-day photoperiods on somatic growth and gonadal development in Nile tilapia (Oreochromis niloticus L.). Aquaculture, 255(1–4): 292–300

    Article  Google Scholar 

  • Reppart S M, Weaver D R, Godson C. 1996. Melatonin receptors step into the light: Cloning and classification of subtypes. Trends in Pharmacological Sciences, 17(3): 100–102

    Article  Google Scholar 

  • Robert K A, Lesku J A, Partecke J, et al. 2015. Artificial light at night desynchronizes strictly seasonal reproduction in a wild mammal. Proceedings of the Royal Society B: Biological Sciences, 282(1816): 20151745, doi: https://doi.org/10.1098/rspb.2015.1745

    Article  Google Scholar 

  • Rocha R M P, Lima L F, Alves A M C V, et al. 2013. Interaction between melatonin and follicle-stimulating hormone promotes in vitro development of caprine preantral follicles. Domestic Animal Endocrinology, 44(1): 1–9

    Article  Google Scholar 

  • Rodriguez C, Mayo J C, Sainz R M, et al. 2004. Regulation of antioxidant enzymes: a significant role for melatonin. Journal of Pineal Research, 36(1): 1–9

    Article  Google Scholar 

  • Sébert M E, Legros C, Weltzien F A, et al. 2008. Melatonin activates brain dopaminergic systems in the eel with an inhibitory impact on reproductive function. Journal of Neuroendocrinology, 20(7): 917–929

    Article  Google Scholar 

  • Sauzet S, Besseau L, Perez P H, et al. 2008. Cloning and retinal expression of melatonin receptors in the European sea bass, Dicentrarchus labrax. General and Comparative Endocrinology, 157(2): 186–195

    Article  Google Scholar 

  • Shin H S, Kim N N, Lee J, et al. 2011. Diurnal and circadian regulations by three melatonin receptors in the brain and retina of olive flounder Paralichthys olivaceus: profiles following exogenous melatonin. Marine and Freshwater Behaviour and Physiology, 44(4): 223–238

    Article  Google Scholar 

  • Soares J M, Jr, Masana M I, Erşahin Ç, et al. 2003. Functional melatonin receptors in rat ovaries at various stages of the estrous cycle. The Journal of Pharmacology and Experimental Therapeutics, 306(2): 694–702

    Article  Google Scholar 

  • Tamura H, Takasaki A, Miwa I, et al. 2008. Oxidative stress impairs oocyte quality and melatonin protects oocytes from free radical damage and improves fertilization rate. Journal of Pineal Research, 44(3): 280–287

    Article  Google Scholar 

  • Tan Dunxian, Chen Lidun, Poeggeler B, et al. 1993. Melatonin: A potent endogenous hydroxyl radical scavenger. Journal of Pineal Research, 1: 57–60

    Google Scholar 

  • Tsutsui K, Ubuka T, Son Y L, et al. 2015. Contribution of GnIH research to the progress of reproductive neuroendocrinology. Frontiers in Endocrinology, 6: 179

    Article  Google Scholar 

  • Vuilleumier R, Besseau L, Boeuf G, et al. 2006. Starting the zebrafish pineal circadian clock with a single photic transition. Endocrinology, 147(5): 2273–2279

    Article  Google Scholar 

  • Wright M L. 2002. Melatonin, diel rhythms, and metamorphosis in anuran amphibians. General and Comparative Endocrinology, 126(3): 251–254

    Article  Google Scholar 

  • Zhang Hongmei, Zhang Yiqiang. 2014. Melatonin: a well-documented antioxidant with conditional pro-oxidant actions. Journal of Pineal Research, 57(2): 131–146

    Article  Google Scholar 

  • Zhao Chunyan, Liu Qinghua, Xu Shihong, et al. 2018a. Identification of type A spermatogonia in turbot (Scophthalmus maximus using a new cell-surface marker of Lymphocyte antigen 75 (ly75/CD205). Theriogenology, 113: 137–145

    Article  Google Scholar 

  • Zhao Chunyan, Xu Shihong, Feng Chengcheng, et al. 2018b. Characterization and differential expression of three GnRH forms during reproductive development in cultured turbot Schophthalmus maximus. Journal of Oceanology and Limnology, 36(4): 1360–1373

    Article  Google Scholar 

  • Zhu Dongmei, Yang Kun, Gul Y, et al. 2014. Effect of photoperiod on growth and gonadal development of juvenile Topmouth Gudgeon Pseudorasbora parva. Environmental Biology of Fishes, 97(2): 147–156

    Article  Google Scholar 

  • Ziv L, Gothilf Y. 2006. Circadian time-keeping during early stages of development. Proceedings of the National Academy of Sciences of the United States of America, 103(11): 4146–4151

    Article  Google Scholar 

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Funding

Foundation item: The National Natural Science Foundation of China under contract No. 31802319; the Key Special Project for Introduced Talents Team of Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou) under contract No. GML2019ZD0402; the National Key Research and Development Program under contract No. 2018YFD0901204; the Major Agricultural Application Technology Innovation Project of Shandong Province under contract No. SD2019YY011; the Natural Science Foundation of Shandong Province under contract No. ZR2018BC053; the Marine S&T Fund of Shandong Province for Pilot National Laboratory for Marine Science and Technology (Qingdao) under contract No. 2018SDKJ0502-2; the Fund of China Agriculture Research System under contract No. CARS-47; the Major Science and Technology for Scientific and Technological Innovation Projects (Shandong) under contract No. 2019JZZY020710; the Science and Technology Service Network Initiative Project under contract Nos KFZD-SW-106, ZSSD-019, 2017T3017 and 2019T3022; the Advanced Talents Foundation of Qingdao Agricultural University under contract No. 6631119055.

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Authors and Affiliations

  1. School of Marine Science and Engineering, Qingdao Agricultural University, Qingdao, 266109, China

    Chunyan Zhao

  2. Key Laboratory of Experimental Marine Biology, Centre for Ocean Mega-Science, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, 266071, China

    Chunyan Zhao, Shihong Xu, Yifan Liu, Chengcheng Feng, Yongshuang Xiao, Yanfeng Wang, Qinghua Liu & Jun Li

  3. Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou, 511458, China

    Jun Li

  4. Marine Biology and Biotechnology Laboratory, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao, 266237, China

    Chunyan Zhao, Shihong Xu, Yifan Liu, Chengcheng Feng, Yongshuang Xiao, Yanfeng Wang, Qinghua Liu & Jun Li

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  1. Chunyan Zhao
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  2. Shihong Xu
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  3. Yifan Liu
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Correspondence to Qinghua Liu or Jun Li.

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Zhao, C., Xu, S., Liu, Y. et al. Changes of melatonin and its receptors in synchronizing turbot (Scophthalmus maximus) seasonal reproduction and maturation rhythm. Acta Oceanol. Sin. 41, 84–98 (2022). https://doi.org/10.1007/s13131-021-1923-y

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