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

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

doi:10.1007/s13131-021-1923-y

Volume 41 Issue 1

Jan. 2022

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Chunyan Zhao, Shihong Xu, Yifan Liu, Chengcheng Feng, Yongshuang Xiao, Yanfeng Wang, Qinghua Liu, Jun Li. Changes of melatonin and its receptors in synchronizing turbot (Scophthalmus maximus) seasonal reproduction and maturation rhythm[J]. Acta Oceanologica Sinica, 2022, 41(1): 84-98. doi: 10.1007/s13131-021-1923-y

Citation:

Chunyan Zhao, Shihong Xu, Yifan Liu, Chengcheng Feng, Yongshuang Xiao, Yanfeng Wang, Qinghua Liu, Jun Li. Changes of melatonin and its receptors in synchronizing turbot (Scophthalmus maximus) seasonal reproduction and maturation rhythm[J]. Acta Oceanologica Sinica, 2022, 41(1): 84-98. doi: 10.1007/s13131-021-1923-y

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

doi: 10.1007/s13131-021-1923-y

Chunyan Zhao^{1, 2, 4},
Shihong Xu^{2, 4},
Yifan Liu^{2, 4},
Chengcheng Feng^{2, 4},
Yongshuang Xiao^{2, 4},
Yanfeng Wang^{2, 4},
Qinghua Liu^{2, 4
,
,},
Jun Li^{2, 3, 4
,}

1.
School of Marine Science and Engineering, Qingdao Agricultural University, Qingdao 266109, China
2.
Key Laboratory of Experimental Marine Biology, Centre for Ocean Mega-Science, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China
3.
Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou 511458, China
4.
Marine Biology and Biotechnology Laboratory, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao 266237, China

Funds: 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.

More Information

Corresponding author: E-mail: qinghualiu@qdio.ac.cn; junli@qdio.ac.cn
Received Date: 2021-02-02
Accepted Date: 2021-05-08

Available Online: 2021-11-08

Publish Date: 2022-01-10

Abstract

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.
- turbot,
- brain,
- melatonin,
- melatonin receptors,
- seasonal reproductive development

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References(61)

References

[1]	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
[2]	Boeuf G, Le Bail P Y. 1999. Does light have an influence on fish growth?. Aquaculture, 177(1–4): 129–152
[3]	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
[4]	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
[5]	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
[6]	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
[7]	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
[8]	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
[9]	Coon S L, Klein D C. 2006. Evolution of arylalkylamine N-acetyltransferase: emergence and divergence. Molecular and Cellular Endocrinology, 252(1–2): 2–10
[10]	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
[11]	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
[12]	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
[13]	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
[14]	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
[15]	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
[16]	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
[17]	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
[18]	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
[19]	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
[20]	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
[21]	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
[22]	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
[23]	Ikegami K, Yoshimura T. 2016. Comparative analysis reveals the underlying mechanism of vertebrate seasonal reproduction. General and Comparative Endocrinology, 227: 64–68
[24]	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
[25]	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
[26]	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
[27]	Kochman K. 2012. Evolution of gonadotropin-releasing hormone (GnRH) structure and its receptor. Journal of Animal and Feed Sciences, 21(1): 3–30
[28]	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
[29]	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
[30]	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
[31]	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
[32]	Mazurais D, Brierley I, Anglade I, et al. 1999. Central melatonin receptors in the rainbow trout: Comparative distribution of ligand binding and gene expression. Journal of Comparative Neurology, 409(2): 313–324
[33]	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
[34]	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
[35]	Nishiwaki-Ohkawa T, Yoshimura T. 2016. Molecular basis for regulating seasonal reproduction in vertebrates. Journal of Endocrinology, 229(3): R117–R127
[36]	Park Y J, Park J G, Hiyakawa N, et al. 2007a. Diurnal and circadian regulation of a melatonin receptor, MT1, in the golden rabbitfish, Siganus guttatus. General and Comparative Endocrinology, 150(2): 253–262
[37]	Park Y J, Park J G, Jeong H B, et al. 2007b. Expression of the melatonin receptor Mel_1c in neural tissues of the reef fish Siganus guttatus. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 147(1): 103–111
[38]	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
[39]	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
[40]	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
[41]	Plant T M. 2015. 60 Years of neuroendocrinology: the hypothalamo-pituitary-gonadal axis. Journal of Endocrinology, 226(2): T41–T54
[42]	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
[43]	Rad F, Bozaoğlu 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
[44]	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
[45]	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: 10.1098/rspb.2015.1745
[46]	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
[47]	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
[48]	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
[49]	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
[50]	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
[51]	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
[52]	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
[53]	Tan Dunxian, Chen Lidun, Poeggeler B, et al. 1993. Melatonin: A potent endogenous hydroxyl radical scavenger. Journal of Pineal Research, 1: 57–60
[54]	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
[55]	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
[56]	Wright M L. 2002. Melatonin, diel rhythms, and metamorphosis in anuran amphibians. General and Comparative Endocrinology, 126(3): 251–254
[57]	Zhang Hongmei, Zhang Yiqiang. 2014. Melatonin: a well-documented antioxidant with conditional pro-oxidant actions. Journal of Pineal Research, 57(2): 131–146
[58]	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
[59]	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
[60]	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
[61]	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