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Chronobiology International
The Journal of Biological and Medical Rhythm Research
Volume 41, 2024 - Issue 3
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Original Article

Circadian patterns and photoperiodic modulation of clock gene expression and neuroendocrine hormone secretion in the marine teleost Larimichthys crocea

, , , , , , , & show all
Pages 329-346 | Received 30 Oct 2023, Accepted 01 Feb 2024, Published online: 18 Feb 2024

References

  • Bani A, Tabarsa M, Falahatkar B, Banan A. 2009. Effects of different photoperiods on growth, stress and haematological parameters in juvenile great sturgeon Huso huso. Aquacult Res. 40:1899–1907. doi: 10.1111/j.1365-2109.2009.02321.x.
  • Bapary MAJ, Fainuulelei P, Takemura A. 2009. Environmental control of gonadal development in the tropical damselfish Chrysiptera cyanea. Marine Bio Res. 5:462–469. doi: 10.1080/17451000802644722.
  • Bayarri MJ, Garcı´a-Allegue R, Lo´pez-Olmeda J, Madrid JA, Sánchez-Vázquez FJ. 2004. Circadian melatonin release in vitro by European sea bass pineal. Fish Physiol Biochem. 30:87–89. doi: 10.1007/s10695-004-6002-8.
  • Begay V, Falcon J, Cahill GM, Klein DC, Coon SL. 1998. Transcripts encoding two melatonin synthesis enzymes in the teleost pineal organ: circadian regulation in pike and zebrafish, but not in trout. Endocrinology. 139:905–912. doi: 10.1210/endo.139.3.5790.
  • Biswas AK, Seoka M, Inoue Y, Takii K, Kumai H. 2005. Photoperiod influences the growth, food intake, feed efficiency and digestibility of red sea bream (Pagrus major). Aquaculture. 250:666–673. doi: 10.1016/j.aquaculture.2005.04.047.
  • Bloch G, Barnes B, Gerkema M, Helm B. 2013. Animal activity around the clock with no overt circadian rhythms: patterns, mechanisms and adaptive value. Proc Biol Sci. 280:20130019. doi: 10.1098/rspb.2013.0019.
  • Bonvini E, Parma L, Gatta PP, Mandrioli L, Sirri R, Martelli G, Nannoni E, Mordenti A, Bonaldo A. 2016. Effects of light intensity on growth, feeding activity and development in common sole (Solea solea L.) larvae in relation to sensory organ ontogeny. Aquacult Res. 47:1809–1819. doi: 10.1111/are.12639.
  • Borja M, Falc6n J, Ravault JP. 1996. Production of melatonin by the gilthead sea bream pineal: an in vivo and in vitro study. Fish Physiol Biochem. 15:413–419. doi: 10.1007/BF01875584.
  • Cahill GM. 2002. Clock mechanisms in zebrafish. Cell Tissue Res. 309:27–34. doi: 10.1007/s00441-002-0570-7.
  • Casey P, Butts IAE, Zadmajid V, Sørensen SR, Litvak MK. 2020. Prolonged photoperiod improves the growth performance for a hatchery reared right-eyed flatfish. Aquacult Eng. 90:102089. doi: 10.1016/j.aquaeng.2020.102089.
  • Cavallari N, Frigato E, Vallone D, Fröhlich N, Lopez-Olmeda JF, Foà A, Berti R, Sánchez-Vázquez FJ, Bertolucci C, Foulkes NS, et al. 2011. A blind circadian clock in cavefish reveals that opsins mediate peripheral clock photoreception. PLoS Biol. 9:e1001142.
  • Collier RJ, Dahl GE, VanBaale MJ. 2006. Major advances associated with environmental effects on dairy cattle. J Dairy Sci. 89:1244–1253. doi: 10.3168/jds.S0022-0302(06)72193-2.
  • Coon S, Begay V, Deurloo D, Falcón J, Klein DC. 1999. Two arylalkylamine n-acetyltransferase genes mediate melatonin synthesis in fish. J Biol Chem. 274:9076–9082. doi: 10.1074/jbc.274.13.9076.
  • Davies W, Tamai T, Zheng L, Fu, J K., Rihel, J., Foster, R G., Whitmore, D., Hankins, M W. 2015. An extended family of novel vertebrate photopigments is widely expressed and displays a diversity of function. Genome Res. doi: 10.1101/gr.189886.115. 25:1666–1679
  • Dibner C, Schibler U, Albrecht U. 2010. The mammalian circadian timing system: organization and coordination of central and peripheral clocks. Annu Rev Physiol. 72:517–549. doi: 10.1146/annurev-physiol-021909-135821.
  • Dunlap JC. 1999. Molecular bases for circadian clocks. Cell. 96:271–290. doi: 10.1016/s0092-8674(00)80566-8.
  • Dvornyk V, Vinogradova O, Nevo E. 2003. Origin and evolution of circadian clock genes in prokaryotes. Proc Natl Acad Sci USA. 100:2495–2500. doi: 10.1073/pnas.0130099100.
  • Ekström P, Meissl H. 1997. The pineal organ of teleost fishes. Rev Fish Bio Fish. 7:199–284. doi: 10.1023/A:1018483627058.
  • Emerson KJ, Bradshaw WE, Holzapfel CM. 2008. Concordance of the circadian clock with the environment is necessary to maximize fitness in natural populations. Evolution. 62:979–983. doi: 10.1111/j.1558-5646.2008.00324.x.
  • Falcon J, Besseau L, Boeuf G. 2006. Molecular and cellular regulation of pineal organ responses. Fish Physiol. 25:243–306. doi: 10.1016/S1546-5098(06)25006-4.
  • Falcon J, Besseau L, Fuentes M, Sauzet S, Magnanou E, Boeuf G. 2009. Structural and functional evolution of the pineal melatonin system in vertebrates. Ann N Y Acad Sci. 1163:101–111. doi: 10.1111/j.1749-6632.2009.04435.x.
  • Falcón J, Migaud H, Muñoz-Cueto J, Carrillo M. 2010. Current knowledge on the melatonin system in teleost fish. Gen Comp Endocrinol. 165:469–482. doi: 10.1016/j.ygcen.2009.04.026.
  • Fernandes AM, Fero K, Driever W, Burgess HA. 2013. Enlightening the brain: linking deep brain photoreception with behavior and physiology. BioEssays. 35:775–779.
  • Gem W, Duvall D, Nervina JM. 1986. Melatonin: a discussion of its evolution and actions in vertebrates. Am Zool. 26:985–996. doi:10.1093/icb/26.4.985.
  • Gupta BBP, Haldar C, Gupta S, Goswami S. 2016. Updates on integrative physiology and comparative endocrinology. Varanasi: Press and Publication Cell, Banaras Hindu University.
  • Huhman KL, Gillespie CF, Marvel CL, Albers HE. 1996. Neuropeptide Y phase shifts circadian rhythms in vivo via a Y2 receptor. Neuroreport. 7:1249–1252. doi: 10.1097/00001756-199605170-00005.
  • Iigo M, Mizusawa K, Yokosuka M, Hara M, Ohtani-Kaneko R, Tabata M, Aida K, Hirata K. 2003. In vitro photic entrainment of the circadian rhythm in melatonin release from the pineal organ of a teleost, ayu (Plecoglossus altivelis) in flow-through culture. Brain Res. 982:131–135. doi: 10.1016/S0006-8993(03)03001-4.
  • Ikegami K, Iigo M, Yoshimura T, Bartell PA. 2013. Circadian clock gene per2 is not necessary for the photoperiodic response in mice. PloS ONE. 8:58482. doi: 10.1371/journal.pone.0058482.
  • Imamura S, Hur S, Takeuchi Y, Badruzzaman M, Mahardini A, Rizky D, Takemura A. 2022. Effect of short- and long-term melatonin treatments on the reproductive activity of the tropical damselfish Chrysiptera cyanea. Fish Physiol Biochem. 48:253–262. doi: 10.1007/s10695-022-01051-x.
  • Inagaki N, Honma S, Ono D, Tanahashi Y, Honma K-I. 2007. Separate oscillating cell groups in mouse suprachiasmatic nucleus couple photoperiodically to the onset and end of daily activity. Proc Natl Acad Sci USA. 104:7664–7669. doi: 10.1073/pnas.0607713104.
  • Ishikawa T, Hirayama J, Kobayashi Y, Todo T. 2002. Zebrafish CRY represses transcription mediated by CLOCK-BMAL heterodimer without inhibiting its binding to DNA. Genes Cells. 7:1073–1086. doi: 10.1046/j.1365-2443.2002.00579.x.
  • Isorna E, Pedro N, Valenciano A, Alonso-Gómez ÁL, Delgado MJ. 2016. Interplay between the endocrine and circadian systems in fishes. J Endocrinol. 232:141–159. doi: 10.1530/JOE-16-0330.
  • Jiang N, Wang Z, Cao J, Dong Y, Chen Y. 2017. Effect of monochromatic light on circadian rhythmic expression of clock genes in the hypothalamus of chick. J Photochem Photobiol B. 173:476–484. doi: 10.1016/j.jphotobiol.2017.06.027.
  • Kong F, Shang J, Ran Z, Zhang M, Liao K, Xu J, Yan X. 2023. Light entrainment and molecular regulation of the circadian clock in razor clam Sinonovacula constricta. Aquaculture. 564:739072. doi: 10.1016/j.aquaculture.2022.739072.
  • Ko C, Takahashi JS. 2006. Molecular components of the mammalian circadian clock. Hum Mol Genet. 15:271–277. doi: 10.1093/hmg/ddl207.
  • Kumar V, Wingfield JC, Dawson A, Ramenofsky M, Rani S, Bartell P. 2010. Biological clocks and regulation of seasonal reproduction and migration in birds. Physiol Biochem Zool. 83:827–835. doi: 10.1086/652243.
  • Kuz’mina VV. 2020. Melatonin. multifunctionality. fish. J Evol Biochem Physiol. 56:89–101. doi: 10.1134/s0022093020020015.
  • Liu Y, Li X, Xu GF, Bai SY, Zhang YQ, Gu W, Mou ZB. 2015. Effect of photoperiod manipulation on the growth performance of juvenile lenok, Brachymystax lenok (Pallas, 1773). J Appl Ichthyol. 31:120–124. doi: 10.1111/jai.12632.
  • Loudon AS. 2012. Circadian biology: a 2.5 billion year old clock. Curr Biol. 22:570–571. doi: 10.1016/j.cub.2012.06.023.
  • Ma H, Liu S, Wei P, Fei F, Ren J, Dai M, Ma Z, Liu Y 2023. Effects of LED spectrum on circadian rhythmic expression of clock genes and aanat2 in the brain of juvenile European seabass (Dicentrarchus labrax). Front Mar Sci. 9. doi: 10.3389/fmars.2022.1005352.
  • Martinez-Chavez C, Al-Khamees S, Campos-Mendoza A, Penman DJ, Migaud H. 2008. Clock-controlled endogenous melatonin rhythms in Nile Tilapia (Oreochromis niloticus niloticus) and African catfish (Clarias gariepinus). Chronobiol Int. 25:31–49. doi: 10.1080/07420520801917547.
  • Matthew PP, Corsi PS. 2002. Unraveling the mechanisms of the vertebrate circadian clock: zebrafish may light the way. BioEssays. 24:419–426. doi: 10.1002/bies.10091.
  • Migaud H, Davie A, Taylor J. 2010. Current knowledge on the photoneuroendocrine regulation of reproduction in temperate fish species. J Fish Biol. 76:27–68. doi: 10.1111/j.1095-8649.2009.02500.x.
  • Mohawk JA, Green CB, Takahashi JS. 2012. Central and peripheral circadian clocks in mammals. Annu Rev Neurosci. 35:445–462. doi: 10.1146/annurev-neuro-060909-153128.
  • Moshe ZB, Alon S, Mracek P, Faigenbloom L, Tovin A, Vatine GD, Eisenberg E, Foulkes NS, Gothilf Y. 2014. The light-induced transcriptome of the zebrafish pineal gland reveals complex regulation of the circadian clockwork by light. Nucleic Acids Res. 42:3749–3767. doi: 10.1093/nar/gkt1359.
  • Okano T, Yamamoto K, Okano K, Hirota T, Kasahara T, Sasaki M, Takanaka Y, Fukada Y. 2001. Chicken pineal clock genes: Implication of BMAL2 as a bidirectional regulator in circadian clock oscillation. Genes Cells. 6:825–836. doi: 10.1046/j.1365-2443.2001.00462.x.
  • Onoue T, Nishi G, Hikima J, Sakai M, Kono T. 2019. Circadian oscillation of TNF-α gene expression regulated by clock gene, BMAL1 and CLOCK1, in the japanese medaka (Oryzias latipes). Int Immunopharmacol. 70:362–371. doi: 10.1016/j.intimp.2019.02.004.
  • Partch CL, Green CB, Takahashi JS. 2013. Molecular architecture of the mammalian circadian clock. Trends Cell Biol. 24:90–99. doi: 10.1016/j.tcb.2013.07.002.
  • Pedrazzini T, Pralong F, Grouzmann E. 2003. Neuropeptide Y: the universal soldier. Cell Mol Life Sci. 60:350–377. doi: 10.1007/s000180300029.
  • Pegoraro M, Tauber E. 2011. Animal clocks: a multitude of molecular mechanisms for circadian timekeeping. Wiley Interdiscip Rev RNA. 2:312–320. doi: 10.1002/wrna.58.
  • Pierce LX, Noche RR, Ponomareua O, Chang C, Liang JO. 2008. Novel functions for period 3 and exo-rhodopsin in rhythmic transcription and melatonin biosynthesis within the zebrafish pineal organ. Brain Res. 1223:11–24. doi: 10.1016/j.brainres.2008.05.020.
  • Pierce LX, Noche RR, Ponomareva O, Chang C, Liang JO. 2008. Novel functions for period 3 and exo-rhodopsin in rhythmic transcription and melatonin biosynthesis within the zebrafish pineal organ. Brain Res. 1223:11–24. doi: 10.1016/j.brainres.2008.05.020.
  • Puvanendran V, Brown JA. 2002. Foraging, growth and survival of atlantic cod larvae reared in different light intensities and photoperiods. Aquaculture. 214:131–151. doi: 10.1016/S0044-8486(02)00045-5.
  • Robertson J, Clifton D, Iglesia H, Steiner RA, Kauffman AS. 2009. Circadian regulation of kiss1 neurons: implications for timing the preovulatory gonadotropin-releasing hormone/luteinizing hormone surge. Endocrinology. 150:3664–3671. doi: 10.1210/en.2009-0247.
  • Ross AW, Russell L, Helfer G, Thomson LM, Dalby MJ, Morgan PJ. 2015. Photoperiod regulates lean mass accretion, but not adiposity, in growing F344 rats fed a high fat diet. PLoS One. 10:e0119763. doi: 10.1371/journal.pone.0119763.
  • Saha S, Singh KM, Gupta BBP. 2019. Melatonin synthesis and clock gene regulation in the pineal organ of teleost fish compared to mammals: similarities and differences. Gen Comp Endocrinol. 279:27–34. doi: 10.1016/j.ygcen.2018.07.010.
  • Sanchez VFJ, Iigo M, Madrid JA, Tabata M. 2000. Pinealectomy does not affect the entrainment to light nor the generation of the circadian demand-feeding rhythms of rainbow trout. Physiol Behav. 69:455–461. doi: 10.1016/S0031-9384(99)00250-4.
  • Sánchez-Vázquez FJ, Iigo M, Madrid JA, Migaud H, López-Patiño MA, Míguez JM. 2019. Environmental cycles, melatonin, and circadian control of stress response in fish. Front Endocrinol. 10:279. doi: 10.3389/fendo.2019.00279.
  • Sanjita Devi H, Rajiv C, Mondal G, Khan ZA, Devi SD, Bharali R, Chattoraj A. 2022. Influence of photoperiod variations on the mRNA expression pattern of melatonin bio-synthesizing enzyme genes in the pineal organ and retina: a study in relation to the serum melatonin profile in the tropical carp Catla catla. J Fish Biol. 101:1569–1581. doi: 10.1111/jfb.15234.
  • Takeuchi Y, Hada N, Imamura S, Hur S-P, Bouchekioua S, Takemura A. 2015. Existence of a photoinducible phase for ovarian development and photoperiod-related alteration of clock gene expression in a damselfish. Comp Biochem Physiol A Mol Integr Physiol. 188:32–39. doi: 10.1016/j.cbpa.2015.06.010.
  • Tamai T, Carr A, Whitmore D. 2005. Zebrafish circadian clocks: cells that see light. Biochem Soc Trans. 33:962–966. doi: 10.1042/BST0330962.
  • Touitou Y. 2016. The circadian system in man: from the internal clock to melatonin secretion. Ann Pharm Fr. 74:331–334. doi: 10.1016/j.pharma.2016.02.001.
  • Turkowska E, Majewski PM, Rai S, Skwarlo-Sonta K. 2014. Pineal oscillator functioning in the chicken–effect of photoperiod and melatonin. Chronobiol Int. 31:134–143. doi: 10.3109/07420528.2013.832279.
  • Vatine G, Vallone D, Gothilf Y, Foulkes, N S. 2011. It’s time to swim! Zebrafish and the circadian clock. FEBS Lett. 585:1485–1494. doi: 10.1016/j.febslet.2011.04.007.
  • Villamizar N, Alcazar AG, V´azquez FJS. 2009. Effect of light spectrum and photoperiod on the growth, development and survival of European sea bass (Dicentrarchus labrax) larvae. Aquaculture. 202:80–86. doi: 10.1016/j.aquaculture.2009.03.045.
  • Welsh DK, Takahashi JS, Kay SA. 2010. Suprachiasmatic nucleus: cell autonomy and network properties. Annu Rev Physiol. 72:551–577. doi: 10.1146/annurev-physiol-021909-135919.
  • Wu L-L, Han M-M, Song Z-C, Xu S, Li J, Li X, Wang Y, Yue X, Li X. 2019. Effects of different light spectra on embryo development and the performance of newly hatched turbot (Scophthalmus maximus) larvae. Fish Shellfish Immunol. 90:328–337. doi: 10.1016/j.fsi.2019.05.007.
  • Wu L-L, Wang Y-N, Han M-M, Song Z, Song C, Xu S, Li J, Wang Y, Li X, Yue X, et al. 2020. Growth, stress and non-specific immune responses of turbot (Scophthalmus maximus) larvae exposed to different light spectra. Aquaculture. 520:734950. doi: 10.1016/j.aquaculture.2020.734950.
  • Yee Hang C, Kitahashi T, Parhar IS. 2016. Neuronal organization of deep brain opsin photoreceptors in adult teleosts. Front Neuroanat. 10:48. doi: 10.3389/fnana.2016.00048.
  • Ying L, Guang L, Haifang W, Du J, Yan J. 2013. Analysis of a gene regulatory cascade mediating circadian rhythm in zebrafish. PLoS Comput Biol. 9:e1002940. doi: 10.1371/journal.pcbi.1002940.
  • Yoshimura T, Suzuki Y, Makino E, Suzuki T, Kuroiwa A, Matsuda Y, Namikawa T, Ebihara S. 2000. Molecular analysis of avian circadian clock genes. Brain Res Mol Brain Res. 78:207–215. doi: 10.1016/s0169-328x(00)00091-7.
  • Yuan Q, Metterville D, Briscoe AD, Reppert SM. 2007. Insect cryptochromes: gene duplication and loss define diverse ways to construct insect circadian clocks. Mol Biol Evol. 24:948–955. doi: 10.1093/molbev/msm01.
  • Zhdanova IV, Reebs SG. 2012. Circadian clocks: lessons from fish. Prog Brain Res. 199:41–57. doi: 10.1016/B978-0-444-59427-3.00003-4.

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