Skip to main content
Log in

Cloning, tissue expression pattern and daily rhythms of Period1, Period2, and Clock transcripts in the flatfish Senegalese sole, Solea senegalensis

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

An extensive network of endogenous oscillators governs vertebrate circadian rhythmicity. At the molecular level, they are composed of a set of clock genes that participate in transcriptional–translational feedback loops to control their own expression and that of downstream output genes. These clocks are synchronized with the environment, although entrainment by external periodic cues remains little explored in fish. In this work, partial cDNA sequences of clock genes representing both positive (Clock) and negative (Period1, Period2) elements of the molecular feedback loops were obtained from the nocturnal flatfish Senegalese sole, a relevant species for aquaculture and chronobiology. All of the above genes exhibited high identities with their respective teleost clock genes, and Per–Arnt–Sim or basic helix–loop–helix binding domains were recognized in their primary structure. They showed a widespread distribution through the animal body and some of them displayed daily mRNA rhythms in central (retina, optic tectum, diencephalon, and cerebellum) and peripheral (liver) tissues. These rhythms were most robust in retina and liver, exhibiting marked Period1 and Clock daily oscillations in transcript levels as revealed by ANOVA and cosinor analysis. Interestingly, expression profiles were inverted in retina and optic tectum compared to liver. Such differences suggest the existence of tissue-dependent zeitgebers for clock gene expression in this species (i.e., light for retina and optic tectum and feeding time for liver). This study provides novel insight into the location of the molecular clocks (central vs. peripheral) and their different phasing and synchronization pathways, which contributes to better understand the teleost circadian systems and its plasticity.

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
Fig. 7

Similar content being viewed by others

References

  • Balsalobre A (2002) Clock genes in mammalian peripheral tissues. Cell Tissue Res 309:193–199

    Article  PubMed  CAS  Google Scholar 

  • Bayarri MJ, Muñoz-Cueto JA, Lopez-Olmeda JF, Vera LM, Rol de Lama MA, Madrid JA, Sanchez-Vazquez FJ (2004) Daily locomotor activity and melatonin rhythms in Senegal sole (Solea senegalensis). Physiol Behav 81:577–583

    Article  PubMed  CAS  Google Scholar 

  • Besharse JC, Zhuang M, Freeman K, Fogerty J (2004) Regulation of photoreceptor Per1 and Per2 by light, dopamine and a circadian clock. Eur J Neurosci 20:167–174

    Article  PubMed  Google Scholar 

  • Blanco-Vives B, Aliaga-Guerrero M, Cañavate JP, Muñoz-Cueto JA, Sanchez-Vazquez FJ (2011a) Does lighting manipulation during incubation affect hatching rhythms and early development of sole? Chronobiol Int 28:300–306

    Article  PubMed  CAS  Google Scholar 

  • Blanco-Vives B, Vera LM, Ramos J, Bayarri MJ, Mañanos E, Sanchez-Vazquez FJ (2011b) Exposure of larvae to daily thermocycles affects gonad development, sex ratio, and sexual steroids in Solea senegalensis, Kaup. J Exp Zool A Ecol Genet Physiol 315:162–169

    Article  PubMed  CAS  Google Scholar 

  • Blanco-Vives B, Aliaga-Guerrero M, Cañavate JP, García-Mateos G, Martín-Robles AJ, Herrera-Pérez P, Muñoz-Cueto JA, Sánchez-Vázquez FJ (2012) Metamorphosis induces a light-dependent switch in Senegalese sole (Solea senegalensis, Kaup) from diurnal to nocturnal behavior. J Biol Rhythms 27:135–145

    Google Scholar 

  • Cavallari N, Frigato E, Vallone D, Fröhlich N, Lopez-Olmeda JF, Foà A, Berti R, Sánchez-Vázquez FJ, Bertolucci C, Foulkes NS (2011) A blind circadian clock in cavefish reveals that opsins mediate peripheral clock photoreception. PLoS Biol 9:e1001142

    Article  PubMed  CAS  Google Scholar 

  • Cermakian N, Whitmore D, Foulkes NS, Sassone-Corsi P (2000) Asynchronous oscillations of two zebrafish CLOCK partners reveal differential clock control and function. Proc Natl Acad Sci USA 97:4339–4344

    Article  PubMed  CAS  Google Scholar 

  • Challet E, Mendoza J (2010) Metabolic and reward feeding synchronises the rhythmic brain. Cell Tissue Res 341:1–11

    Article  PubMed  Google Scholar 

  • Chaurasia SS, Pozdeyev N, Haque R, Visser A, Ivanova TN, Iuvone PM (2006) Circadian clockwork machinery in neural retina: evidence for the presence of functional clock components in photoreceptor-enriched chick retinal cell cultures. Mol Vis 12:215–223

    PubMed  CAS  Google Scholar 

  • Confente F, Rendon MC, Besseau L, Falcon J, Muñoz-Cueto JA (2010) Melatonin receptors in a pleuronectiform species, Solea senegalensis: cloning, tissue expression, day-night and seasonal variations. Gen Comp Endocrinol 167:202–214

    Article  PubMed  CAS  Google Scholar 

  • Damiola F, Le Minh N, Preitner N, Kornmann B, Fleury-Olela F, Schibler U (2000) Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. Genes Dev 14:2950–2961

    Article  PubMed  CAS  Google Scholar 

  • Falcon J, Migaud H, Muñoz-Cueto JA, Carrillo M (2010) Current knowledge on the melatonin system in teleost fish. Gen Comp Endocrinol 165:469–482

    Article  PubMed  CAS  Google Scholar 

  • Feliciano A, Vivas Y, de Pedro N, Delgado MJ, Velarde E, Isorna E (2011) Feeding time synchronizes clock gene rhythmic expression in brain and liver of goldfish (Carassius auratus). J Biol Rhythms 26:24–33

    Article  PubMed  CAS  Google Scholar 

  • Galtier N, Gouy M, Gautier C (1996) SEAVIEW and PHYLO_WIN: Two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci 12:543–548

    PubMed  CAS  Google Scholar 

  • Guilding C, Piggins HD (2007) Challenging the omnipotence of the suprachiasmatic timekeeper: are circadian oscillators present throughout the mammalian brain? Eur J Neurosci 25:3195–3216

    Article  PubMed  Google Scholar 

  • Hall JC (1995) Tripping along the trail to the molecular mechanisms of biological clocks. Trends Neurosci 18:230–240

    Article  PubMed  CAS  Google Scholar 

  • Helfer G, Fidler AE, Vallone D, Foulkes NS, Brandstaetter R (2006) Molecular analysis of clock gene expression in the avian brain. Chronobiol Int 23:113–127

    Article  PubMed  CAS  Google Scholar 

  • Herrera-Perez P, Rendon MC, Besseau L, Sauzet S, Falcon J, Muñoz-Cueto JA (2010) Melatonin receptors in the brain of the European sea bass: an in situ hybridization and autoradiographic study. J Comp Neurol 518:3495–3511

    Article  PubMed  CAS  Google Scholar 

  • Hirayama J, Sassone-Corsi P (2005) Structural and functional features of transcription factors controlling the circadian clock. Curr Opin Genet Dev 15:548–556

    Article  PubMed  CAS  Google Scholar 

  • Isorna E, El M’rabet A, Confente F, Falcon J, Muñoz-Cueto JA (2009) Cloning and expression of arylalkylamine N-acetyltranferase-2 during early development and metamorphosis in the sole Solea senegalensis. Gen Comp Endocrinol 161:97–102

    Article  PubMed  CAS  Google Scholar 

  • Isorna E, Aliaga-Guerrero M, M’Rabet AE, Servili A, Falcon J, Muñoz-Cueto JA (2011) Identification of two arylalkylamine N-acetyltranferase 1 genes with different developmental expression profiles in the flatfish Solea senegalensis. J Pineal Res 51:434–444

    Google Scholar 

  • Iuvone PM, Tosini G, Pozdeyev N, Haque R, Klein DC, Chaurasia SS (2005) Circadian clocks, clock networks, arylalkylamine N-acetyltransferase, and melatonin in the retina. Prog Retin Eye Res 24:433–456

    Article  PubMed  CAS  Google Scholar 

  • Iuvone PM, Velarde E, Delgado MJ, Alonso-Gomez AL, Haque R (2010) Circadian clocks in retina of goldfish. In: Kulczykowska E, Popek W, Kapoor BG (eds) Biological clock in fish. Science Publisher, Lebanon, pp 251–264

    Chapter  Google Scholar 

  • Kamphuis W, Cailotto C, Dijk F, Bergen A, Buijs RM (2005) Circadian expression of clock genes and clock-controlled genes in the rat retina. Biochem Biophys Res Commun 330:18–26

    Article  PubMed  CAS  Google Scholar 

  • King DP, Zhao Y, Sangoram AM, Wilsbacher LD, Tanaka M, Antoch MP, Steeves TD, Vitaterna MH, Kornhauser JM, Lowrey PL, Turek FW, Takahashi JS (1997) Positional cloning of the mouse circadian clock gene. Cell 89:641–653

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi Y, Ishikawa T, Hirayama J, Daiyasu H, Kanai S, Toh H, Fukuda I, Tsujimura T, Terada N, Kamei Y, Yuba S, Iwai S, Todo T (2000) Molecular analysis of zebrafish photolyase/cryptochrome family: two types of cryptochromes present in zebrafish. Genes Cells 5:725–738

    Article  PubMed  CAS  Google Scholar 

  • Kojima D, Mano H, Fukada Y (2000) Vertebrate ancient-long opsin: a green-sensitive photoreceptive molecule present in zebrafish deep brain and retinal horizontal cells. J Neurosci 20:2845–2851

    PubMed  CAS  Google Scholar 

  • Lahiri K, Foulkes NS (2010) Fishing for links between the circadian clock and cell cycle. In: Kulczykowska E, Popek W, Kapoor BG (eds) Biological clock in fish. Science Publisher, Lebanon, pp 93–110

    Chapter  Google Scholar 

  • Lee C, Etchegaray JP, Cagampang FR, Loudon AS, Reppert SM (2001) Posttranslational mechanisms regulate the mammalian circadian clock. Cell 107:855–867

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Lopez-Olmeda JF, Tartaglione EV, de la Iglesia HO, Sanchez-Vazquez FJ (2010) Feeding entrainment of food-anticipatory activity and per1 expression in the brain and liver of zebrafish under different lighting and feeding conditions. Chronobiol Int 27:1380–1400

    Article  PubMed  Google Scholar 

  • Martin-Robles AJ, Isorna E, Whitmore D, Muñoz-Cueto JA, Pendon C (2011) The clock gene Period3 in the nocturnal flatfish Solea senegalensis: molecular cloning, tissue expression and daily rhythms in central areas. Comp Biochem Physiol A: Mol Integr Physiol 159:7–15

    Article  Google Scholar 

  • Mazurais D, Brierley I, Anglade I, Drew J, Randall C, Bromage N, Michel D, Kah O, Williams LM (1999) Central melatonin receptors in the rainbow trout: comparative distribution of ligand binding and gene expression. J Comp Neurol 409:313–324

    Article  PubMed  CAS  Google Scholar 

  • Menaker M, Moreira LF, Tosini G (1997) Evolution of circadian organization in vertebrates. Braz J Med Biol Res 30:305–313

    Article  PubMed  CAS  Google Scholar 

  • Meyer A, Van de Peer Y (2005) From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). BioEssays 27:937–945

    Article  PubMed  CAS  Google Scholar 

  • Migaud H, Davie A, Martinez Chavez CC, Al-Khamees S (2007) Evidence for differential photic regulation of pineal melatonin synthesis in teleosts. J Pineal Res 43:327–335

    Article  PubMed  CAS  Google Scholar 

  • Miyamoto Y, Sancar A (1999) Circadian regulation of cryptochrome genes in the mouse. Brain Res Mol Brain Res 71:238–243

    Article  PubMed  CAS  Google Scholar 

  • Namihira M, Honma S, Abe H, Masubuchi S, Ikeda M, Honma K-i (2001) Circadian pattern, light responsiveness and localization of rPer1 and rPer2 gene expression in the rat retina. NeuroReport 12:471–475

    Article  PubMed  CAS  Google Scholar 

  • Navarro DB, Rubio VC, Luz RK, Madrid JA, Sanchez-Vazquez FJ (2009) Daily feeding rhythms of Senegalese sole under laboratory and farming conditions using self-feeding systems. Aquaculture 291:130–135

    Article  Google Scholar 

  • Nelson W, Tong YL, Lee JK, Halberg F (1979) Methods for cosinor-rhythmometry. Chronobiologia 6:305–323

    PubMed  CAS  Google Scholar 

  • Oliveira C, Lopez-Olmeda JF, Delgado MJ, Alonso-Gomez AL, Sanchez-Vazquez FJ (2008) Melatonin binding sites in Senegal sole: day/night changes in density and location in different regions of the brain. Chronobiol Int 25:645–652

    Article  PubMed  CAS  Google Scholar 

  • Oliveira C, Dinis MT, Soares F, Cabrita E, Pousao-Ferreira P, Sanchez-Vazquez FJ (2009) Lunar and daily spawning rhythms of Senegal sole Solea senegalensis. J Fish Biol 75:61–74

    Article  PubMed  CAS  Google Scholar 

  • Oliveira C, Duncan NJ, Pousao-Ferreira P, Mananos E, Sanchez-Vazquez FJ (2010) Influence of the lunar cycle on plasma melatonin, vitellogenin and sex steroids rhythms in Senegal sole, Solea senegalensis. Aquaculture 306:343–347

    Article  CAS  Google Scholar 

  • Pando MP, Sassone-Corsi P (2002) Unraveling the mechanisms of the vertebrate circadian clock: zebrafish may light the way. BioEssays 24:419–426

    Article  PubMed  CAS  Google Scholar 

  • Pando MP, Pinchak AB, Cermakian N, Sassone-Corsi P (2001) A cell-based system that recapitulates the dynamic light-dependent regulation of the vertebrate clock. Proc Natl Acad Sci USA 98:10178–10183

    Article  PubMed  CAS  Google Scholar 

  • Park JG, Park YJ, Sugama N, Kim SJ, Takemura A (2007) Molecular cloning and daily variations of the Period gene in a reef fish Siganus guttatus. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 193:403–411

    Article  PubMed  CAS  Google Scholar 

  • Patiño MA, Rodriguez-Illamola A, Conde-Sieira M, Soengas JL, Miguez JM (2011) Daily rhythmic expression patterns of Clock1a, Bmal1, and Per1 genes in retina and hypothalamus of the rainbow trout, Oncorhynchus mykiss. Chronobiol Int 28:381–389

    Article  PubMed  Google Scholar 

  • Peirson SN, Butler JN, Duffield GE, Takher S, Sharma P, Foster RG (2006) Comparison of clock gene expression in SCN, retina, heart, and liver of mice. Biochem Biophys Res Commun 351:800–807

    Article  PubMed  CAS  Google Scholar 

  • Plautz JD, Kaneko M, Hall JC, Kay SA (1997) Independent photoreceptive circadian clocks throughout Drosophila. Science 278:1632–1635

    Article  PubMed  CAS  Google Scholar 

  • Reppert SM, Weaver DR (2002) Coordination of circadian timing in mammals. Nature 418:935–941

    Article  PubMed  CAS  Google Scholar 

  • Sanchez JA, Sanchez-Vazquez FJ (2009) Feeding entrainment of daily rhythms of locomotor activity and clock gene expression in zebrafish brain. Chronobiol Int 26:1120–1135

    PubMed  CAS  Google Scholar 

  • Sanchez JA, Madrid JA, Sanchez-Vazquez FJ (2010) Molecular cloning, tissue distribution, and daily rhythms of expression of per1 gene in European sea bass (Dicentrarchus labrax). Chronobiol Int 27:19–33

    Article  PubMed  CAS  Google Scholar 

  • Shearman LP, Zylka MJ, Weaver DR, Kolakowski LF Jr, Reppert SM (1997) Two period homologs: circadian expression and photic regulation in the suprachiasmatic nuclei. Neuron 19:1261–1269

    Article  PubMed  CAS  Google Scholar 

  • Stokkan KA, Yamazaki S, Tei H, Sakaki Y, Menaker M (2001) Entrainment of the circadian clock in the liver by feeding. Science 291:490–493

    Article  PubMed  CAS  Google Scholar 

  • Tamai TK, Carr AJ, Whitmore D (2005) Zebrafish circadian clocks: cells that see light. Biochem Soc Trans 33:962–966

    Article  PubMed  CAS  Google Scholar 

  • Tosini G, Kasamatsu M, Sakamoto K (2007) Clock gene expression in the rat retina: effects of lighting conditions and photoreceptor degeneration. Brain Res 1159:134–140

    Article  PubMed  CAS  Google Scholar 

  • Tosini G, Pozdeyev N, Sakamoto K, Iuvone PM (2008) The circadian clock system in the mammalian retina. BioEssays 30:624–633

    Article  PubMed  CAS  Google Scholar 

  • Velarde E, Haque R, Iuvone PM, Azpeleta C, Alonso-Gomez AL, Delgado MJ (2009) Circadian clock genes of goldfish, Carassius auratus: cDNA cloning and rhythmic expression of period and cryptochrome transcripts in retina, liver, and gut. J Biol Rhythms 24:104–113

    Article  PubMed  CAS  Google Scholar 

  • Vera LM, De Oliveira C, Lopez-Olmeda JF, Ramos J, Mananos E, Madrid JA, Sanchez-Vazquez FJ (2007) Seasonal and daily plasma melatonin rhythms and reproduction in Senegal sole kept under natural photoperiod and natural or controlled water temperature. J Pineal Res 43:50–55

    Article  PubMed  CAS  Google Scholar 

  • Wang H (2008a) Comparative analysis of period genes in teleost fish genomes. J Mol Evol 67:29–40

    Article  PubMed  CAS  Google Scholar 

  • Wang H (2008b) Comparative analysis of teleost fish genomes reveals preservation of different ancient clock duplicates in different fishes. Mar Genom 1:69–78

    Article  Google Scholar 

  • Whitmore D, Foulkes NS, Strahle U, Sassone-Corsi P (1998) Zebrafish Clock rhythmic expression reveals independent peripheral circadian oscillators. Nat Neurosci 1:701–707

    Article  PubMed  CAS  Google Scholar 

  • Whitmore D, Foulkes NS, Sassone-Corsi P (2000) Light acts directly on organs and cells in culture to set the vertebrate circadian clock. Nature 404:87–91

    Article  PubMed  CAS  Google Scholar 

  • Yamazaki S, Numano R, Abe M, Hida A, Takahashi R, Ueda M, Block GD, Sakaki Y, Menaker M, Tei H (2000) Resetting central and peripheral circadian oscillators in transgenic rats. Science 288:682–685

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Zhdanova IV, Yu L, Lopez-Patiño M, Shang E, Kishi S, Guelin E (2008) Aging of the circadian system in zebrafish and the effects of melatonin on sleep and cognitive performance. Brain Res Bull 75:433–441

    Article  PubMed  CAS  Google Scholar 

  • Zhu H, LaRue S, Whiteley A, Steeves TD, Takahashi JS, Green CB (2000) The Xenopus clock gene is constitutively expressed in retinal photoreceptors. Brain Res Mol Brain Res 75:303–308

    Article  PubMed  CAS  Google Scholar 

  • Zhuang M, Wang Y, Steenhard BM, Besharse JC (2000) Differential regulation of two period genes in the Xenopus eye. Brain Res Mol Brain Res 82:52–64

    Article  PubMed  CAS  Google Scholar 

  • Zylka MJ, Shearman LP, Weaver DR, Reppert SM (1998) Three period homologs in mammals: differential light responses in the suprachiasmatic circadian clock and oscillating transcripts outside of brain. Neuron 20:1103–1110

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the Spanish Ministerio de Ciencia e Innovación (MICINN, AGL2007-66507-C02-01) and Junta de Andalucía (P06-AGR-01939) to José A. Muñoz-Cueto, and a predoctoral fellow of the Spanish MICINN (BES-2005-8629) to Águeda J. Martín-Robles. We thank Francesca Confente for her help in sampling. We also thank all staff from the “Planta de Cultivos Marinos” (University of Cádiz) for maintaining the animals used in these studies. Sequencing analyses were performed in Servicio Central de Ciencia y Tecnología (University of Cádiz). This is the contribution nº 1 from the CEIMAR Journal Publication Series.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Carlos Pendón or José A. Muñoz-Cueto.

Additional information

Communicated by G. Heldmaier.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Martín-Robles, Á.J., Whitmore, D., Sánchez-Vázquez, F.J. et al. Cloning, tissue expression pattern and daily rhythms of Period1, Period2, and Clock transcripts in the flatfish Senegalese sole, Solea senegalensis . J Comp Physiol B 182, 673–685 (2012). https://doi.org/10.1007/s00360-012-0653-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-012-0653-z

Keywords

Navigation