Seasonal variations in clock -gene expression in atlantic salmon (Salmo Salar)

Chronobiology International

Volumn 26, Issue 3, 2009, Pages 379-395

  Davie, Andrew ^a   Minghetti, Matteo ^a   Migaud, Herve ^a  

^a UNIVERSITY OF STIRLING   (United Kingdom)

Author keywords

Atlantic salmon; Circadian clock; Clock; Per2; Photoperiodism; Salmo salar

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; ATLANTIC SALMON; BMAL1 GENE; BRAIN; CLOCK GENE; CONTROLLED STUDY; CRY2 GENE; FEMALE; GENE; GENE EXPRESSION; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PER2 GENE; PHOTOPERIODICITY; SEASONAL VARIATION; ZEBRA FISH;

ANIMALS; BASE SEQUENCE; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CIRCADIAN RHYTHM; FEMALE; GENE EXPRESSION; MALE; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PHOTOPERIOD; RNA, MESSENGER; SALMON; SEASONS; TRANS-ACTIVATORS;

DANIO RERIO; SALMO SALAR; TELEOSTEI; VERTEBRATA;

EID: 67651148046     PISSN: 07420528     EISSN: 15256073     Source Type: Journal    
DOI: 10.1080/07420520902820947     Document Type: Article

References (71)

1. Allendorf FW, Thorgaard GH. (1984). Tetraploidy and the evolution of salmonid fishes. In Turner BJ (ed.) Evolutionary genetics of fishes. New York: Plenum, pp. 1-46.
2. Aubin-Horth N, Landry CR, Letcher BH, Hormann HA. (2005). Alternative life histories shape brain gene expression profiles in males of the same population. P. Roy. Soc. Lond. B. Bio. 272: 1655-1662.
3. Bhattacharya S, Chattoraj A, Maitra SK. (2007). Melatonin in the regulation of annual testcular events in carp Catla catla: Evidence from studies on the effects of exogenous melatonin, continuous light, and continuous darkness. Chronobiol. Int. 24:629-650.
4. Bolliet V, Ali MA, Lapointe F-J, Falcon J. (1996). Rhythmic melatonin secretion in different teleost species: An in vitro study. J. Comp. Physiol. B 165B:677-683.
5. Brandstatter R. (2003). Encoding time of day and time of year by the avian circadian system. J. Neuroendocrinol. 15:398-404.
6. Brierley I, Mazurais D, Drew J, Morgan P, Ross A, Anglade I, Randall C, Bromage N, Kah O, Williams LM. (1999). Melatonin receptor and PER1 gene expression in the teleost fish brain. In Norberg B, Kjesbu OS, Taranger GL, Andersson E, Stefansson SO (eds.) Reproductive physiology of fish. Bergen, Norway: John Grieg AS, p. 341.
7. Bromage N, Porter M, Randall C. (2001). The environmental regulation of maturation in farmed finfish, with special reference to the role of photoperiod and melatonin. Aquaculture 197:63-98.
8. Cahill GM. (2002). Clock mechanisms in zebrafish. Cell Tissue Res. 309:27-34.
9. Carr A-JF, Johnston JD, Semikhodskii AG, Nolan T, Cagampang FRA, Stirland JA, Loudon ASI. (2003). Photoperiod differentially regulates circadian oscillators in central and peripheral tissues of the Syrian hamster. Curr. Biol. 13:1543-1548.
10. Cermakian N, Whitmore D, Foulkes NS, Sassone-Corsi P. (2000). Asynchronous oscillations of two zeb-rafish CLOCK partners reveal differential clock control and function. PNAS 97:4339-4344.
11. Chemineau P, Malpaux B, Brillard JP, Fostier A. (2007). Seasonality of reproduction and production in farm fishes, birds and mammals. Animal 1:419-432.
12. Daan S, Merrow M, Roenneberg T. (2002). External time-internal time. J. Biol. Rhythm 17:107-109.
13. Dardente H, Cermakian N. (2007). Molecular circadian rhythms in central and peripheral clocks in mammals. Chronobiol. Int. 24:195-213.
14. Duffield GE. (2003). DNA microarray analyses of circadian timing: The genomic basis of biological time. J. Neuroendocrinol. 15:991-1002.
15. Dunlap JC. (1999). Molecular bases for circadian clocks. Cell 96:271-290.
16. Duston J, Bromage N. (1988). The entrainment and gating of the endogenous circannual rhythm of reproduction in the female rainbow trout (Salmo gairdneri). J. Comp. Physiol. A 164:259-268.
17. Duston J, Saunders RL. (1992). Effects of 6-, 12-, and 18-month photoperiod cycles on smolting and sexual maturation in juvenile Atlantic salmon (Salmo salar). Can. J. Fish. Aquat. Sci. 49:2273-2280.
18. Eriksson LO, Lundqvist H. (1982). Circannual rhythms and photoperiod regulation of growth and smolting in Baltic salmon. Salmo salar L. Aquaculture 128:113-121.
19. Falcon J, Besseau L, Sauzet S, Boeuf G. (2007). Melatonin effects on the hypothalamo-pituitary axis in fish. Trends Endocrinol. Metab. 18:81-88.
20. Felsenstein J. (1985). Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39: 783-791.
21. Foster RG. (2002). Photoentrainment of vertebrate circadian rhythms. In Kumar V (ed.) Biological rhythms. New Delhi, India: Springer-Verlag, pp. 107-119.
22. Foster RG, Kreitzman L. (2005). Rhythms of life: The biological clocks that control the daily lives of every living thing. London: Profile Books Ltd., 288 pages.
23. Gern WA, Greenhouse SS, Nervina JM, Gasser PJ. (1992). The rainbow trout pineal organ: An endocrine photometer. In Ali M (ed.) Rhythms in fishes. New York: Plenum Press, pp. 199-219.
24. 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.
25. Holmqvist Bo I, Ostholm T, Ekstrom P. (1992). Retinohypothalamic projections and the suprachiasmatic nucleus in the teleost brain. In Ali MA (ed.) Proceedings of a NATO Advanced Study Institute on rhythms in fishes: Rhythms in fishes. New York: Plenum Press, pp. 293-318.
26. Iigo M, Abe T, Kambayashi S, Oikawa K, Masuda T, Mizusawa K, Kitamura S, Azuma T, Takagi Y, Aida K, Yanagisawa T. (2007). Lack of circadian regulation of in vitro melatonin release from the pineal organ of salmonid teleosts. Gen. Comp. Endocrinol. 154:91-97.
27. Johnston JD, Ebling FJP, Hazlerigg DG. (2005). Photoperiod regulates multiple gene expression in the suprachiasmatic nuclei and pars tuberalis of the Siberian hamster (Phodopus sungorus). Eur. J. Neurosci. 21:2967-2974.
28. 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.
29. Larkin P, Baehr W, Semple-Rowland SL. (1999). Circadian regulation of iodopsin and clock is altered in the retinal degeneration chicken retina. Mol. Brain Res. 70:253-263.
30. Leder EH, Danzmann RG, Ferguson MM. (2006). The candidate gene, clock, localizes to a strong spawning time quantitative trait locus region in rainbow trout. J. Hered. 97:74-80.
31. Lincoln G, Messager S, Andersson H, Hazlerigg D. (2002). Temporal expression of seven clock genes in the suprachiasmatic nucleus and the pars tuberalis of the sheep: Evidence for an internal coincidence timer. PNAS 99:13890-13895.
32. Lincoln G, Andersson H, Loudon A. (2003). Clock genes in calendar cells as the basis of annual timekeeping in mammals - a unifying hypothesis. J. Endocrinol. 179:1-13.
33. Mayer I, Bornestaf C, Borg B. (1997). Melatonin in non-mammalian vertebrates: Physiological role in reproduction? Comp. Biochem. Phys. A. 118A:515-531.
34. Mazurais D, Drean GL, Brierley I, Anglade I, Bromage N, Williams LM, Kah O. (2000). Expression of clock gene in the brain of rainbow trout: Comparison with the distribution of melatonin receptors. J. Comp. Neurol. 422:612-620.
35. Messager S, Hazlerigg DG, Mercer JG, Morgan PJ. (2000). Photoperiod differentially regulates the expression of Per1 and ICER in the pars tuberalis and the suprachiasmatic nucleus of the Siberian hamster. Eur. J. Neurosci. 12:2865-2870.
36. Meseguer C, Ramos J, Bayarri MJ, Oliveira C, Sánchez- Válquez FJ. (2008). Light synchronization of the daily spawning rhythms of gilthead sea bream (Sparus aurata L) kept under different photo-period and after shifting the LD cycle. Chronobiol. Int. 25:666-679.
37. Migaud H, Davie A, Chavez CC, Al-Khamees S. (2007). Evidence for differential photic regulation of pineal melatonin synthesis in teleosts. J. Pineal Res. 43:327-335.
38. O'Malley KG, Camara MD, Banks MA. (2007). Candidate loci reveal genetic differentiation between temporally divergent migratory runs in Chinook salmon (Oncorhynchus tshawytscha). Mol. Ecol. 16:4930-4941.
39. Pando MP, Sassone-Corsi P. (2002). Unravelling the mechanisms of the vertebrate circadian clock: Zeb-rafish may light the way. Bioessays 24:419-426.
40. 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. PNAS 98:10178-10183.
41. 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 193:403-411.
42. Portaluppi F, Touitou Y, Smolensky MH. (2008). Ethical and methodological standards for laboratory and medical chronobiology research. Chronobiol. Int. 25:999-1016.
43. Porter MJR, Randall CF, Bromage NR. (1996). The effect of pineal removal on circulating melatonin levels in Atlantic salmon parr. J. Fish Biol. 48:1011-1013.
44. Porter MJR, Randall CF, Bromage NR, Thorpe JE. (1998). The role of melatonin and the pineal gland on development and smoltification of Atlantic salmon (Salmo salar) parr. Aquaculture 168:139-155.
45. Porter MJR, Duncan N, Stefansson SO, Bromage N. (2001). Temperature, light intensity and plasma melatonin levels in juvenile Atlantic salmon. J. Fish Biol. 58:431-438.
46. Randall CF, Bromage NR, Thorpe JE, Miles MS, Muir JS. (1995). Melatonin rhythms in Atlantic salmon, Salmo salar, maintained under natural and out-of-phase photoperiods. Gen. Comp. Endocrinol. 98:73-86.
47. Randall CF, Bromage NR, Duston J, Symes J. (1998). Photoperiod induced phase-shifts of the endogenous clock controlling reproduction in rainbow trout: A circannual phase-response curve. J. Reprod. Fertil. 112:399-405.
48. Saitou N, Neil M. (1987). The neighbour-joining method: A new method for reconstructing phyloge-netic trees. Mol. Biol. Evol. 4:406-425.
49. Sanchez-Vazquez FJ, Tabata M. (1998). Circadian rhythms in demand feeding and locomotor activity in rainbow trout. J. Fish Biol. 52:255-267.
50. Steinlechner S, Jacobmeier B, Scherbarth F, Dernbach H, Kruse F, Albrecht U. (2002). Robust circadian rhythmicity of Per1 and Per2 mutant mice in constant light, and dynamics of Per1 and Per2 gene expression under long and short photoperiods. J. Biol. Rhythms 17:202-209.
51. Stewart DC, Smith GW, Youngson AF. (2002). Tributary-specific variation in timing of return of adult Atlantic salmon (Salmo salar) to fresh water has a genetic component. Can. J. Fish. Aquat. Sci. 59: 276-281.
52. Stewart DC, Middlemas SJ, Youngson AF. (2006). Population structuring in Atlantic salmon (Salmo salar): Evidence of genetic influence on the timing of smolt migration in sub-catchment stocks. Ecol. Freshw. Fish 15:552-558.
53. Sugama N, Park JG, Park YJ, Takeuchi Y, Kim SJ, Takemura A. (2008). Moonlight affects nocturnal Period2 transcript levels in the pineal gland of the reef fish Siganus guttatus. J. Pineal Res. 45: 133-141.
54. Sumova A, Jac M, Sladek M, Sauman I, Illnerova H. (2003). Clock gene daily profiles and their phase relationship in the Rat suprachiasmatic nucleus are affected by photoperiod. J. Biol. Rhythms 18: 134-144.
55. Sumova A, Bendova Z, Sladek M, Kovacikova Z, Illnerova H. (2004). Seasonal molecular timekeeping within the rat circadian clock. Physiol. Res. 53:S167-S176.
56. Tamai TK, Carr AJ, Whitmore D. (2005). Zebrafish circadian clocks: Cells that see light. Biochem. Soc. T. 33:962-966.
57. Tamura K, Nei M, Kumar S. (2004). Prospects for inferring very large phylogenies by using the neighbor-joining method. PNAS 101:11030-11035.
58. Tamura K, Dudley J, Nei M, Kumar S. (2007). MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0. Mol. Biol. Evol. 24:1596-1599.
59. Thompson JD, Plewniak F, Thierry JC, Poch O. (2000). DbClustal: Rapid and reliable global multiple alignments of protein sequences detected by database searches. Nucleic Acids Res. 28:2919-2926.
60. Tournier BB, Menet JS, Dardente H, Poirel VJ, Malan A, Masson-Pevet M, Pevet P, Vuillez P. (2003). Photoperiod differentially regulates clock genes' expression in the suprachiasmatic nucleus of Syrian hamster. Neuroscience 118:317-322.
61. Tournier BB, DardenteH, Simonneaux V, Vivien-Roels B, Pevet P,Masson-PevetM,VuillezP. (2007). Seasonal variations of clock gene expression in the suprachiasmatic nuclei and pars tuberalis of the European hamster (Cricetus cricetus). Eur. J. Neurosci. 25:1529-1536.
62. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. (2002). Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3(7)research0034.1-0034.11.
63. Wagner GC, Johnston JD, Clarke IJ, Lincoln GA, Hazlerigg DG. (2008). Redefining the limits of day length responsiveness in a seasonal mammal. Endocrinology 149:32-39.
64. Wang H. (2008). Comparative analysis of Period genes in the teleost fish genomes. J. Mol. Evol. 67: 29-40.
65. Whitmore D, Foulkes NS, Strahle U, Sassone-Corse P. (1998). Zebrafish Clock rhythmic expression reveals independent peripheral circadian oscillators. Nat. Neurosci. 1:701-707.
66. Whitmore D, Foulkes NS, Sassone-Corse P. (2000). Light acts directly on organs and cells in culture to set the vertebrate circadian clock. Nature 404:87-90.
67. Yasuo S, Watanabe M, Okabayashi N, Ebihara S, Yoshimura T. (2003). Circadian clock genes and photoperiodism: Comprehensive analysis of clock gene expression in the mediobasal hypothalamus, the suprachiasmatic nucleus, and the pineal gland of Japanese quail under various light schedules. Endocrinology 144:3742-3748.
68. Yoshimura T, Suzuki Y, Makino E, Suzuki T, Kuroiwa A, Matsuda Y, Namikawa T, Ebihara S. (2000). Molecular analysis of avian circadian clock genes. Mol. Brain Res. 78:207-215.
69. Zaunreiter M, Brandstatter R, Goldschmid A. (1998a). Evidence for an endogenous clock in the retina or rainbow trout, I: Retinomotor movements, dopamine and melatonin. Neuroreport 9: 1205-1209.
70. Zaunreiter M, Brandstatter R, Goldschmid A. (1998b). Evidence for an endogenous clock in the retina of rainbow trout, II: Circadian rhythmicity or serotonin metabolism. Neuroreport 9:1475-1479.
71. Ziv L, Gothilf Y. (2006). Period 2 expression pattern and its role in the development of the pineal cir-cadian clock in zebrafish. Chronobiol. Int. 23:101-112.