Eur. J. Entomol. 100 (2): 255-265, 2003 | DOI: 10.14411/eje.2003.041

TIMELESS: A link between fly's circadian and photoperiodic clocks?

Jaroslav PAVELKA1,2,*, Kimio SHIMADA1, Vladimir KOSTAL2
1 Institute of Low Temperature Science, Hokkaido University, Sapporo, Japan
2 Institute of Entomology, Academy of Sciences, Branišovská 31, CZ-370 05 České Budějovice, Czech Republic

Potential involvement of circadian clock genes in so far unknown mechanism of photoperiodic time measurement is an important question of insect life-cycle regulation science. Here we report about the cloning of full-length cDNA of the structural homologue of the Drosophila's timeless gene in Chymomyza costata. Its expression was compared in two strains: a wild-type strain, responding to short days by entering larval diapause and a npd-mutant strain, showing no photoperiodic response. The timeless mRNA transcripts were not detectable by Northern blot analysis in the fly heads of npd-mutants, while they were detectable and showed typical daily oscillations in the wild-type strain. After disrupting the normal process of timeless transcription in the wild-type strain by injection of timeless double-strandRNA into early embryos of wild-type (RNAi method: Kennerdell & Carthew 1998, 2000), a certain proportion of the individuals adopted a npd-mutant phenotype, showing no-diapause in response to short-daylength. Cloning of genomic DNA fragments revealed that npd-mutants carry a different allele, timelessnpd, with a 13-bp insertion in an intron positioned within the 5'-leader sequence. Genetic linkage analysis showed that the 13-bp insertion (a marker for timelessnpd) and the absence of response to short days (a marker for npd-phenotype) are strictly co-inherited in the F2 progeny of the reciprocal crosses between wild-type and npd-mutant flies. Such results indicated that the locus npd could code for the timeless gene in C. costata and its product might thus represent a molecular link between circadian and photoperiodic clock systems in this fly.

Keywords: Insect, Chymomyza costata, diapause, circadian clocks, photoperiodism, time measurement, period, timeless

Received: September 30, 2002; Revised: November 22, 2002; Accepted: December 18, 2002; Published: June 25, 2003  Show citation

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PAVELKA, J., SHIMADA, K., & KOSTAL, V. (2003). TIMELESS: A link between fly's circadian and photoperiodic clocks? EJE, 100(2), 255-265. doi: 10.14411/eje.2003.041
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    References

    1. Allada R., White N.E., So W.V., Hall J.C. & Rosbash M. 1998: A mutant Drosophila homologue of mammalian clock disrupts circadian rhythms and transcription of period and timeless. Cell 93: 791-804 Go to original source...
    2. Buenning E. 1936: Die endogene Tagesrhythmik als Grundlage der photoperiodischen Reaktion. Ber. Dt. Bot. Ges. 54: 590-607 Go to original source...
    3. Darlington T.K., Wager-Smith K., Ceriani M.F., Staknis D., Gekakis N., Steeves T.D.L., Weitz C.J., Takahashi J.S. & Kay S.A. 1998: Closing the circadian loop: CLOCK-induced transcription of its own inhibitors per and tim. Science 280: 1599-1603 Go to original source...
    4. Denlinger D.L. 2000: Molecular regulation of insect diapause. In: Storey K.B. & Storey J.M. (eds): Environmental Stressors and Gene Responses. Elsevier Science, Amsterdam, pp. 259-275 Go to original source...
    5. Denlinger D.L. 2002: Regulation of diapause. Annu. Rev. Entomol. 47: 93-122 Go to original source...
    6. Dunlap J.C. 1999: Molecular bases for circadian clocks. Cell 96: 271-290 Go to original source...
    7. Goldman B.D. 2001: Mammalian photoperiodic system: formal properties and neuroendocrine mechanisms of photoperiodic time measurement. J. Biol. Rhythms 16: 283-301 Go to original source...
    8. Goto S.G. & Denlinger D.L. 2002: Shrot-day and long-day expression patterns of genes involved in the flesh fly clock mechanism: period, timeless, cycle and cryptochrome. J. Insect Physiol. 48: 803-816 Go to original source...
    9. Harmer S.L., Panda S. & Kay S.A. 2001: Molecular bases of circadian rhythms. Annu. Rev. Cell Dev. Biol. 17: 215-253 Go to original source...
    10. Kennerdell J.R. & Carthew R.W. 1998: Use of dsRNA-mediated genetic interference to demonstrate that frizzled and frizzled2 act in the wingless pathway. Cell 95: 1017-1026 Go to original source...
    11. Kennerdell J.R. & Carthew R.W. 2000: Heritable gene silencing in Drosophila using double-stranded RNA. Nat. Biotechnol. 18: 896-898 Go to original source...
    12. Konopka R.J. & Benzer S. 1971: Clock mutants of Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 68: 2112-2116 Go to original source...
    13. Kostal V., Shimada K. & Hayakawa Y. 2000a: Induction and development of winter larval diapause in a drosophilid fly Chymomyza costata. J. Insect Physiol. 46: 417-428 Go to original source...
    14. Kostal V., Noguchi H., Shimada K. & Hayakawa Y. 2000b: Circadian component influences the photoperiodic induction of diapause in a drosophilid fly, Chymomyza costata. J. Insect Physiol. 46: 887-896 Go to original source...
    15. Kostal V. & Shimada K. 2001: Malfunction of circadian clock in the non-photoperiodic-diapause mutants of the drosophilid fly, Chymomyza costata. J. Insect Physiol. 47: 1269-1274 Go to original source...
    16. Lakovaara S. 1969: Malt as a culture medium for Drosophila species. Drosoph. Inf. Serv. 44: 128
    17. Lankinen P. 1986: Genetic correlation between circadian eclosion rhythm and photoperiodic diapause in Drosophila littoralis. J. Biol. Rhythms 2: 101-118 Go to original source...
    18. Lankinen P. & Riihimaa A.J. 1992: Weak circadian eclosion rhythmicity in Chymomyza costata (Diptera: Drosophilidae), and its independence of diapause type. J. Insect Physiol. 38: 803-811 Go to original source...
    19. Lankinen P. & Riihimaa A.J. 1997: Effects of temperature on weak circadian eclosion rhythmicity in Chymomyza costata (Diptera: Drosophilidae). J. Insect Physiol. 43: 251-260 Go to original source...
    20. Liu Y.G., Mitsukawa N., Oosumi T. & Whittier R.F. 1995: Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR. Plant J. 8: 457-463 Go to original source...
    21. Loudon A.S.I., Ihara N. & Menaker M. 1998: Effect of a circadian mutation on seasonality in Syrian hamsters (Mesocricetus auratus). Proc. R. Soc. London B265: 517-521 Go to original source...
    22. Majercak J., Sidote D., Hardin P.E. & Edery I. 1999: How a circadian clock adapts to seasonal decreases in temperature and day length. Neuron 24: 219-230 Go to original source...
    23. Matsumoto A., Tomioka K., Chiba Y. & Tanimura T. 1999: timrit lengthens circadian period in a temperature-dependent manner through suppression of PERIOD protein cycling and nuclear localization. Mol. Cell. Biol. 19: 4343-4354 Go to original source...
    24. Messager S., Ross A.W., Barrett P. & Morgan P.J. 1999: Decoding photoperiodic time through Per1 and ICER gene amplitude. Proc. Natl. Acad. Sci. USA 96: 9938-9943 Go to original source...
    25. Myers M.P., Wager-Smith K., Wesley C.S., Young M.W. & Sehgal A. 1995: Positional cloning and sequence analysis of the Drosophila clock gene timeless. Science 270: 805-808 Go to original source...
    26. Nuesslein-Hildesheim B., O'Brien J.A., Ebling F.J.P., Maywood E.S. & Hastings M.H. 2000: The circadian cycle of mPER clock gene products in the suprachiasmatic nucleus of the Siberian hamster encodes both daily and seasonal time. Eur. J. Neurosci. 12: 2856-2864 Go to original source...
    27. Ousley A., Zafarullah K., Chen Y., Emerson M., Hickman L. & Sehgal A. 1998: Conserved regions of the timeless (tim) clock gene in Drosophila analysed through phylogenetic and functional studies. Genetics 148: 815-825 Go to original source...
    28. Riihimaa A.J. 1996: Genetic variation in diapause, cold-hardiness and pupal eclosion rhythm in Chymomyza costata. Acta Univ. Ouluensis A274: 1-60
    29. Riihimaa A.J. & Kimura M.T. 1988: A mutant strain of Chymomyza costata (Diptera: Drosophilidae) insensitive to diapause-inducing action of photoperiod. Physiol. Entomol. 13: 441-445 Go to original source...
    30. Riihimaa A.J. & Kimura M.T. 1989: Genetics of the photoperiodic larval diapause in Chymomyza costata (Diptera; Drosophilidae). Hereditas 110: 193-200 Go to original source...
    31. Rothenfluh A., Abodeeley M., Price J.L. & Young M.W. 2000: Isolation and analysis of six timeless alleles that cause short- or long-period circadian rhythms in Drosophila. Genetics 156: 665-675 Go to original source...
    32. Roenneberg T. & Merrow M. 2001: Seasonality and photoperiodism in Fungi. J. Biol. Rhythms 16: 403-414 Go to original source...
    33. Rubin G.M. & Spradling A.C. 1982: Genetic transformation of Drosophila with transposable element vectors. Science 218: 348-353 Go to original source...
    34. Rutila J.E., Zeng H., Le M., Curtin K.D., Hall J.C. & Rosbash M. 1996: The timSL mutant of the Drosophila rhythm gene timeless manifests allele-specific interactions with period gene mutants. Neuron 17: 921-929 Go to original source...
    35. Rutila J.E., Suri V., Le M., So W.V., Rosbash M. & Hall J.C. 1998: CYCLE is a second bHLH-PAS clock protein essential for circadian rhythmicity and transcription of Drosophila period and timeless. Cell 93: 805-814 Go to original source...
    36. Samach A. & Coupland G. 2000: Time measurement and the control of flowering in plants. BioEssays 22: 38-47 Go to original source...
    37. Sambrook J., Fritsch E.F. & Maniatis T. 1989: Molecular Cloning, A Laboratory Manual. 2nd ed., Cold Spring Harbor Laboratory Press, New York. Saunders D.S. 2002: Insect Clocks. 3rd ed., Elsevier Science, Amsterdam, 576 pp
    38. Saunders D.S., Henrich V.C. & Gilbert L.I. 1989: Induction of diapause in Drosophila melanogaster: Photoperiodic regulation and the impact of arrhythmic clock mutations on time measurement. Proc. Natl. Acad. Sci. USA 86: 3748-3752 Go to original source...
    39. Sehgal A., Price J.L., Man B. & Young M.W. 1994: Loss of circadian behavioral rhythms and per RNA oscillations in the Drosophila mutant timeless. Science 263: 1603-1606 Go to original source...
    40. Shimada K. 1999: Genetic linkage analysis of photoperiodic clock genes in Chymomyza costata (Diptera: Drosophilidae). Entomol. Sci. 2: 575-578
    41. Sumova A., Sladek M., Jac M. & Illnerova H. 2002: The circadian rhythm of Per1 gene product in the rat suprachiasmatic nucleus and its modulation by seasonal changes in daylength. Brain Res. 947: 260-270 Go to original source...
    42. Suzuki L. & Johnson C.H. 2001: Algae know the time of day: circadian and photoperiodic programs. J. Phycol. 37: 933-942 Go to original source...
    43. Tauber E. & Kyriacou B.P. 2001: Insect photoperiodism and circadian clocks: models and mechanisms. J. Biol. Rhythms 16: 381-390 Go to original source...
    44. Veerman A. 2001: Photoperiodic time measurement in insects and mites: a critical evaluation of the oscillator-clock hypothesis. J. Insect Physiol. 47: 1097-1109 Go to original source...
    45. Wehr T.A. 2001: Photoperiodism in humans and other primates: evidence and implications. J. Biol. Rhythms 16: 348-364 Go to original source...
    46. Yoshida T. & Kimura M.T. 1995: The photoperiodic clock in Chymomyza costata. J. Insect Physiol. 41: 217-222 Go to original source...

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