Eur. J. Entomol. 100 (2): 267-273, 2003 | 10.14411/eje.2003.042

Period gene expression in relation to seasonality and circadian rhythms in the linden bug, Pyrrhocoris apterus (Heteroptera)

Magdalena HODKOVÁ, Zdeňka SYROVÁ, David DOLEŽEL, Ivo ŠAUMAN
Institute of Entomology, Academy of Sciences, České Budějovice, CZ-370 05 Czech Republic; e-mail: magda@entu.cas.cz

Wild females of Pyrrhocoris apterus exhibit seasonal changes in neuroendocrine activity and, consequently, reproduction. Long days (18 h light/6 h dark) (LD) stimulate reproduction, whereas short days (12 h light/12 h dark) (SD) induce reproductive arrest (diapause). This study reveals how photoperiod influences the expression of the circadian clock gene, period (per) in the insect's head. There is only a weak diurnal rhythm in per mRNA expression under LD and SD. However, levels of per mRNA are consistently higher (up to 10-fold) under SD than under LD. The influence of photoperiod on per gene expression is linked to a developmental output (diapause vs. reproduction); mutant females, reproducing under both LD and SD, show low per mRNA levels under both photoperiodic conditions. Thus, the magnitude of per gene expression may be important to the translation of photoperiodic signals into a hormonal message. Levels of per mRNA are related to properties of locomotor activity rhythms. Low per mRNA levels (displayed by wild females in LD and mutant females in both LD and SD) are associated with long free-running periods (τ~26-27 h) and late peaks of activity (ψR,L~10-12 h), whereas high per mRNA levels coincide with short free-running periods (τ~24 h) and early peaks of activity (ψR,L~4-6 h). Overall, the data provide a background for a molecular approach to the long-standing question about the role of the circadian system in insect photoperiodism.

Keywords: circadian clock, per mRNA, photoperiod, diapause, locomotor activity rhythms

Received: December 10, 2002; Accepted: April 3, 2003; Published: June 25, 2003

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References

  1. Barrett K.P. & Page T.L. 1989: Effects of light on circadian pacemaker development. I. The freerunning period. J. Comp. Physiol. A 165: 41-49 Go to original source...
  2. Baylies M.K., Bargiello T.A., Jackson F.R. & Young M.W. 1987: Changes in abundance or structure of the per gene product can alter periodicity of the Drosophila clock. Nature 326: 390-392 Go to original source...
  3. Dunlap J.C. 1999: Molecular bases for circadian clock. Cell 96: 271-290 Go to original source...
  4. Goto S.G. & Denlinger D.L. 2002: Short-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...
  5. Hong S.-F. & Saunders D.S. 1998: Internal desynchronisation of the circadian locomotor rhythm in the blow fly, Calliphora vicina, as evidence for the involvement of a complex pacemaker. Biol. Rhythm Res. 29: 387-396 Go to original source...
  6. Hodek I. 1971: Termination of adult diapause in Pyrrhocoris apterus (Heteroptera: Pyrrhocoridae) in the field. Entomol. Exp. Appl. 14: 212-222 Go to original source...
  7. Hodkova M. 1976: Nervous inhibition of corpora allata by photoperiod in Pyrrhocoris apterus. Nature 263: 521-523 Go to original source...
  8. Hodkova M. 1994: Photoperiodic regulation of mating behaviour in the linden bug, Pyrrhocoris apterus is mediated by a brain inhibitory factor. Experientia 50: 742-744 Go to original source...
  9. Hodkova M. 1999: Regulation of diapause and reproduction in Pyrrhocoris apterus (L.) (Heteroptera) - Neuroendocrine outputs (mini-review). Entomol. Sci. 2: 563-566
  10. Hodkova M., Okuda T. & Wagner R.M. 2001: Regulation of corpora allata in females of Pyrrhocoris apterus (Heteroptera) (a mini-review). In vitro Cell. Dev. Biol.-Animal 37: 560-563 Go to original source...
  11. 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...
  12. Lankinen P. 1986: Geographical variation in circadian eclosion rhythm and photoperiodic adult diapause in Drosophila littoralis. J. Comp. Physiol. A 159: 123-142 Go to original source...
  13. 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...
  14. Messager S., Ross A.W., Barrett P. & Morgan P.J. 1999: Decoding photoperiodic time through Per 1 and ICER gene amplitude. Proc. Natl. Acad. Sci. USA 96: 9938-9943 Go to original source...
  15. Pavelka J., Shimada K. & Kostal V. 2003: Timeless: A link between fly's circadian and photoperiodic clocks? Eur. J. Entomol. 100 Go to original source...
  16. Pittendrigh C.S. 1981: Circadian systems: entrainment. In Aschoff J. (ed.): Biological Rhythms. Handbook of Behavioral Neurobiology 4, Plenum Press, New York, pp. 95-124
  17. Pittendrigh C.S., Elliot J. & Takamura T. 1984: The circadian component in photoperiodic induction. In: Porter R. & Collins G.M. (eds): Photoperiodic Regulation of Insect and Molluscan Hormones. Ciba Foundation Symposium No. 104. Pitman, London, pp. 26-47
  18. Refinetti R. 2000: Circadian Physiology. CRC Press, Boca Raton, 184 pp
  19. Reppert S.M. & Weaver D.R. 2000: Comparing clockworks: mouse versus fly. J. Biol. Rhythms 15: 357-364 Go to original source...
  20. Sauman I. & Hashimi H. 1999: Insect clocks: what are they telling us besides time? Entomol. Sci. 2: 589-596
  21. Saunders D.S. 1987a: Maternal influence on the incidence and duration of larval diapause in Calliphora vicina. Physiol. Entomol. 12: 331-338 Go to original source...
  22. Saunders D.S. 1987b: Insect photoperiodism: the linden bug, Pyrrhocoris apterus, a species that measures daylength rather than nightlength. Experientia 43: 935-937 Go to original source...
  23. Saunders D.S. 1990: The circadian basis of ovarian diapause regulation in Drosophila melanogaster: Is the period gene causally involved in photoperiodic time measurement? J. Biol. Rhythms 5: 315-331 Go to original source...
  24. Saunders D.S. 1998: Insect circadian rhythms and photoperiodism. Invertebr. Neurosci. 3: 155-164 Go to original source...
  25. Saunders D.S. 2001: Geographical strains and selection for the diapause trait in Calliphora vicina. In: Denlinger D.L., Giebultowicz J. & Saunders D.S. (eds): Insect Timing: Circadian Rhythmicity to Seasonality. Elsevier, Amsterdam, pp. 113-121
  26. Schotlant A. & Sehgal A. 2001: Molecular control of Drosophila circadian rhythms. In: Denlinger D.L., Giebultowicz J. & Saunders D.S. (eds): Insect Timing: Circadian Rhythmicity to Seasonality. Elsevier, Amsterdam, pp. 15-30
  27. Syrova Z., Hodkova M., Dolezel D. & Sauman I. 2001: Identification of putative circadian clock cells in a heteropteran insect, Pyrrhocoris apterus. Abstr. Cells III. Ceske Budejovice
  28. Tomioka K., Uwozumi K. & Matsumoto N. 1997: Light cycles given during development affect freerunning period of circadian locomotor rhythm of period mutants in Drosophila melanogaster. J. Insect Physiol. 43: 297-305 Go to original source...
  29. Vaz Nunes M., Koveos D.S. & Veerman A. 1990: Geographical variation in photoperiodic induction in the spider mite (Tetranychus urticae): A causal relation between critical nightlength and circadian period ? J. Biol. Rhythms. 5: 47-57 Go to original source...
  30. Vaz Nunes M. & Saunders D.S. 1999: Photoperiodic time measurement in insects: A review of clock models. J. Biol. Rhythms 14: 84-104 Go to original source...
  31. 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...
  32. Wattari Y. 2002: Comparison of the circadian eclosion rhythm between non-diapause and diapause pupae in the onion fly, Delia antiqua. J. Insect Physiol. 48: 83-89 Go to original source...
  33. Yin C.-M., Takeda M. & Wang Z.-S. 1987: A juvenile hormone analogue, methoprene as a circadian and developmental modulator in Diatraea grandiosella (Pyralidae): J. Insect Physiol. 33: 95-102 Go to original source...