Photoperiodic diapause under the control of circadian clock genes in an insect

Abstract

BackgroundMost organisms have evolved a circadian clock in order to anticipate daily environmental changes and many of these organisms are also capable of sophisticated measurement of daylength (photoperiodism) that is used to regulate seasonal events such as diapause, migration and polymorphism. It has been generally accepted that the same elements are involved in both circadian (daily) and seasonal (annual) rhythms because both rely upon daily light-dark cycles. However, as reasonable as this sounds, there remains no conclusive evidence of such a molecular machinery in insects. We have approached this issue by using RNA interference (RNAi) in Riptortus pedestris.ResultsThe cuticle deposition rhythm exhibited the major properties of circadian rhythms, indicating that the rhythm is regulated by a circadian clock. RNAi directed against the circadian clock genes of period and cycle, which are negative and positive regulators in the circadian clock, respectively, disrupted the cuticle deposition rhythm and distinct cuticle layers were produced by these RNAi. Simultaneously, period RNAi caused the insect to avert diapause under a diapause-inducing photoperiod whereas cycle RNAi induced diapause under a diapause-averting photoperiod. The expression patterns of juvenile hormone-regulated genes and the application of juvenile hormone analogue suggested that neither ovarian development itself nor a downstream cascade of juvenile hormone secretion, were disturbed by period and cycle RNAi.ConclusionsThis study revealed that the circadian clock genes are crucial not only for daily rhythms but also for photoperiodic diapause. RNAi directed against period and cycle had opposite effects not only in the circadian cuticle deposition rhythm but also in the photoperiodic diapause. These RNAi also had opposite effects on juvenile hormone-regulated gene expression. It is still possible that the circadian clock genes pleiotropically affect ovarian development but, based on these results, we suggest that the circadian clock operated by the circadian clock genes, period and cycle, governs seasonal timing as well as the daily rhythms.See Commentary: http://www.biomedcentral.com/1741-7007/8/115

The involvement of the brain region containing pigment-dispersing factor-immunoreactive neurons in the photoperiodic response of the bean bug Riptortus pedestris

“…Circadian clock genes and their protein products are expressed in a variety of tissues, but only a small number of neurons in the brain are responsible for the circadian clock regulating locomotor activity (Helfrich-Förster, 2003;Tomioka et al, 2012). While the involvement of the circadian clock genes in the photoperiodic response has been demonstrated in several insect species (Pavelka et al, 2003;Sakamoto et al, 2009;Ikeno et al, 2010;Ikeno et al, 2011b;Ikeno et al, 2011c;Ikeno et al, 2013;Bajgar et al, 2013a;Bajgar et al, 2013b), less is known about the neuronal mechanism of the circadian clock underlying photoperiodism (Shiga, 2012).…”

“…Riportus pedestris is one of the best-studied insects for involvement of the circadian clock in photoperiodism at the molecular level. RNAi targeting for the core circadian clock genes, period, mammalian-type cryptochrome, cycle and Clock, abolished both the circadian rhythm in cuticle deposition and the photoperiodic response, indicating that the same molecular elements are involved in the underlying clock mechanisms of circadian rhythm and photoperiodism (Ikeno et al, 2010;Ikeno et al, 2011a;Ikeno et al, 2011b;Ikeno et al, 2011c;Ikeno et al, 2013). Here, we hypothesized that photoperiodic and daily timing systems share not only molecular but also neuronal mechanisms of the circadian clock; therefore, the ablation of putative circadian clock neurons, PDF-ir neurons, would disrupt the photoperiodic response of R. pedestris.…”

Post-Embryonic Development of Circadian Oscillations Within and Outside the Optic Lobe in the Cricket,Gryllus bimaculatus

“…The treated nymphs showed a pattern of adult emergence under longday or short-day conditions that resembled the pattern neither of long-day nor short-day conditions, but had close resemblance to that in constant darkness , which clearly suggests that the circadian clock is a prerequisite for photoperiodic time measurement in this species. Importance of the circadian clock has been stressed by subsequent studies used different insect species (Ikeno et al, 2010;Ikeno et al, 2011). However, the cricket would be an excellent model for the molecular study of photoperiodic time measurement because, as mentioned above, it shows clear photoperiodic responses and clear behavioral rhythms as a gauge of the circadian clock, and its clock machinery as well as photoperiodic receptors has been studied.…”

Transcriptome profiling reveals mechanisms for the evolution of insect seasonality

“…Within our nominated gene lists, transcripts involved in insulin signaling and circadian rhythms are some of the most promising candidates for Pdd because both pathways are sensitive to light and temperature (Suttie et al, 1991;Chan et al, 1999;Shingleton et al, 2005;Taylor et al, 2005;Luckenbach et al, 2007;Sim and Denlinger, 2009), environmental factors that are known to stimulate diapause termination in corn borers (McLeod and Beck, 1963;Glover et al, 1992). These two pathways are also proposed regulators of dormancy or diapause in other species (Ikeno et al, 2010;Hahn and Denlinger, 2011). Of the 48 candidates, we focus on four with direct involvement in these pathways.…”

“…Laboratory studies also support a role for Per in diapause. RNA interference of Per in the bean bug (Riptortus pedestris) disrupts both circadian rhythms and photoperiodic response (Ikeno et al, 2010), and artificial selection for enhanced diapause in grey flesh fly (Sarcophaga bullata) is associated with a deletion at the Per locus that is 33 amino acids long (Han and Denlinger, 2009). …”