Roles of circadian clock genes in insect photoperiodism

Goto, Shin G.

doi:10.1111/ens.12000

Cited by 115 publications

(82 citation statements)

References 92 publications

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“…Although the precise role of the circadian clock in regulating a photoperiodic response such as this is still a bit unclear, there is growing evidence that circadian clocks do in fact contribute to the decision to enter diapause (46,47). Knocking down expression of period or timeless, two of the canonical clock genes, prevents Cx.…”

Section: Cell Cycle and Developmentalmentioning

confidence: 99%

Identification of FOXO targets that generate diverse features of the diapause phenotype in the mosquito Culex pipiens

Sim

Kang

Kim

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

123

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Insulin and juvenile hormone signaling direct entry of the mosquito Culex pipiens into its overwintering adult diapause, and these two critical signaling pathways appear to do so by converging on the regulation of forkhead transcription factor (FOXO). Diapause is a complex phenotype, and FOXO emerges as a prime candidate for activating many of the diverse physiological pathways that generate the diapause phenotype. Here, we used ChIP sequencing to identify direct targets of FOXO. The nearest gene in a 10-kb region surrounding a predicted binding site was extracted for each binding site, resulting in a dataset containing genes potentially regulated by FOXO. By selecting candidate genes based on their functional relevance to diapause, we identified five gene categories of potential interest, including stress tolerance, metabolic pathways, lifespan extension, cell cycle and growth regulation, and circadian rhythms. Twelve targets were prioritized for further analysis, 10 of which were validated by ChIP-quantitative PCR and quantitative real-time PCR. These 10 genes activated by FOXO are highly up-regulated during diapause and are thus strong candidates for implementation of the diapause syndrome.diapause | Culex pipiens | forkhead transcription factor | insulin D iapause is a complex phenotype characterized not only by its hallmark trait of arrested development, but also by switches in behavior, suppressed metabolism, and enhanced responses to a range of environmental insults (1, 2). In the mosquito Culex pipiens, the diapause syndrome encompasses a cessation of reproductive maturation, a switch from blood feeding to sugar feeding, migration to protective overwintering sites, suppression of metabolism, and enhanced stress responses to combat low temperature, desiccation, and pathogens (3-7). These characteristics are indeed diverse, and it is not at all clear how the major hormonal signals that govern diapause are translated into the suite of features that comprise the diapause phenotype. A shutdown in the production of juvenile hormone (JH) is a nearly universal endocrine mechanism for insect diapauses that occur in the adult stage (8), and, more recently, the insulin signaling (IS) pathway has also been implicated in diapause regulation (9-12). The JH and IS pathways merge, as shown in Fig. 1. The IS pathway is linked to stimulation of the corpora allata to produce JH, and the IS and JH signaling pathways appear to collaboratively mediate expression of the forkhead transcription factor (FOXO). In the absence of IS and JH signaling, FOXO is activated, and this activation is critical for fat accumulation (13), cessation of ovarian development (9), and the elevated antioxidant responses (14) associated with diapause in Cx. pipiens. The genetic pathway involving IS and FOXO appears to also play a critical role in regulating dauer formation in the nematode Caenorhabditis elegans (15) and reproductive diapause in the fruit fly Drosophila melanogaster (16), thus suggesting a common mechanism regulating these diverse for...

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Section: Cell Cycle and Developmentalmentioning

confidence: 99%

Identification of FOXO targets that generate diverse features of the diapause phenotype in the mosquito Culex pipiens

Sim

Kang

Kim

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

123

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“…In this model, a circadian oscillator is entrained by lights off and programs a photo-inducible phase that, if illuminated, causes the insect to avert diapause. Such classic experiments have demonstrated the circadian basis of photoperiodic diapause initiation in several insect species (see reviews by Saunders, 2002;Saunders and Bertossa, 2011;Goto, 2013;Meuti and Denlinger, 2013), including a northern fruit fly, D. montana (Kauranen et al, 2013), and the mosquito Aedes atropalpus (Beach and Craig, 1977).…”

Section: Introductionmentioning

confidence: 99%

Functional circadian clock genes are essential for the overwintering diapause of the Northern house mosquito,Culex pipiens

Meuti

Stone

Ikeno

et al. 2015

Journal of Experimental Biology

135

101

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The short day lengths of late summer are used to program the overwintering adult diapause (dormancy) of the Northern house mosquito, Culex pipiens. Here, we investigated the role of clock genes in initiating this diapause and asked whether the circadian cycling of clock gene expression persists during diapause. We provide evidence that the major circadian clock genes continue to cycle throughout diapause and after diapause has been terminated. RNA interference (RNAi) was used to knock down the core circadian clock genes and to then assess the impact of the various clock genes on the ability of females to enter diapause. RNAi directed against negative circadian regulators (period, timeless and cryptochrome2) caused females that were reared under diapause-inducing, short day conditions to avert diapause. In contrast, knocking down the circadian-associated gene pigment dispersing factor caused females that were reared under diapause-averting, long day conditions to enter a diapause-like state. Our results implicate the circadian clock in the initiation of diapause in C. pipiens.

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“…To achieve the photoperiodic response, measuring the length of day (or night) is a crucial process. Although the mechanism of time measurement is still elusive in insects, it has been widely accepted that photoperiodic timing is based on an endogenous circadian clock (Saunders, 2002;Saunders, 2011;Goto, 2013). The circadian clock is a daily timing system used to generate a variety of circadian rhythms in behaviour, physiology and metabolism (Saunders, 2002).…”

Section: Introductionmentioning

confidence: 99%

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

Ikeno

Numata

Goto

et al. 2013

Journal of Experimental Biology

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The concept of insect photoperiodism based on a circadian clock has been supported by many studies demonstrating that the behavioural circadian rhythm and the photoperiodic response are driven by the same circadian clock genes. However, the neuronal mechanism of the circadian clock underlying photoperiodism is poorly understood. To examine whether circadian rhythm and photoperiodism share a neuronal mechanism, we focused on the neurons that express neuropeptide pigment-dispersing factor (PDF) in the bean bug, Riptortus pedestris. PDF has been identified as an important regulator of the insect circadian rhythm and is expressed in circadian clock neurons of various insect species. In R. pedestris, PDF immunoreactivity was detected in some clusters of cells and their fibres in the optic lobe and the protocerebrum. cDNA encoding a PDF precursor protein was highly conserved between R. pedestris and many other insects. Differences between day and night were not observed in the immunolabelling intensity in cell bodies of PDFimmunoreactive neurons and pdf mRNA expression levels in the head. Surgical removal of the region containing PDF-immunoreactive cell bodies at the medulla disrupted the photoperiodic regulation of diapause. However, gene suppression of pdf by RNA interference did not affect the photoperiodic response. These results suggest that the region containing PDF-immunoreactive somata is important for the photoperiodic response in R. pedestris, but pdf mRNA expression is probably not required for the response.

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Roles of circadian clock genes in insect photoperiodism

Cited by 115 publications

References 92 publications

Identification of FOXO targets that generate diverse features of the diapause phenotype in the mosquito Culex pipiens

Identification of FOXO targets that generate diverse features of the diapause phenotype in the mosquito Culex pipiens

Functional circadian clock genes are essential for the overwintering diapause of the Northern house mosquito,Culex pipiens

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

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