Circadian Clock Gene Period Contributes to Diapause via GABAeric-Diapause Hormone Pathway in Bombyx mori

Cui, Wen-Zhao; Qiu, Jian-Feng; Dai, Tai-Ming; Chen, Zhuo; Li, Jiang-Lan; Li, Kai; Wang, Yujun; Sima, Yang-Hu; Xu, Shiqiang

doi:10.3390/biology10090842

Cited by 19 publications

(34 citation statements)

References 80 publications

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“…Secretion of diapause hormone is promoted in oocytes destined for diapause by environmental perception of the mother pre-deposition. Significant work has dissected the regulation of B. mori diapause in relation to numerous aspects of physiology, including other endocrine molecules, but thus far diapause hormone appears to be exclusive to moths ( Ichikawa et al, 1997 ; Cui et al, 2021 ; Tsuchiya et al, 2021 ). While diapause hormone likely impacts lifespan, research in the biology of aging most clearly benefits from examination of mechanisms in diapause that are well-conserved.…”

Section: Future Directions and Conclusionmentioning

confidence: 99%

Endocrine Regulation of Lifespan in Insect Diapause

Hutfilz

2022

Front. Physiol.

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Diapause is a physiological adaptation to conditions that are unfavorable for growth or reproduction. During diapause, animals become long-lived, stress-resistant, developmentally static, and non-reproductive, in the case of diapausing adults. Diapause has been observed at all developmental stages in both vertebrates and invertebrates. In adults, diapause traits weaken into adaptations such as hibernation, estivation, dormancy, or torpor, which represent evolutionarily diverse versions of the traditional diapause traits. These traits are regulated through modifications of the endocrine program guiding development. In insects, this typically includes changes in molting hormones, as well as metabolic signals that limit growth while skewing the organism’s energetic demands toward conservation. While much work has been done to characterize these modifications, the interactions between hormones and their downstream consequences are incompletely understood. The current state of diapause endocrinology is reviewed here to highlight the relevance of diapause beyond its use as a model to study seasonality and development. Specifically, insect diapause is an emerging model to study mechanisms that determine lifespan. The induction of diapause represents a dramatic change in the normal progression of age. Hormones such as juvenile hormone, 20-hydroxyecdysone, and prothoracicotropic hormone are well-known to modulate this plasticity. The induction of diapause—and by extension, the cessation of normal aging—is coordinated by interactions between these pathways. However, research directly connecting diapause endocrinology to the biology of aging is lacking. This review explores connections between diapause and aging through the perspective of endocrine signaling. The current state of research in both fields suggests appreciable overlap that will greatly contribute to our understanding of diapause and lifespan determination.

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Section: Future Directions and Conclusionmentioning

confidence: 99%

Endocrine Regulation of Lifespan in Insect Diapause

Hutfilz

2022

Front. Physiol.

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“…However, the expression patterns of both negative elements differed between p50T and Kosetsu. This may be caused by differences in B. mori strains since previous studies showed differing per and tim expression rhythms among tissues, stages, and strains (Cui et al, 2021; Ikeda et al, 2019, 2021; Iwai et al, 2006; Tao et al, 2017). In the per Δ2 strain, tim expression was upregulated at all time points ( P < 0.001, two-way ANOVA; Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Both mutants lost eclosion and hatching rhythms, indicating that core clock genes are indispensable for circadian rhythms in B. mori . In addition, two groups independently described per’s involvement in photoperiodic diapause induction (Cui et al, 2021; Ikeda et al, 2021). Ikeda et al demonstrated that per knockout in the Kosetsu strain abolishes photoperiod sensitivity during the larval stage and inhibits diapause egg production.…”

Section: Introductionmentioning

confidence: 99%

“…Ikeda et al demonstrated that per knockout in the Kosetsu strain abolishes photoperiod sensitivity during the larval stage and inhibits diapause egg production. Cui et al (2021) showed knocking out per in the Dazao strain attenuates the effects of temperature and photoperiod on diapause induction during the embryonic stage thorough GABAergic signals. Since both studies only focused on a single negative element, it is difficult to conclude whether clock genes control photoperiodic diapause induction as a unit.…”

Section: Introductionmentioning

confidence: 99%

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Knockouts of positive and negative elements of the circadian clock disrupt photoperiodic diapause induction in the silkworm,Bombyx mori

Tobita

Kiuchi

2022

Preprint

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Diapause is one of the most important traits that have sustained insects to thrive. Insects can prospectively arrest their development and increase environmental stress-resistance by entering diapause. The photoperiod is the signal that indicates insects the proper timing to enter diapause. Circadian clock genes are shown to be involved in photoperiodic diapause induction in various insect species. The silkworm, Bombyx mori, enters diapause at the embryonic stage. In bivoltine strains, diapause determination is affected by embryonic temperature and photoperiodic conditions during embryonic and larval stages. Two independent studies showed that knocking out the core clock gene, period, perturb photoperiodic diapause induction. However, whether the circadian clock as whole or individual clock genes are responsible for the photoperiodic diapause induction remains unknown. In this study, using CRISPR/Cas9 we knocked out negative (period and timeless) and positive elements (Clock and cycle) in p50T, a bivoltine strain which exhibits photoperiodic diapause induction during both embryonic and larval stages. The temporal expression patterns of clock genes changed in each core clock gene knockout strain, suggesting disruption of normal feedback loops produced by circadian clock genes. Furthermore, photoperiodic diapause induction during both embryonic and larval stages was lost in all knockout strains. Our results indicate the involvement of circadian clock in photoperiodic diapause induction in B. mori.HighlightsWe established knockout Bombyx mori strains of four core clock genesThe temporal expression patterns of clock genes changed in knockout strainsPhotoperiodic diapause induction was not observed in any knockout strainsGraphical abstract

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“…The present study’s findings indicate that the clock genes per , tim , Clk , cyc , and cry2 are involved in temperature-dependent diapause induction. Involvement of clock genes in photoperiodic induction of diapause has been shown in various insects, including B. mori (e.g., Pavelka et al, 2003 ; Sakamoto et al, 2009 ; Ikeno et al, 2010 ; Merlin et al, 2013 ; Meuti et al, 2015 ; Cui et al, 2021 ; Ikeda et al, 2021 ). However, the role of clock genes in temperature-dependent diapause induction has not been shown.…”

Section: Discussionmentioning

confidence: 99%

Circadian Clock Genes Regulate Temperature-Dependent Diapause Induction in Silkworm Bombyx mori

Homma

Murata²,

Ikegami³

et al. 2022

Front. Physiol.

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The bivoltine strain of the domestic silkworm, Bombyx mori, exhibits a facultative diapause phenotype that is determined by maternal environmental conditions during embryonic and larval development. Although a recent study implicated a circadian clock gene period (per) in circadian rhythms and photoperiod-induced diapause, the roles of other core feedback loop genes, including timeless (tim), Clock (Clk), cycle (cyc), and cryptochrome2 (cry2), have to be clarified yet. Therefore, the aim of this study was to elucidate the roles of circadian clock genes in temperature-dependent diapause induction. To achieve this, per, tim, Clk, cyc, and cry2 knockout (KO) mutants were generated, and the percentages of diapause and non-diapause eggs were determined. The results show that per, tim, Clk, cyc, and cry2 regulated temperature-induced diapause by acting upstream of cerebral γ-aminobutyric acid (GABA)ergic and diapause hormone signaling pathways. Moreover, the temporal expression of the clock genes in wild-type (wt) silkworms was significantly different from that of thermosensitive transient receptor potential ankyrin 1 (TRPA1) KO mutants during embryonic development. Overall, the findings of this study provide target genes for regulating temperature-dependent diapause induction in silkworms.

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Circadian Clock Gene Period Contributes to Diapause via GABAeric-Diapause Hormone Pathway in Bombyx mori

Cited by 19 publications

References 80 publications

Endocrine Regulation of Lifespan in Insect Diapause

Endocrine Regulation of Lifespan in Insect Diapause

Knockouts of positive and negative elements of the circadian clock disrupt photoperiodic diapause induction in the silkworm,Bombyx mori

Circadian Clock Genes Regulate Temperature-Dependent Diapause Induction in Silkworm Bombyx mori

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