Roles of the circadian clock and endocrine regulator in the photoperiodic response of the brown‐winged green bug <scp><i>Plautia stali</i></scp>

Tamai, Takaaki; Shiga, Sakiko; Goto, Shin G.

doi:10.1111/phen.12274

Cited by 41 publications

(6 citation statements)

References 76 publications

(107 reference statements)

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“…Primer sets for amplifying the cDNA containing the T7 promoter are shown in SI Appendix, Table S3. The primers for bla and per were created by referring to previous studies (11,60). The concentration of dsRNA was adjusted to 1 μg/μL, with pure water as the working solution.…”

Section: Methodsmentioning

confidence: 99%

Oviposition-promoting pars intercerebralis neurons showperiod-dependent photoperiodic changes in their firing activity in the bean bug

Hasebe

Shiga

2021

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

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Animals show photoperiodic responses in physiology and behavior to adapt to seasonal changes. Recent genetic analyses have demonstrated the significance of circadian clock genes in these responses. However, the importance of clock genes in photoperiodic responses at the cellular level and the physiological roles of the cellular responses are poorly understood. The bean bug Riptortus pedestris shows a clear photoperiodic response in its reproduction. In the bug, the pars intercerebralis (PI) is an important brain region for promoting oviposition. Here, we analyzed the role of the photoperiodic neuronal response and its relationship with clock genes, focusing on PI neurons. Large PI neurons exhibited photoperiodic firing changes, and high firing activities were primarily found under photoperiodic conditions suitable for oviposition. RNA interference-mediated knockdown of the clock gene period abolished the photoperiodic response in PI neurons, as well as the response in ovarian development. To clarify whether the photoperiodic response in the PI was dependent on ovarian development, we performed an ovariectomy experiment. Ovariectomy did not have significant effects on the firing activity of PI neurons. Finally, we identified the output molecules of the PI neurons and analyzed the relevance of the output signals in oviposition. PI neurons express multiple neuropeptides—insulin-like peptides and diuretic hormone 44—and RNA interference of these neuropeptides reduced oviposition. Our results suggest that oviposition-promoting peptidergic neurons in the PI exhibit a circadian clock-dependent photoperiodic firing response, which contributes to the photoperiodic promotion of oviposition.

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Section: Methodsmentioning

confidence: 99%

Oviposition-promoting pars intercerebralis neurons showperiod-dependent photoperiodic changes in their firing activity in the bean bug

Hasebe

Shiga

2021

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

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“…Advanced genetic analyses using insect models have suggested that circadian clock genes are involved in photoperiodism [8][9][10][11][12][13]33,[40][41][42]. However, neural signaling pathways that convey the photoperiodic information based on clock genes remain largely unknown.…”

Section: Discussionmentioning

confidence: 99%

“…In 1936, Bu ¨nning proposed a model in which endogenous circadian rhythms underlie the time measurement of photoperiod [1], and subsequent studies have examined the relationship between the circadian clock system and photoperiodic responses in both vertebrates and invertebrates [2][3][4][5][6][7]. Previous studies using insect models demonstrated that genetic suppression of expression of clock genes disrupted not only circadian rhythms but also photoperiodic responses of reproduction [8][9][10][11][12][13][14]. Thus, the molecular basis of the circadian clock is essential for photoperiodic responses.…”

Section: Introductionmentioning

confidence: 99%

Clock gene-dependent glutamate dynamics in the bean bug brain regulate photoperiodic reproduction

Hasebe

Shiga

2022

PLoS Biol

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Animals adequately modulate their physiological status and behavior according to the season. Many animals sense photoperiod for seasonal adaptation, and the circadian clock is suggested to play an essential role in photoperiodic time measurement. However, circadian clock-driven neural signals in the brain that convey photoperiodic information remain unclear. Here, we focused on brain extracellular dynamics of a classical neurotransmitter glutamate, which is widely used for brain neurotransmission, and analyzed its involvement in photoperiodic responses using the bean bug Riptortus pedestris that shows clear photoperiodism in reproduction. Extracellular glutamate levels in the whole brain were significantly higher under short-day conditions, which cause a reproductive diapause, than those under long-day conditions. The photoperiodic change in glutamate levels was clearly abolished by knockdown of the clock gene period. We also demonstrated that genetic modulation of glutamate dynamics by knockdown of glutamate-metabolizing enzyme genes, glutamate oxaloacetate transaminase (got) and glutamine synthetase (gs), attenuated photoperiodic responses in reproduction. Further, we investigated glutamate-mediated photoperiodic modulations at a cellular level, focusing on the pars intercerebralis (PI) neurons that photoperiodically change their neural activity and promote oviposition. Electrophysiological analyses showed that L-Glutamate acts as an inhibitory signal to PI neurons via glutamate-gated chloride channel (GluCl). Additionally, combination of electrophysiology and genetics revealed that knockdown of got, gs, and glucl disrupted cellular photoperiodic responses of the PI neurons, in addition to reproductive phenotypes. Our results reveal that the extracellular glutamate dynamics are photoperiodically regulated depending on the clock gene and play an essential role in the photoperiodic control of reproduction via inhibitory pathways.

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“…Moreover, it was proven that in Drosophila sNPF acts synergistically with PDF to inhibit reproductive arrest via activation of insulins producing cells in the brain (Nagy et al, 2019). Additionally, other neuropeptides, like diuretic hormone 44 (DH44) (Hasebe and Shiga, 2021) or Myoinhibitory peptides (MIPs) (Tamai et al, 2019) whose release is under circadian clock control, were shown to also participate in the regulation of imaginal diapause. Taken together, our data show that the photoperiodic regulation of the P. apterus diapause is regulated by CRY-m via the regulation of the PDF level in the Dp and others, currently unknown factors.…”

Section: Connection Of the Cry-m And Pdf To The Photoperiodic Regulat...mentioning

confidence: 99%

Pigment Dispersing Factor Is a Circadian Clock Output and Regulates Photoperiodic Response in the Linden Bug, Pyrrhocoris apterus

et al. 2022

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Daily and annually cycling conditions manifested on the Earth have forced organisms to develop time-measuring devices. Circadian clocks are responsible for adjusting physiology to the daily cycles in the environment, while the anticipation of seasonal changes is governed by the photoperiodic clock. Circadian clocks are cell-autonomous and depend on the transcriptional/translational feedback loops of the conserved clock genes. The synchronization among clock centers in the brain is achieved by the modulatory function of the clock-dependent neuropeptides. In insects, the most prominent clock neuropeptide is Pigment Dispersing Factor (PDF). Photoperiodic clock measures and computes the day and/or night length and adjusts physiology accordingly to the upcoming season. The exact mechanism of the photoperiodic clock and its direct signaling molecules are unknown but, in many insects, circadian clock genes are involved in the seasonal responses. While in Drosophila, PDF signaling participates both in the circadian clock output and in diapause regulation, the weak photoperiodic response curve of D. melanogaster is a major limitation in revealing the full role of PDF in the photoperiodic clock. Here we provide the first description of PDF in the linden bug, Pyrrhocoris apterus, an organism with a robust photoperiodic response. We characterize in detail the circadian and photoperiodic phenotype of several CRISPR/Cas9-generated pdf mutants, including three null mutants and two mutants with modified PDF. Our results show that PDF acts downstream of CRY and plays a key role as a circadian clock output. Surprisingly, in contrast to the diurnal activity of wild-type bugs, pdf null mutants show predominantly nocturnal activity, which is caused by the clock-independent direct response to the light/dark switch. Moreover, we show that together with CRY, PDF is involved in the photoperiod-dependent diapause induction, however, its lack does not disrupt the photoperiodic response completely, suggesting the presence of additional clock-regulated factors. Taken together our data provide new insight into the role of PDF in the insect’s circadian and photoperiodic systems.

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Roles of the circadian clock and endocrine regulator in the photoperiodic response of the brown‐winged green bug Plautia stali

Cited by 41 publications

References 76 publications

Oviposition-promoting pars intercerebralis neurons showperiod-dependent photoperiodic changes in their firing activity in the bean bug

Oviposition-promoting pars intercerebralis neurons showperiod-dependent photoperiodic changes in their firing activity in the bean bug

Clock gene-dependent glutamate dynamics in the bean bug brain regulate photoperiodic reproduction

Pigment Dispersing Factor Is a Circadian Clock Output and Regulates Photoperiodic Response in the Linden Bug, Pyrrhocoris apterus

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