Seasonal cues act through the circadian clock and pigment-dispersing factor to control EYES ABSENT and downstream physiological changes

Hidalgo, Sergio; Anguiano, Maribel; Tabuloc, Christine A.; Chiu, Joanna C.

doi:10.1016/j.cub.2023.01.006

Cited by 27 publications

(38 citation statements)

References 86 publications

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“…Here, PDF from the s‐LN v terminals signals to the DILP neurons in the PI increasing their cAMP levels (Nagy et al., 2019). Subsequently, PKA is activated, which phosphorylates the transcription factor Eyes absent 3 (EYA3) and leads to its degradation (Hidalgo et al., 2023). EYA3 accumulates at high levels under winter conditions and promotes dormancy in D. melanogaster (Abrieux et al., 2020).…”

Section: Resultsmentioning

confidence: 99%

“…EYA3 accumulates at high levels under winter conditions and promotes dormancy in D. melanogaster (Abrieux et al., 2020). Since PDF levels in the s‐LN v terminals are higher under summer conditions than under winter conditions, PDF promotes EYA3 degradation in the summer, thereby keeping the flies in the reproductive state (Hidalgo et al., 2023). Future studies are needed to show whether a similar molecular mechanism works in D. littoralis .…”

Section: Resultsmentioning

confidence: 99%

“…The PDF‐ and sNPF‐expressing s‐LN v s, which are important for circadian rhythmicity and keeping D. melanogaster flies in the reproductive summer state (Grima et al., 2004; Helfrich‐Förster, 1998; Hidalgo et al., 2023; Nagy et al., 2019; Shafer & Taghert, 2009), appear to be less important in D. littoralis . These neurons in D. littoralis express only low amounts of PER and very little PDF and lack sNPF completely, which altogether suggests that their circadian clock is impaired.…”

Section: Discussionmentioning

confidence: 99%

“…PDF may even be released via the CC and could target peripheral tissues that express the PDF receptor (Krupp et al, 2013;Talsma et al, 2012). PDF might also affect DILP neurons in the PI and block EYA3 action and thereby keep the flies in the summer state as was shown by Hidalgo et al (2023) in D. melanogaster. Other neuropeptides expressed in the PL may then induce reproductive diapause as soon as night length exceeds a critical value in D. littoralis.…”

Section: 2mentioning

confidence: 99%

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Characterization of clock‐related proteins and neuropeptides in Drosophila littoralis and their putative role in diapause

Manoli

Zandawala

Yoshii

et al. 2023

J of Comparative Neurology

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Insects from high latitudes spend the winter in a state of overwintering diapause, which is characterized by arrested reproduction, reduced food intake and metabolism, and increased life span. The main trigger to enter diapause is the decreasing day length in summer–autumn. It is thus assumed that the circadian clock acts as an internal sensor for measuring photoperiod and orchestrates appropriate seasonal changes in physiology and metabolism through various neurohormones. However, little is known about the neuronal organization of the circadian clock network and the neurosecretory system that controls diapause in high‐latitude insects. We addressed this here by mapping the expression of clock proteins and neuropeptides/neurohormones in the high‐latitude fly Drosophila littoralis. We found that the principal organization of both systems is similar to that in Drosophila melanogaster, but with some striking differences in neuropeptide expression levels and patterns. The small ventrolateral clock neurons that express pigment‐dispersing factor (PDF) and short neuropeptide F (sNPF) and are most important for robust circadian rhythmicity in D. melanogaster virtually lack PDF and sNPF expression in D. littoralis. In contrast, dorsolateral clock neurons that express ion transport peptide in D. melanogaster additionally express allatostatin‐C and appear suited to transfer day‐length information to the neurosecretory system of D. littoralis. The lateral neurosecretory cells of D. littoralis contain more neuropeptides than D. melanogaster. Among them, the cells that coexpress corazonin, PDF, and diuretic hormone 44 appear most suited to control diapause. Our work sets the stage to investigate the roles of these diverse neuropeptides in regulating insect diapause.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: 2mentioning

confidence: 99%

See 2 more Smart Citations

Characterization of clock‐related proteins and neuropeptides in Drosophila littoralis and their putative role in diapause

Manoli

Zandawala

Yoshii

et al. 2023

J of Comparative Neurology

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“…In fruit flies and cockroaches, PDF is an essential output molecule of specific circadian clock neurons that control behavioural rhythmicity and serves additionally as a communication factor within the circadian clock network [9,11–13]. In addition, what is most relevant for the present report is that, in several insects, including fruit flies, PDF is implicated in seasonal timing [14–20] and, in one moth species, in annual rhythms [21]. In the blow fly Protophormia terraenovae , the ablation of the PDF-positive clock neurons renders the flies unable to discriminate between long days (LDs) and short days (SDs) [14] and thus unable to prepare in time for the coming winter.…”

Section: Introductionmentioning

confidence: 99%

Pigment-dispersing factor is present in circadian clock neurons of pea aphids and may mediate photoperiodic signalling to insulin-producing cells

et al. 2023

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The neuropeptide pigment-dispersing factor (PDF) plays a pivotal role in the circadian clock of most Ecdysozoa and is additionally involved in the timing of seasonal responses of several photoperiodic species. The pea aphid, Acyrthosiphon pisum, is a paradigmatic photoperiodic species with an annual life cycle tightly coupled to the seasonal changes in day length. Nevertheless, PDF could not be identified in A. pisum so far . In the present study, we identified a PDF-coding gene that has undergone significant changes in the otherwise highly conserved insect C-terminal amino acid sequence. A newly generated aphid-specific PDF antibody stained four neurons in each hemisphere of the aphid brain that co-express the clock protein Period and have projections to the pars lateralis that are highly plastic and change their appearance in a daily and seasonal manner, resembling those of the fruit fly PDF neurons. Most intriguingly, the PDF terminals overlap with dendrites of the insulin-like peptide (ILP) positive neurosecretory cells in the pars intercerebralis and with putative terminals of Cryptochrome (CRY) positive clock neurons. Since ILP has been previously shown to be crucial for seasonal adaptations and CRY might serve as a circadian photoreceptor vital for measuring day length, our results suggest that PDF plays a critical role in aphid seasonal timing.

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Drosophila ezoana uses morning and evening oscillators to adjust its rhythmic activity to different daylengths but only the morning oscillator to measure night length for photoperiodic responses

2023

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Animals living at high latitudes are exposed to prominent seasonal changes to which they need to adapt to survive. By applying Zeitgeber cycles of different periods and photoperiods we show here that high-latitude D. ezoana flies possess evening oscillators and highly damped morning oscillators that help them adapting their activity rhythms to long photoperiods. In addition, the damped morning oscillators are involved in timing diapause. The flies measure night length and use external coincidence for timing diapause. We discuss the clock protein TIMELESS (d-TIM) as the molecular correlate and the small ventrolateral clock neurons (s-LNvs) as the anatomical correlates of the components measuring night length.

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Seasonal cues act through the circadian clock and pigment-dispersing factor to control EYES ABSENT and downstream physiological changes

Cited by 27 publications

References 86 publications

Characterization of clock‐related proteins and neuropeptides in Drosophila littoralis and their putative role in diapause

Characterization of clock‐related proteins and neuropeptides in Drosophila littoralis and their putative role in diapause

Pigment-dispersing factor is present in circadian clock neurons of pea aphids and may mediate photoperiodic signalling to insulin-producing cells

Drosophila ezoana uses morning and evening oscillators to adjust its rhythmic activity to different daylengths but only the morning oscillator to measure night length for photoperiodic responses

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