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

Abstract

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.

The circadian and photoperiodic clock of the pea aphid

“…Very recently, we found the reason for the apparent absence of PDF in aphids (Colizzi et al 2023 ). Indeed, we finally identified the aphid PDF coding gene and showed that it shows significant differences to the so far known insect PDFs appearing to lack the 7 C-terminal amino acids that are typical for it.…”

“…7 b). The PDF terminals in the pars lateralis overlap with the putative dendrites of the ILP4 neurons, and Pdf expression and the length of the terminals have been shown to be modulated by photoperiod (Colizzi et al 2023 ). On short days, Pdf expression increases, and PDF terminals lengthen, while on long days, Pdf expression is significantly lower and PDF terminals are shorter.…”

“…PDF signalling to neurosecretory cells of the pars intercerebralis or lateralis has already been demonstrated in other insects (Shiga and Numata 2009 ; Nagy et al 2019 ; Hidalgo et al 2023 ), making it likely that this also occurs in aphids. PDF appears to promote the sexual reproductive mode of aphids (Colizzi et al 2023 ) and the diapause mode of bugs in autumn (Kotwica-Rolinska et al 2022 ), while it appears important for reproduction of Drosophila in spring and summer (Hidalgo et al 2023 ).…”

A clock for all seasons

“…Nevertheless, the photoperiodic responses of aphids can also be attributed to a strongly dampened circadian clock. Recent studies have identified the molecular components and the location of the circadian clock in the brain of the pea aphid and demonstrated that it is intricately connected to the neurohormonal system controlling aphid reproduction (Colizzi et al 2023a ; Cuti et al 2021 ). In their study, Francesca S. Colizzi and colleagues provide an overview of the putative mechanisms of photoperiodic control in aphids, from the photoreceptors involved in this process to the circadian clock and the neuroendocrine system (Colizzi et al 2023 b).…”

One seasonal clock fits all?

“…Both involve the conversion of serotonin to melatonin as an initial step to break diapause, but the photoperiodic pathway uses the day length measure of the circadian clock, while the non-photic pathway is triggered by environmental factors such as temperature. Downstream, a number of species-dependent neuroendocrine pathways are involved, with pigment dispersing factor (PDF) as one common main factor conveying the photoperiodic information (Colizzi et al 2023a , b ; Hamanaka et al 2023 ).…”