Anatomical characterization of PDF‐tri neurons and peptidergic neurons associated with eclosion behavior in Drosophila

Abstract

The peptidergic Pigment-dispersing factor (PDF)-Tri neurons are a group of non-clock neurons that appear transiently around the time of adult ecdysis (=eclosion) in the fruit fly Drosophila melanogaster. This specific developmental pattern points to a function of these neurons in eclosion or other processes that are active around pupal-adult transition. As a first step to understand the role of these neurons, we here characterize the anatomy of the PDF-Tri neurons. In addition, we describe a further set of peptidergic neurons that have been associated with eclosion behavior, eclosion hormone (EH), and crustacean cardioactive peptide (CCAP) neurons, to single cell level in the pharate adult brain. PDF-Tri neurons as well as CCAP neurons co-express a classical transmitter indicated by the occurrence of small clear vesicles in addition to dense-core vesicles containing the peptides. In the tritocerebrum, gnathal ganglion and the superior protocerebrum PDF-Tri neurites contain peptidergic varicosities and both pre- and postsynaptic sites, suggesting that the PDF-Tri neurons represent modulatory rather than pure interneurons that connect the subesophageal zone with the superior protocerebrum. The extensive overlap of PDF-Tri arborizations with neurites of CCAP- and EH-expressing neurons in distinct brain regions provides anatomical evidence for a possible function of the PDF-Tri neurons in eclosion behavior.

Recent advances in neuropeptide signaling in Drosophila, from genes to physiology and behavior

“…Detailed mapping of ETHR-A expression in Drosophila showed that the receptor is expressed in several larval peptidergic neurons including corazonin, myosuppressin, DH31 and NPF, suggesting that these neuropeptides could also be part of the Drosophila ecdysis circuit [517]. In addition, PDF neurons in the tritocerebrum, which appear around the time of ecdysis and have neurites overlapping with CCAP and eclosion hormone neurons, could also be involved [519].…”

Neuron secreted chemokine-like Orion is involved in the transformation of glial cells into phagocytes in different neuronal remodeling paradigms

“…In contrast, peptidergic vCrz + and PDF-Tri neurons exhibit complete neurite degeneration, and their cell bodies undergo apoptotic death and are eventually completely eliminated. This elimination occurs at different developmental stages: the vCrz + neuron apoptosis initiates in early pupae, whereas the PDF-Tri neuron apoptosis starts early after adult eclosion (Helfrich-Forster 1997; Choi et al 2006; Gatto and Broadie 2011; Selcho et al 2018). We show here that Orion is involved in the elimination of both types of peptidergic neurons, extending the role of orion to the elimination of apoptotic neurons.…”

Getting into rhythm: developmental emergence of circadian clocks and behaviors

“…However, the specific role of clock genes in regulating developmental time remains debated (125). The circadian clock does coordinate a final key developmental event in flies: the timing of eclosion through interactions between the PG and LN neurons (126,127) ensuring that flies eclose at dawn. Consistent with its role in regulating developmental transitions, the circadian clock also regulates the timing of cell proliferation across phylogeny (21).…”

“…However, the specific role of clock genes in regulating developmental time remains debated [125]. The circadian clock does coordinate a final key developmental event in flies: the timing of eclosion through interactions between the PG and LN neurons [126,127] ensuring that flies eclose at dawn.…”