Abstract
Accurate control of innate behaviors associated with developmental transitions requires functional integration of hormonal and neural signals. Insect molting is regulated by a set of neuropeptides, which trigger periodic pulses in ecdysteroid hormone titers and coordinate shedding of the old cuticle during ecdysis. In the current study, we demonstrate that crustacean cardioactive peptide (CCAP), a structurally conserved neuropeptide described to induce the ecdysis motor program, also exhibits a previously unknown prothoracicostatic activity to regulate ecdysteroid production in the desert locust, Schistocerca gregaria. We identified the locust genes encoding the CCAP precursor and three G protein-coupled receptors that are activated by CCAP with EC50 values in the (sub)nanomolar range. Spatiotemporal expression profiles of the receptors revealed expression in the prothoracic glands, the endocrine organs where ecdysteroidogenesis occurs. RNAi-mediated knockdown of CCAP precursor or receptors resulted in significantly elevated transcript levels of several Halloween genes, which encode ecdysteroid biosynthesis enzymes, and in elevated ecdysteroid levels one day prior to ecdysis. Moreover, prothoracic gland explants exhibited decreased secretion of ecdysteroids in the presence of CCAP. Our results unequivocally identify CCAP as the first prothoracicostatic peptide discovered in a hemimetabolan species and reveal the existence of an intricate interplay between CCAP signaling and ecdysteroidogenesis.
Highlights
A central tenet in the molting process of arthropods is that this developmental process is initiated by a pulse of ecdysteroid hormones
We demonstrate that the crustacean cardioactive peptide (CCAP) signaling system controls the ecdysis motor program in the desert locust, Schistocerca gregaria, and plays a prothoracicostatic role
Since our results demonstrate that CCAP is pivotal for the initiation of the ecdysis motor program in this species, it is likely that CCAP release follows a similar pattern during ecdysis of S. gregaria
Summary
A central tenet in the molting process of arthropods is that this developmental process is initiated by a pulse of ecdysteroid hormones. The prothoracic gland (PG) functions as a central node that integrates both intrinsic and extrinsic signals to fine-tune ecdysteroidogenesis and maximize fitness outcomes and developmental progress. Prothoracicotropic hormone (PTTH) was the first discovered neurohormone to act as an ecdysteroidogenesis stimulating factor on the prothoracic gland. The release of PTTH controlling developmental timing of metamorphosis via triggered synthesis and secretion of ecdysteroids is a widely accepted paradigm [3]. Additional brain-originated peptides have since been found to aid in the proper regulation of the circulating ecdysteroid titer by exerting either stimulatory (“tropic”) or inhibitory (“static”) effects on the prothoracic gland of holometabolan species.
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