Insect capa neuropeptides impact desiccation and cold tolerance

Abstract

The success of insects is linked to their impressive tolerance to environmental stress, but little is known about how such responses are mediated by the neuroendocrine system. Here we show that the capability (capa) neuropeptide gene is a desiccation-and cold stressresponsive gene in diverse dipteran species. Using targeted in vivo gene silencing, physiological manipulations, stress-tolerance assays, and rationally designed neuropeptide analogs, we demonstrate that the Drosophila melanogaster capa neuropeptide gene and its encoded peptides alter desiccation and cold tolerance. Knockdown of the capa gene increases desiccation tolerance but lengthens chill coma recovery time, and injection of capa peptide analogs can reverse both phenotypes. Immunohistochemical staining suggests that capa accumulates in the capa-expressing Va neurons during desiccation and nonlethal cold stress but is not released until recovery from each stress. Our results also suggest that regulation of cellular ion and water homeostasis mediated by capa peptide signaling in the insect Malpighian (renal) tubules is a key physiological mechanism during recovery from desiccation and cold stress. This work augments our understanding of how stress tolerance is mediated by neuroendocrine signaling and illustrates the use of rationally designed peptide analogs as agents for disrupting protective stress tolerance.environmental stress | insects | neuropeptides | capa | desiccation and cold tolerance

Transcriptome analysis reveals nutrition‐ and age‐related patterns of gene expression in the fat body of pre‐overwintering bumble bee queens

“…These receptors were down‐regulated in queens given a more sucrose‐rich diet in our study. Capa and its receptor are expressed primarily in the abdominal ventral nerve cord and regulate diuresis (Predel & Wegener, ) and also influence desiccation and cold tolerance (Terhzaz et al, , ). The gene encoding this receptor was up‐regulated as a function of diet in our study.…”

CRISPR-induced null alleles show that Frost protects Drosophila melanogaster reproduction after cold exposure

“…Because Fst is encoded in an intron of Dh-44, a gene that may have a role in water balance and therefore cold tolerance (Terhzaz et al, 2015;Overgaard and Macmillan, 2017), we measured Dh-44 expression patterns in our mutant lines. Fst and Dh-44 expression are not correlated, and we show that the expression of Dh-44 is unaffected by Fst deletion or by insertion of w + in the Fst locus.…”

“…ionoregulatory system (Dow and Davies, 2006), and are therefore likely important in recovery from cold exposure (Terhzaz et al, 2015). However, in addition to their role in ion homeostasis, Malpighian tubules produce and export many proteins (Marshall, 1973;Dow and Davies, 2006).…”

“…Basal FST mRNA expression is most abundant in the Malpighian tubules (Chintapalli et al, 2007), although the site of expression induced by cold exposure has not been investigated. The position of Fst in an intron of the diuretic hormone gene Dh-44 potentially links Fst with the ion and water balance consequences of cold exposure in Drosophila (MacMillan et al, 2015b;Terhzaz et al, 2015), although FST and DH-44 mRNA expression do not appear to be co-regulated (Bing et al, 2012). The Frost (FST) protein sequence is rich in polar and charged amino acids, with the motif 'PEEST' occurring multiple times.…”

DINeR — A Database for Insect Neuropeptide Research

“…In insects, neuropeptides play an important role in coordinating complex homeostatic processes, such as development, metabolism, mating, water and ion homeostasis, reproduction, aggression and are also known to act as neuromodulators in circuits of the central nervous system (Caers et al, 2012;Nassel and Winther, 2010;Schoofs et al, 2017;Terhzaz et al, 2015). Since the discovery of the first insect neuropeptide, proctolin, in the American cockroach (Starratt and Brown, 1975), insect neuroendocrinology has progressed rapidly.…”