Insect capa neuropeptides impact desiccation and cold tolerance.
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 stress-responsive 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.
Institute of Molecular, Cell and Systems Biology, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, G12 8QQ, Scotland, United Kingdom; selim.terhzaz@glasgow.ac.uk denlinger.1@osu.edu shireen.davies@glasgow.ac.uk.
Selim
S
Terhzaz
Departments of Entomology and Evolution, Ecology, and Organismal Biology, The Ohio State University, Columbus, OH 43210;
Nicholas M
NM
Teets
Institute of Molecular, Cell and Systems Biology, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, G12 8QQ, Scotland, United Kingdom;
Pablo
P
Cabrero
Institute of Molecular, Cell and Systems Biology, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, G12 8QQ, Scotland, United Kingdom;
Louise
L
Henderson
Centre for Biological Diversity, School of Biology, University of St. Andrews, St. Andrews, Fife KY16 9TS, Scotland, United Kingdom; and.
Michael G
MG
Ritchie
Insect Control and Cotton Disease Research Unit, Southern Plains Agricultural Research Center, US Department of Agriculture, College Station, TX 77845.
Ronald J
RJ
Nachman
Institute of Molecular, Cell and Systems Biology, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, G12 8QQ, Scotland, United Kingdom;
Julian A T
JA
Dow
Departments of Entomology and Evolution, Ecology, and Organismal Biology, The Ohio State University, Columbus, OH 43210; selim.terhzaz@glasgow.ac.uk denlinger.1@osu.edu shireen.davies@glasgow.ac.uk.
David L
DL
Denlinger
Institute of Molecular, Cell and Systems Biology, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, G12 8QQ, Scotland, United Kingdom; selim.terhzaz@glasgow.ac.uk denlinger.1@osu.edu shireen.davies@glasgow.ac.uk.
Shireen-A
SA
Davies
D000818:Animals; D003080:Cold Temperature; D058639:Cold-Shock Response; D003681:Dehydration / Q000235:genetics / Q000378:metabolism* / Q000473:pathology; D029721:Drosophila Proteins / Q000096:biosynthesis* / Q000235:genetics; D004331:Drosophila melanogaster; D005786:Gene Expression Regulation; D008317:Malpighian Tubules / Q000378:metabolism* / Q000473:pathology; D009474:Neurons / Q000378:metabolism* / Q000473:pathology; D009479:Neuropeptides / Q000096:biosynthesis* / Q000235:genetics; D015398:Signal Transduction / Q000235:genetics
D029721:Drosophila Proteins; D009479:Neuropeptides; C455043:capa protein, Drosophila
capa; desiccation and cold tolerance; environmental stress; insects; neuropeptides