Heat-sensing receptor pathway promotes thermal tolerance via chitin remodeling in an invasive lepidopteran pest

The ability of insects to adapt to variable environmental stresses, including temperature fluctuation, is critical for survival.The fall webworm, Hyphantria cunea, is a rapidly spreading invasive pest with strong adaptability to various temperature conditions.However, little is known about the mechanism underlying its tolerance to heat stress.Here we identified two H. cunea neuropeptide genes, capability-1 and 2 (HcCAPA-1 and HcCAPA-2), which appear to be heat stress-responsive genes.We showed that tolerance to heat in H. cunea is dramatically impacted by CAPA peptide signaling.Knock-down of the CAPA receptor (CAPA-R) gene decreased heat tolerance and prolonged hot coma recovery time, but this effect was reversed after injection of CAPA peptides.Western blot and ELISA assay suggested that CAPA accumulates in brain cells during non-lethal heat stress and is released during recovery time from heat.We further demonstrated that an ionotropic receptor (IR), HcIR68a, is highly expressed in the legs of H. cunea larvae and regulates the expression of CAPAs in the brain.mRNA levels of CAPAs in the brain reduced after knocking down HcIR68a.Finally, we found chitin biosynthesis enzymes which act as downstream signals of HcCAPA-R in regulating heat stress.Our study revealed the role and mechanism of HcIR68a and CAPA/CAPA-R signaling in heat shock response and adaptation to heat acclimation, thus providing more promising molecular targets for the development of new pest-specific control products.