Gustatory receptor 4 mediates oxidative stress signals to modulate adaptive feeding of Ostrinia furnacalis larvae under extreme temperatures.

BACKGROUND

Environmental temperature critically shapes feeding behavior in ectotherms, yet the molecular mechanisms that integrate temperature stress signals with adaptive feeding decisions remain poorly understood. In this study, we explored a neuro-antioxidant circuit that links temperature sensing to feeding modulation via reactive oxygen species (ROS) signaling.

RESULTS

To dissect the molecular basis of temperature-dependent feeding plasticity, we characterized larval phenotypes under different thermal regimes, and showed that the feeding-promoting neuropeptide F (NPF) and the salivary gland-enriched gustatory receptor 4 (Gr4) form a positive feedback loop for larval feeding and growth. NPF and Gr4 exhibited a gland-specific and temperature-bidirectional expression pattern. At 38 °C, their transcript levels were suppressed in the mandibular gland; at 18 °C, they were induced in the labial gland, relative to a temperature of 28 °C. Extreme temperatures alter ROS levels, which in turn regulate Gr4 expression. Furthermore, we identify catalase (CAT) as the dominant antioxidant enzyme in salivary glands, whose expression and activity are differentially modulated across glands and temperatures. Intriguingly, Gr4 and CAT, as a bidirectional regulatory relationship, together maintain redox homeostasis. Disruption of either component elevates ROS and impairs feeding and growth across temperatures.

CONCLUSION

This study reveals a previously unrecognized NPF-Gr4-CAT regulatory axis. This dual-regulatory axis, prioritizing energy intake in the cold and antioxidant defense under heat or host plant challenge, reveals how insects integrate environmental threats to balance survival and growth. These findings provide a mechanistic basis for understanding how adaptive behavioral plasticity evolves in response to complex ecological stressors. © 2026 Society of Chemical Industry.