FoxO directly regulates the expression of odorant receptor genes to govern olfactory plasticity upon starvation in Bactrocera dorsalis

Under nutrient-poor conditions, animals must save energy by adjusting their behavior and physiology in order to survive. Although the impact of feeding state on olfactory sensory neuron activity has been well studied, the regulatory mechanisms underlying the transcriptional changes in odorant receptors (Ors) induced by feeding signals are seldom mentioned. Here, we showed that starvation could attenuate antennal responses of Bactrocera dorsalis toward multiple odorants, which could be reverted by sugar re-feeding, but not by a protein-rich diet. Using methyl eugenol (ME) as a paradigm, our study provided molecular evidence that Forkhead Box protein O (FoxO) can be expressed in antennal tissues to govern starvation-induced olfactory modifications by binding to the upstream regulatory regions of ME-responsive Ors and regulating their expressions. Since the consensus FoxO binding motif was also identified in other 17 Ors whose expression levels were also significantly altered upon FoxO knockdown and starvation, our data suggest that FoxO-dependent binding is likely a universal regulatory mechanism for Or genes during starvation and re-feeding cycles. Taken together, the FoxO-Ors axis elucidated in this study provides an improved understanding of how the insulin signaling pathway senses the feeding state and certain macronutrient composition to shape olfactory plasticity, allowing flies to dynamically alter chemosensory sensitivities toward different odors. Our study also highlights sugar as a satiety signal, which could increase ME -mediated trap efficiency in the field.

Automated summary

Animals under nutrient-poor conditions save energy by adjusting behavior and physiology. Starvation attenuates olfactory responses in Bactrocera dorsalis, which can be reversed by sugar re-feeding but not protein-rich diet. The study reveals the FoxO-Ors axis as a regulatory mechanism for odorant receptors during starvation and re-feeding cycles, providing an improved understanding of how the insulin signaling pathway shapes olfactory plasticity.