Metabolic and Behavioral Impacts of Gustatory Receptor NlGr23 Silencing in the Brown Planthopper

The brown planthopper (BPH), Nilaparvata lugens, is the most destructive insect pest of rice. BPH infestations severely threaten rice yield worldwide. The gustatory receptor NlGr23 plays a critical role in mediating the repulsive reaction to oxalic acid of the BPH. We integrated transcriptomic and proteomic analyses to determine the metabolic and behavioral consequences of NlGr23 silencing. The RNAi-mediated knockdown of NlGr23 increased body weight and honeydew production, indicating enhanced feeding activity. The results of multiomics profiling revealed disrupted lipid homeostasis, identifying 187 differentially expressed genes and 150 differentially expressed proteins. These genes were enriched in pathways including glycerophospholipid metabolism, fatty acid biosynthesis, and AMPK signaling. The results of biochemical assays showed that NlGr23 silencing elevated triacylglycerol levels by 68.83%, and reduced glycerol and free fatty acid levels, suggesting impaired lipolysis. The NlGr23 loss-of-function mutation mechanistically activates the AMPK pathway, suppresses lipid breakdown, and promotes energy storage. This study established NlGr23 as a key regulator linking chemosensation to metabolic reprogramming, providing new insights into gustatory receptor-mediated energy homeostasis in the BPH.