A bitter taste receptor liganded by oxalic acid inhibits brown planthopper feeding by promoting CREB phosphorylation via the PI3K-AKT signaling pathway

Int J Biol Macromol. 2024 Dec 19:290:138999. doi: 10.1016/j.ijbiomac.2024.138999. Online ahead of print.

Abstract

Insect gustatory receptors play a critical role in modulating feeding behaviors by detecting external nutritional cues through complex biochemical pathways. Bitter taste receptors are essential for insects to identify and avoid toxins. However, the detailed molecular and cellular mechanisms by which these receptors influence insect feeding behavior remain poorly understood. Our previous research identified the bitter taste receptor NlGr23a in the brown planthopper (BPH), which specifically binds to oxalic acid and elicits a significant feeding rejection response. In this study, using an Sf9 cell line stably expressing NlGr23a, we demonstrated that oxalic acid exposure significantly enhances phosphorylation of cyclic adenosine monophosphate response element-binding protein (CREB), a protein associated with BPH food consumption. Further analysis revealed the involvement of phosphatidylinositol 3-kinase (PI3K)-protein kinase B (AKT) signaling pathway in facilitating CREB phosphorylation upon activation by oxalic acid-NlGr23a binding. These in vitro findings were corroborated by in vivo experiments examining the expression profiles of relevant proteins and protein kinases in BPHs fed an oxalic acid-supplemented diet. Our results elucidate the biochemical cascades triggered by oxalic acid-NlGr23a interaction, advancing our understanding of insect gustatory receptor-mediated feeding behavior modulation and potentially informing novel strategies for integrated pest management.

Keywords: CREB; Feeding; Gustatory receptor; Nilaparvata lugens; Oxalic acid; PI3K/AKT.