The fungicide jinggangmycin stimulates fecundity of Nilaparvata lugens Stål via ILP/Foxo signaling

The brown planthopper (BPH), Nilaparvata lugens is a typical pesticide-induced resurgent rice pest. A previous study showed that a fungicide, jinggangmycin (JGM)-treated rice led to markedly increased sugar content and (Insulin-like Peptide 2) ILP2 in response to sugar-mediated TOR signaling and stimulated fecundity in BPH. However, the role of the other ILPs in response to types of carbohydrate compounds remained poorly understood. The present studies showed that JGM treatment led to strongly increased glucose content and slightly increased sucrose and trehalose contents in rice plants. The 5th instar nymphs feeding with JGM-treated rice or exogenous glucose-supplied artificial diets markedly upregulated transcription of ILP2 and ILP3 , triggered ILP/Foxo signaling transduction, and further induced ILP3 secretion in the female brain. Moreover, silencing of ILP3 in the nymphal stage through RNAi led to a significant decrease of ILP3 secretion in the brain compared with dsGFP-treated females and inhibited ILP/Foxo signaling transduction. Suppression of ILP3 decreased soluble protein content in the ovary and fat body, inhibited Vg expression and protein synthesis, and further blocked ovarian development in female adults. Finally, depletion of ILP3 significantly influenced reproductive parameters, including the number of laid eggs, oviposition period, number of offspring, hatching rate, and population growth indexes of BPH. The current study revealed the mechanism of diet glucose regulating BPH reproduction by inducing ILP3 expression, which complements the theory of pesticide-induced resurgence of rice pests and also provides an important gene target for green control of BPH.