Small brown planthopper infestation enhances it reproduction and insecticide tolerance by manipulating glucose distribution and levels in rice

The evolutionary arms race between plants and insects involves not only direct defense and counter-defense but also sophisticated resource manipulation. However, how herbivorous insects exploit host nutritional signals for adaptation remains unclear. This study investigates how the small brown planthopper (SBPH, Laodelphax striatellus ) manipulates host plant carbohydrate allocation, and to elucidate the molecular mechanisms by which the acquired glucose enhances SBPH fecundity and insecticide tolerance. Using molecular, pharmacological, and biochemical approaches, we found that SBPH infestation induced systemic carbohydrate reallocation in rice, elevating whole-plant glucose levels by promoting aerial accumulation while depleting root reserves. Host-derived glucose enhanced SBPH fecundity by activating the target of rapamycin (TOR) pathway, upregulating juvenile hormone (JH) signaling, and increasing vitellogenin production. For imidacloprid tolerance, glucose boosted glutathione S-transferase (GST) activity via two synergistic mechanisms: by upregulating glutamate cysteine ligase (GCL) to increase glutathione synthesis, and transcriptionally via the glucose-TOR-JH axis to induce LsGSTe1 and LsGSTo1 expression. Our findings establish host-derived glucose as a central signaling molecule that SBPH exploits to simultaneously optimize reproduction and insecticide resistance. This reveals a multifaceted resource-manipulation strategy in insect pests and identifies the glucose-TOR-JH axis as critical molecular targets for developing nutrient-based pest control strategies.