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

Abstract 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 respond to host nutritional signals to modulate their fitness traits 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 (SBPH epsilon class GST) and LsGSTo1 (SBPH omega class GST) expression. Our findings establish host-derived glucose as a central signaling molecule that SBPH utilizes to modulate conserved pathways for simultaneous optimization of reproduction and insecticide resistance. This reveals a multifaceted nutrient-responsive mechanism in insect pests and identifies the glucose-TOR-JH axis as critical molecular targets for developing nutrient-based pest control strategies, such as disrupting insect nutrient-sensing pathways or modulating host carbohydrate metabolism. Highlights SBPH infestation elevates whole-plant glucose levels by promoting aerial accumulation while suppressing root abundance. SBPH-induced glucose in the rice aerial tissues boosts reproduction of SBPH via TOR-JH-Vg pathway. SBPH-induced glucose in the rice aerial tissues enhances imidacloprid tolerance of SBPH through GCL-GSH-GST and TOR-JH-GST axis. Competing Interest Statement The authors have declared no competing interest. Footnotes None of the figures in the manuscript have been revised and the revisions are primarily directed at improving the accuracy of wording and enhancing the rigor of the Discussion section, specifically as follows: 1, Conceptual framing and linguistic refinement：All overstated statements regarding evolutionary adaptation have been systematically revised throughout the text. Terminology such as exploit, co-opt, manipulation and adaptive strategy has been replaced with neutral and prudent expressions. The research conclusions have been rephrased to interpret the physiological phenomenon as a conserved nutrient-responsive physiological mechanism of insects against host nutritional signals, rather than a species-specific adaptive evolution driven by insecticide stress. We further clarified that the increased insecticide tolerance is merely an incidental byproduct arising from the activation of conserved metabolic and endocrine pathways, rather than an adaptative advantage acquired through active evolution. Ambiguous descriptions including "dual benefits" have also been deleted to improve the conceptual rigor of the manuscript. 2, Supplement of mechanistic conservation and generality: Revisions and supplementary content have been added to the Abstract, Introduction and Discussion sections. We cited relevant literature on conserved nutrient-sensing pathways in Drosophila, and further refined the research scope to hemipteran insects. We updated the research progress on carbohydrate metabolic reallocation in related planthopper species, highlighted the universality of plant carbohydrate allocation alteration in plant-insect interaction systems, and added explanations to illustrate the potential cross-species conservation of the identified nutrient signaling cascade. 3, Elucidation of research limitations and future prospects: A standalone subsection entitled Limitations and Future Research Directions has been newly added to the Discussion. We explicitly acknowledged that the present study only focuses on the small brown planthopper, and the generality of the underlying mechanism remains to be validated in closely related planthopper species. Meanwhile, we underscored that the upstream signals regulating glucose reallocation in rice remain uncharacterized, and it is necessary to expand insecticide tolerance assays to more types of agrochemicals, both of which are key priorities for future research. 4, Enrichment of practical application implications: An independent paragraph has been supplemented in the Discussion to elaborate the translational and application value of our findings. We proposed novel sustainable pest management strategies from three perspectives: rice variety breeding, development of small-molecule inhibitors targeting the TOR-JH signaling axis, and optimization of field fertilizer and water management. These mechanistic findings are further linked to practical eco friendly pest control and the mitigation of insecticide resistance in agricultural systems.