The brown planthopper (Nilaparvata lugens Stål; BPH) is a specialist herbivore on rice (Oryza sativa) that ingests phloem sap from the plant through its stylet mouthparts. Electronic penetration graphs revealed that BPH insects spent more time wandering over plants carrying the resistance genes Bph14 and Bph15, but less time ingesting phloem than they did on susceptible plants. They also showed that their feeding was frequently interrupted. Tests with [ 14 C]sucrose showed that insects ingested much less phloem sap from the resistant than the susceptible plants. BPH feeding up-regulated callose synthase genes and induced callose deposition in the sieve tubes at the point where the stylet was inserted. The compact callose remained intact in the resistant plants, but genes encoding b-1,3-glucanases were activated, causing unplugging of the sieve tube occlusions in susceptible plants. Continuing ingestion led to a remarkable reduction in the susceptible plants' sucrose content and activation of the RAmy3D gene, leading to starch hydrolysis and ultimately carbohydrate deprivation in the plants. Our results demonstrate that BPH feeding induces the deposition of callose on sieve plates in rice and that this is an important defense mechanism that prevents insects from ingesting phloem sap. In response, however, the BPH can unplug sieve tube occlusions by activating b-1,3-glucanase genes in rice plants.

HighlightThis study identified the novel gene UAP1 in rice. UAP1 is involved in early leaf senescence and defence responses.

Brown planthopper (BPH) is a notorious pest of rice plants attacking leaf sheaths and seriously affecting global rice production. However, how rice plants respond against BPH remains to be fully understood. To understand systems metabolic responses of rice plants to BPH infestation, we analyzed BPH-induced metabolic changes in leaf sheaths of both BPH-susceptible and resistant rice varieties using NMR-based metabonomics and measured expression changes of 10 relevant genes using quantitative real-time PCR. Our results showed that rice metabonome was dominated by more than 30 metabolites including sugars, organic acids, amino acids, and choline metabolites. BPH infestation caused profound metabolic changes for both BPH-susceptible and resistant rice plants involving transamination, GABA shunt, TCA cycle, gluconeogenesis/glycolysis, pentose phosphate pathway, and secondary metabolisms. BPH infestation caused more drastic overall metabolic changes for BPH-susceptible variety and more marked up-regulations for key genes regulating GABA shunt and biosynthesis of secondary metabolites for BPH-resistant variety. Such observations indicated that activation of GABA shunt and shikimate-mediated secondary metabolisms was vital for rice plants to resist BPH infestation. These findings filled the gap of our understandings in the mechanistic aspects of BPH resistance for rice plants and demonstrated the combined metabonomic and qRT-PCR analysis as an effective approach for understanding plant-herbivore interactions.