Small Brown Planthopper Nymph Infestation Regulates Plant Defenses by Affecting Secondary Metabolite Biosynthesis in Rice

The small brown planthopper (SBPH, Laodelphax striatellus) is one of the most destructive insect pests in rice (Oryza sativa), which is the world's major grain crop. The dynamic changes in the rice transcriptome and metabolome in response to planthopper female adult feeding and oviposition have been reported. However, the effects of nymph feeding remain unclear. In this study, we found that pre-infestation with SBPH nymphs increased the susceptibility of rice plants to SBPH infestation. We used a combination of broadly targeted metabolomic and transcriptomic studies to investigate the rice metabolites altered by SBPH feeding. We observed that SBPH feeding induced significant changes in 92 metabolites, including 56 defense-related secondary metabolites (34 flavonoids, 17 alkaloids, and 5 phenolic acids). Notably, there were more downregulated metabolites than upregulated metabolites. Additionally, nymph feeding significantly increased the accumulation of seven phenolamines and three phenolic acids but decreased the levels of most flavonoids. In SBPH-infested groups, 29 differentially accumulated flavonoids were downregulated, and this effect was more pronounced with infestation time. The findings of this study indicate that SBPH nymph feeding suppresses flavonoid biosynthesis in rice, resulting in increased susceptibility to SBPH infestation.