Rice, a vital crop, faces significant threats from the brown planthopper (BPH), which impacts plant growth and yield. Pyramiding the BPH resistance genes BPH14 and BPH15 provides rice crops with reliable and lasting protection against BPH. Nonetheless, current research lacks clarity on the molecular processes responsible for BPH14/BPH15-mediated resistance to BPH. In this study, utilizing high-throughput metabolomics and integrating transcriptomic data, we investigated the metabolic adaptations of the BPH14/BPH15 pyramiding line (B1415) and its recurrent parent (RP) during early and late infestation stages. The analysis identified 1007 metabolites, mainly consisting of lipids and lipid-like molecules, together with phenylpropanoid and polyketide classes. Differentially accumulated metabolites (DAMs) displayed different patterns in B1415 and RP, particularly in flavonoid and phenylpropanoid biosynthesis pathways, which were more pronounced in the resistant B1415. Furthermore, ferulic acid (FA) was found to negatively regulate BPH resistance. These findings elucidate critical metabolic pathways involved in rice defense mechanisms and underscore the potential of B1415’s enhanced metabolic responses in conferring durable resistance against BPH.

The brown planthopper (Nilaparvata lugens Stål, BPH) is a destructive pest of rice. Non-coding RNAs (ncRNAs) regulate the defense mechanisms in rice and the adaptive strategies of BPHs. In rice, ncRNAs modulate key resistance pathways such as jasmonic acid biosynthesis, flavonoid production, and phenylpropanoid metabolism, which increases BPH resistance. In BPHs, ncRNAs regulate processes such as reproduction, metabolism, and wing polyphenism, which facilitate adaptation and virulence. Cross-kingdom interactions between rice and BPHs reveal the dynamic molecular interplay that underpins this pest–host relationship. These new insights into ncRNA functions will help improve innovative pest management strategies and equip rice varieties with enhanced BPH resistance.