Integrated Transcriptomic and Metabolomic Analyses Reveal Coordinated Defense Strategies Underlying Brown Planthopper Resistance in Wild Rice Species (Oryza nivara and Oryza rufipogon)

Rice (Oryza sativa L.) suffers severe yield losses from the brown planthopper (Nilaparvata lugens Stål; BPH), a phloem-feeding insect pest, and durable host resistance is widely regarded as the most economical strategy for its management. Wild relatives of rice harbor rich but largely untapped reservoirs of resistance. However, the molecular and metabolic mechanisms that underlie their contrasting resistance phenotypes remain poorly understood. Here, we integrated insect bioassays, transcriptome profiling, and widely targeted metabolomics to compare the responses of the resistant Oryza nivara and the susceptible Oryza rufipogon to BPH feeding. BPH showed significantly reduced weight gain, honeydew excretion, and survival on O. nivara, consistent with strong antibiosis-based resistance. Transcriptomic and metabolomic analyses revealed that O. nivara preferentially activated jasmonic acid signaling and phenylpropanoid-flavonoid biosynthesis and accumulated flavonoids and lignans/coumarins, whereas O. rufipogon mainly induced ribosomal and primary-metabolism genes and accumulated amino acids, nucleotides, and lipids. Integrated analyses uncovered a coordinated shikimate-phenylpropanoid-flavonoid metabolic axis in O. nivara, coupled with elevated jasmonic acid and salicylic acid signaling and suppressed auxin biosynthesis. Exogenous application of jasmonic or salicylic acid enhanced resistance in the susceptible O. rufipogon. Our results reveal a coordinated defense strategy in wild rice against BPH and highlight key metabolic and regulatory nodes that can be targeted to breed durable resistance into cultivated rice.