Summary Phytohormone, particularly jasmonate (JA) and salicylate (SA) signaling, plays a central role in plant responses to herbivore and pathogen attack. Generally, SA mediates resistance responses against biotrophic pathogens and phloem‐feeding insects, while JA mediates responses against necrotrophic pathogens and chewing insects. The phytohormonal responses mediating rice resistance to a piercing‐sucking herbivore, the brown planthopper (BPH), remains unknown. Here, we combined transcriptome analysis, hormone measurements, genetic analysis and a field study to address this issue. Infestation by BPH adult females resulted in significant transcriptional reprograming. The upregulated genes were enriched in the JA signaling pathway. Consistently, the concentrations of JAs, but not SA, were dramatically increased in response to BPH attack. Two JA‐deficient lines (AOC and MYC2 knockout) and two SA‐deficient lines (nahG overexpression and NPR1 knockout) were constructed. BPH performed better on JA‐deficient lines than on wild‐type (WT) plants, but similarly on SA‐deficient and WT plants. During BPH attack, the accumulation of defensive secondary metabolites was attenuated in JA‐deficient lines compared with WT plants. Moreover, MYC2 mutants were more susceptible to planthoppers than WT plants in nature. This study reveals that JA signaling functions in rice defense against BPH.

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The phytohormone jasmonic acid (JA) plays a core role in plant defence against herbivores. When attacked by herbivores, JA and its bioactive derivatives are accumulated at the damage site, and subsequently perceived by the jasmonate co‐receptors COI1 and JAZ proteins. The (+)‐7‐iso‐jasmonoyl‐L‐isoleucine (JA‐Ile) is known to be the main active JA derivative controlling vascular plant responses to herbivores as well as other JA‐regulated processes. However, whether other endogenous JA‐amino acid conjugates (JA‐AAs) are involved in herbivore‐induced defence responses remain unknown. Here, we investigated the role of herbivore‐elicited JA‐AAs in the crop plant rice. The levels of five JA‐AAs were significantly increased under the armyworm, leaf folder and brown planthopper attack. Of the elicited JA derivatives, JA‐Ile, JA‐Val and JA‐Leu could serve as ligands to promote the interaction between rice COI1 and JAZs, inducing OsJAZ4 degradation in vivo. JA‐Val or JA‐Leu treatment increased the expression of JA‐ and defence‐related pathway genes but not JA‐Ile levels, suggesting that these JA‐AAs may directly function in JA signalling. Furthermore, the application of JA‐Val or JA‐Leu resulted in JA‐mediated plant growth inhibition, while enhancing plant resistance to herbivore attack. This study uncovers that JA‐Val and JA‐Leu also play a role in rice defence against herbivores.