Summary: The jasmonic acid (JA) pathway plays a central role in plant defense responses against insects. Some phloem‐feeding insects also induce the salicylic acid (SA) pathway, thereby suppressing the plant’s JA response. These phenomena have been well studied in dicotyledonous plants, but little is known about them in monocotyledons. We cloned a chloroplast‐localized type 2 13‐lipoxygenase gene of rice, OsHI‐LOX , whose transcripts were up‐regulated in response to feeding by the rice striped stem borer (SSB) Chilo suppressalis and the rice brown planthopper (BPH) Niaparvata lugens , as well as by mechanical wounding and treatment with JA. Antisense expression of OsHI‐LOX (as‐ lox ) reduced SSB‐ or BPH‐induced JA and trypsin protease inhibitor (TrypPI) levels, improved the larval performance of SBB as well as that of the rice leaf folder (LF) Cnaphalocrocis medinalis , and increased the damage caused by SSB and LF larvae. In contrast, BPH, a phloem‐feeding herbivore, showed a preference for settling and ovipositing on WT plants, on which they consumed more and survived better than on as‐ lox plants. The enhanced resistance of as‐ lox plants to BPH infestation correlated with higher levels of BPH‐induced H ₂ O ₂ and SA, as well as with increased hypersensitive response‐like cell death. These results imply that OsHI‐LOX is involved in herbivore‐induced JA biosynthesis, and plays contrasting roles in controlling rice resistance to chewing and phloem‐feeding herbivores. The observation that suppression of JA activity results in increased resistance to an insect indicates that revision of the generalized plant defense models in monocotyledons is required, and may help develop novel strategies to protect rice against insect pests.

Summary: Ethylene responsive factors (ERFs) are a large family of plant‐specific transcription factors that are involved in the regulation of plant development and stress responses. However, little to nothing is known about their role in herbivore‐induced defense. We discovered a nucleus‐localized ERF gene in rice (Oryza sativa), OsERF3, that was rapidly up‐regulated in response to feeding by the rice striped stem borer (SSB) Chilo suppressalis. Antisense and over‐expression of OsERF3 revealed that it positively affects transcript levels of two mitogen‐activated protein kinases (MAPKs) and two WRKY genes as well as concentrations of jasmonate (JA), salicylate (SA) and the activity of trypsin protease inhibitors (TrypPIs). OsERF3 was also found to mediate the resistance of rice to SSB. On the other hand, OsERF3 was slightly suppressed by the rice brown planthopper (BPH) Nilaparvata lugens (Stål) and increased susceptibility to this piercing sucking insect, possibly by suppressing H₂O₂ biosynthesis. We propose that OsERF3 affects early components of herbivore‐induced defense responses by suppressing MAPK repressors and modulating JA, SA, ethylene and H₂O₂ pathways as well as plant resistance. Our results also illustrate that OsERF3 acts as a central switch that gears the plant’s metabolism towards an appropriate response to chewing or piercing/sucking insects.

Plants generally respond to herbivore attack by increasing resistance and decreasing growth. This prioritization is achieved through the regulation of phytohormonal signaling networks. However, it remains unknown how this prioritization affects resistance against non-target herbivores. In this study, we identify WRKY70 as a specific herbivore-induced, mitogen-activated protein kinase-regulated rice transcription factor that physically interacts with W-box motifs and prioritizes defence over growth by positively regulating jasmonic acid (JA) and negatively regulating gibberellin (GA) biosynthesis upon attack by the chewing herbivore Chilo suppressalis. WRKY70-dependent JA biosynthesis is required for proteinase inhibitor activation and resistance against C. suppressalis. In contrast, WRKY70 induction increases plant susceptibility against the rice brown planthopper Nilaparvata lugens. Experiments with GA-deficient rice lines identify WRKY70-dependent GA signaling as the causal factor in N. lugens susceptibility. Our study shows that prioritizing defence over growth leads to a significant resistance trade-off with important implications for the evolution and agricultural exploitation of plant immunity.