Plants recognize identity and intensity of herbivores to adaptively reconfigure metabolism

Plant specialized metabolites play central roles in defending against herbivorous insects. Yet, how the diversity of phytochemicals contributes to defense across different contexts of herbivory remains incompletely understood. Here, we analyse the leaf metabolome of Arabidopsis thaliana exposed to four herbivore species at three attack intensities to determine the herbivore-specific metabolic responses. We show species-specific and intensity-dependent metabolic patterns that exceed differences expected from feeding guild or host range, both among different metabolic pathways and within the glucosinolate biosynthetic pathway. Mutant analyses further reveal that metabolic specificity arises from distinct contributions of phytohormonal signaling and membrane-associated receptor complexes. Through 520 matched metabolome-bioassay pairs, we identify putative herbivore-resistant metabolites that are preferentially induced by the corresponding herbivore species; these responses are diminished in membrane coreceptor mutants. Together, our results highlight multiple dimensions of metabolic diversity and specificity in plant defenses and demonstrate their functional consequences with unprecedented coverage and resolution. Using untargeted metabolomics and herbivore bioassays, the authors demonstrate that plants exhibit species-specific metabolic defense against multiple herbivore species. This process depends on both phytohormone and membrane receptor functioning.