Arabidopsis perceives caterpillar oral secretion to increase resistance by reactive oxygen species-enhanced glucosinolate hydrolysis.

In Arabidopsis, the outbreaks of reactive oxygen species (ROS) occur upon pathogen recognition by pattern- and effector-triggered immunity (PTI and ETI, respectively), which plays a significant role in disease resistance. Here, we found that Arabidopsis also experiences two outbreaks of ROS (oral secretion (OS)-induced ROS (ROSOS)) upon the perception of OS from cotton bollworm (Helicoverpa armigera) and other lepidopterans. Oral secretion-induced ROS burst requires the PTI machinery, including BRI1-ASSOCIATED RECEPTOR KINASE1 (BAK1) and BOTRYTIS-INDUCED KINASE1 (BIK1). Oral secretion-induced ROS are primarily produced by respiratory burst oxidase homologue D (RBOHD) in the apoplast, and the double mutant, rbohdf, exhibits reduced resistance to lepidopterans. Insect biting rather than wounding induces the gene expressions of plant defense-associated respiratory burst and toxin catabolic processes, facilitating the breakdown of leaf glucosinolates into bioactive intermediates, like sulforaphane, thereby impeding insect herbivory. Our investigation demonstrates that Arabidopsis perceives insect OS in a BAK1-BIK1-dependent manner and employs RBOHD to produce ROS in the apoplast, thereby enhancing its insect resistance by accelerating glucosinolate hydrolysis.