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

Abstract

• 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 (ROS^OS)) 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.