Molecular Dissection of Early Defense Signaling Underlying Volatile-Mediated Defense Regulation and Herbivore Resistance in Rice

Herbivore-induced plant volatiles prime plant defenses and resistance, but how they are integrated into early defense signaling and whether a causal relationship exists between volatile defense priming and herbivore resistance is unclear. Here, we investigated the impact of indole, a common herbivore-induced plant volatile and modulator of many physiological processes in plants, bacteria, and animals, on early defense signaling and herbivore resistance in rice (Otyza sativa). Rice plants infested by fall armyworm (Spodoptera frugiperda) caterpillars release indole at a rate of up to 25 ng*h(-1). Exposure to equal doses of exogenous indole enhances rice resistance to S. frugiperda. Screening of early signaling components revealed that indole pre-exposure directly enhances the expression of the leucine-rich repeat-receptor-like kinase OsLRR-RLK1. Pre-exposure to indole followed by simulated herbivory increases (i.e. primes) the transcription, accumulation, and activation of the mitogen-activated protein kinase OsMPK3 and the expression of the downstream WRKY transcription factor gene OsWRKY70 as well as several jasmonate biosynthesis genes, resulting in higher jasmonic acid (JA) accumulation. Analysis of transgenic plants defective in early signaling showed that OsMPK3 is required and that OsMPK6 and OsWRKY70 contribute to indole-mediated defense priming of JA-dependent herbivore resistance. Therefore, herbivore-induced plant volatiles increase plant resistance to herbivores by positively regulating early defense signaling components.