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 (<i>Oryza sativa</i>). Rice plants infested by fall armyworm (<i>Spodoptera frugiperda</i>) caterpillars release indole at a rate of up to 25 ng*h^-1 Exposure to equal doses of exogenous indole enhances rice resistance to <i>S. frugiperda</i> Screening of early signaling components revealed that indole pre-exposure directly enhances the expression of the leucine-rich repeat-receptor-like kinase <i>OsLRR-RLK1</i> 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 <i>OsWRKY70</i> as well as several jasmonate biosynthesis genes, resulting in higher jasmonic acid (JA) accumulation. Analysis of transgenic plants defective in early signaling showed that <i>OsMPK3</i> is required and that <i>OsMPK6</i> and <i>OsWRKY70</i> 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.