Molecular dissection of early defense signaling underlying volatile-mediated defense priming and herbivore resistance in rice

Herbivore-induced plant volatiles prime plant defenses and resistance. How volatiles are integrated into early defense signaling is not well understood. Furthermore, whether there is a causal relationship between volatile defense priming and herbivore resistance is unclear. Here, we investigated the impact of indole, a common herbivore-induced plant volatile and known defense priming cue, on early defense signaling and herbivore resistance in rice. We show that rice plants infested by Spodoptera frugiperda caterpillars release up to 25 ng*h-1. Exposure to equal doses of synthetic indole enhances rice resistance to S. frugiperda. Screening of early signaling components reveals that indole directly enhances the expression of the receptor like kinase OsLRR-RLK1. Furthermore, indole specifically primes the transcription, accumulation and activation of the mitogen-activated protein kinase OsMPK3 as well as the expression of the downstream WRKY transcription factor OsWRKY70 and several jasmonate biosynthesis genes, resulting in a higher accumulation of jasmonic acid (JA). Using transgenic plants defective in early signaling, we show that OsMPK3 is required, and that OsMPK6 and OsWRKY70 contribute to indole-mediated defense priming of JA-dependent herbivore resistance. We conclude that volatiles can increase herbivore resistance of plants by priming early defense signaling components.