Microbe-induced resistance involves priming of direct or indirect defenses according to the stage of herbivory

Abstract

Microbe-induced resistance (MIR) encompasses a broad range of plant responses that mediate both direct and indirect defenses against herbivores. However, previous studies have addressed MIR in relation to either direct or indirect defenses in isolation, overlooking potential conflicts or synergies that may arise between MIR-elicited defense strategies. We hypothesize that in multitrophic contexts, MIR-driven elicitation of direct and indirect defenses interacts, thereby shaping overall MIR phenotypes. To test this, we used two MIR-eliciting fungi: an arbuscular mycorrhizal and Trichoderma species; and the tri-trophic system including tomato plants, the herbivore Manduca sexta, and the parasitoid Cotesia congregata. We conducted a series of MIR bioassays, including performance and behavioral assays, and explored the main mechanisms underlying MIR phenotypes. We found that MIR involves a dynamic elicitation of direct and indirect defense-related traits that plastically adjust to herbivory time. Upon short-term herbivory, MIR primed jasmonate-regulated defenses, thereby enhancing the mortality of early-instar larvae. After a longer period of herbivory, MIR, especially triggered by Trichoderma, boosted green leaf volatile emissions, enhancing parasitoid attraction. Parasitoid performance was improved by MIR. Our study revealed that MIR enhances resistance by priming both direct and indirect defenses at different herbivory stages. This fosters complementary and synergistic responses, enhancing MIR phenotypes.