Root symbionts alter herbivore-induced indirect defenses of tomato plants by enhancing predator attraction

Abstract

Beneficial root microbes are among the most frequently used biocontrol agents in cropping systems, since they have been shown to promote plant growth and crop yield. Moreover, they are able to enhance protection against pathogens and insect herbivores by activating plant resistance mechanisms. Plant defense responses against herbivorous insects include the induction of metabolic pathways involved in the synthesis of defense-related metabolites. These metabolites include volatile organic compounds (VOCs), which attract natural enemies of the herbivores as a form of indirect resistance. Considering that beneficial root microbes may affect direct herbivore resistance, we hypothesized that also indirect resistance may be affected. We tested this hypothesis in a study system composed of tomato, the arbuscular mycorrhizal fungusRhizophagus irregularis, the growth-promoting fungusTrichoderma harzianum, the generalist chewing herbivoreSpodoptera exiguaand the omnivorous predatorMacrolophus pygmaeus. Using a Y-tube olfactometer we found thatM. pygmaeuspreferred plants withS. exiguaherbivory, but microbe-inoculated plants more than non-inoculated ones. We used a targeted GC-MS approach to assess the impact of beneficial microbes on the emission of volatiles 24 h after herbivory to explain the choice ofM. pygmaeus. We observed that the volatile composition of the herbivore-infested plants differed from that of the non-infested plants, which was driven by the higher emission of green leaf volatile compounds, methyl salicylate, and several monoterpenes and sesquiterpenes. Inoculation with microbes had only a marginal effect on the emission of some terpenoids in our experiment. Gene expression analysis showed that the marker genes involved in the jasmonic and salicylic acid pathways were differentially expressed in the microbe-inoculated plants after herbivory. Our results pinpoint the role of root symbionts in determining plant-microbe-insect interactions up to the third trophic level, and elucidates their potential to be used in plant protection.