RESUMEN
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 fungus Rhizophagus irregularis, the growth-promoting fungus Trichoderma harzianum, the generalist chewing herbivore Spodoptera exigua and the omnivorous predator Macrolophus pygmaeus. Using a Y-tube olfactometer we found that M. pygmaeus preferred plants with S. exigua herbivory, 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 of M. 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.
RESUMEN
Root mutualistic microbes can modulate the production of plant secondary metabolites affecting plant-herbivore interactions. Still, the main mechanisms underlying the impact of root mutualists on herbivore performance remain ambiguous. In particular, little is known about how changes in the plant metabolome induced by root mutualists affect the insect metabolome and post-larval development. By using bioassays with tomato plants (Solanum lycopersicum), we analyzed the impact of the arbuscular mycorrhizal fungus Rhizophagus irregularis and the growth-promoting fungus Trichoderma harzianum on the plant interaction with the specialist insect herbivore Manduca sexta. We found that root colonization by the mutualistic microbes impaired insect development, including metamorphosis. By using untargeted metabolomics, we found that root colonization by the mutualistic microbes altered the secondary metabolism of tomato shoots, leading to enhanced levels of steroidal glycoalkaloids. Untargeted metabolomics further revealed that root colonization by the mutualists affected the metabolome of the herbivore, leading to an enhanced accumulation of steroidal glycoalkaloids and altered patterns of fatty acid amides and carnitine-derived metabolites. Our results indicate that the changes in the shoot metabolome triggered by root mutualistic microbes can cascade up altering the metabolome of the insects feeding on the colonized plants, thus affecting the insect development.
RESUMEN
Beneficial microorganisms are known to promote plant growth and confer resistance to biotic and abiotic stressors. Soil-borne beneficial microbes in particular have shown potential in protecting plants against pathogens and herbivores via the elicitation of plant responses. In this study, we evaluated the role of Fusarium solani strain K (FsK) in altering plant responses to the two spotted spider mite Tetranychus urticae in tomato. We found evidence that FsK, a beneficial endophytic fungal strain isolated from the roots of tomato plants grown on suppressive compost, affects both direct and indirect tomato defenses against spider mites. Defense-related genes were differentially expressed on FsK-colonized plants after spider mite infestation compared to clean or spider mite-infested un-colonized plants. In accordance, spider mite performance was negatively affected on FsK-colonized plants and feeding damage was lower on these compared to control plants. Notably, FsK-colonization led to increased plant biomass to both spider mite-infested and un-infested plants. FsK was shown to enhance indirect tomato defense as FsK-colonized plants attracted more predators than un-colonized plants. In accordance, headspace volatile analysis revealed significant differences between the volatiles emitted by FsK-colonized plants in response to attack by spider mites. Our results highlight the role of endophytic fungi in shaping plant-mite interactions and may offer the opportunity for the development of a novel tool for spider mite control.