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

Dimitra Papantoniou; Dongik Chang; Ainhoa Martínez-Medina; Nicole M van Dam; Alexander Weinhold

doi:10.3389/fphys.2022.1003746

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

Front Physiol. 2022 Oct 21:13:1003746. doi: 10.3389/fphys.2022.1003746. eCollection 2022.

Authors

Dimitra Papantoniou^{1

2}, Dongik Chang^{1

2}, Ainhoa Martínez-Medina³, Nicole M van Dam^{1

2}, Alexander Weinhold^{1

2}

Affiliations

¹ German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig, Germany.
² Institute of Biodiversity, Friedrich-Schiller Universität Jena, Jena, Germany.
³ Plant-Microorganism Interaction, Institute of Natural Resources and Agrobiology of Salamanca, Salamanca, Spain.

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 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.

Keywords: GC-MS; Macrolophus pygmaeus; Spodoptera exigua; Trichoderma; arbuscular mycorrhizal fungi; herbivore-induced plant volatiles; multi-trophic interactions.