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

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...

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Autores principales: Papantoniou, Dimitra, Chang, Dongik, Martínez-Medina, Ainhoa, van Dam, Nicole M., Weinhold, Alexander
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9634184/
https://www.ncbi.nlm.nih.gov/pubmed/36338467
http://dx.doi.org/10.3389/fphys.2022.1003746
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author Papantoniou, Dimitra
Chang, Dongik
Martínez-Medina, Ainhoa
van Dam, Nicole M.
Weinhold, Alexander
author_facet Papantoniou, Dimitra
Chang, Dongik
Martínez-Medina, Ainhoa
van Dam, Nicole M.
Weinhold, Alexander
author_sort Papantoniou, Dimitra
collection PubMed
description 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.
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spelling pubmed-96341842022-11-05 Root symbionts alter herbivore-induced indirect defenses of tomato plants by enhancing predator attraction Papantoniou, Dimitra Chang, Dongik Martínez-Medina, Ainhoa van Dam, Nicole M. Weinhold, Alexander Front Physiol Physiology 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. Frontiers Media S.A. 2022-10-21 /pmc/articles/PMC9634184/ /pubmed/36338467 http://dx.doi.org/10.3389/fphys.2022.1003746 Text en Copyright © 2022 Papantoniou, Chang, Martínez-Medina, van Dam and Weinhold. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Physiology
Papantoniou, Dimitra
Chang, Dongik
Martínez-Medina, Ainhoa
van Dam, Nicole M.
Weinhold, Alexander
Root symbionts alter herbivore-induced indirect defenses of tomato plants by enhancing predator attraction
title Root symbionts alter herbivore-induced indirect defenses of tomato plants by enhancing predator attraction
title_full Root symbionts alter herbivore-induced indirect defenses of tomato plants by enhancing predator attraction
title_fullStr Root symbionts alter herbivore-induced indirect defenses of tomato plants by enhancing predator attraction
title_full_unstemmed Root symbionts alter herbivore-induced indirect defenses of tomato plants by enhancing predator attraction
title_short Root symbionts alter herbivore-induced indirect defenses of tomato plants by enhancing predator attraction
title_sort root symbionts alter herbivore-induced indirect defenses of tomato plants by enhancing predator attraction
topic Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9634184/
https://www.ncbi.nlm.nih.gov/pubmed/36338467
http://dx.doi.org/10.3389/fphys.2022.1003746
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