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Article

Cascading Effects of Root Microbial Symbiosis on the Development and Metabolome of the Insect Herbivore Manduca sexta L.

1
German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Puschstrasse 4, 04103 Leipzig, Germany
2
Institute of Biodiversity, Friedrich-Schiller Universität Jena, Dornburger Str. 159, 07743 Jena, Germany
3
Departamento de Ecología Tropical, Campus de Ciencias Biológicas y Agropecuarias, Universidad Autónoma de Yucatán, Apartado Postal 4-116, Itzimná 97000, Mexico
4
Department of Food Science, University of Copenhagen Rolighedsvej 26, 1958 Frederiksberg C, Denmark
5
Department of Plant and Environmental Sciences, Faculty of Science, University of Copenhagen, Thorvaldsensvej 40, 1871 Frederiksberg C, Denmark
6
Plant-Microorganism Interaction, Institute of Natural Resources and Agrobiology of Salamanca, 37008 Salamanca, Spain
*
Authors to whom correspondence should be addressed.
These authors contributed equally.
Academic Editor: David J. Beale
Metabolites 2021, 11(11), 731; https://doi.org/10.3390/metabo11110731
Received: 6 July 2021 / Revised: 6 October 2021 / Accepted: 20 October 2021 / Published: 25 October 2021
(This article belongs to the Special Issue Metabolomics in Chemical Ecology)
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. View Full-Text
Keywords: arbuscular mycorrhizal fungi; Trichoderma; Manduca sexta; Solanum lycopersicum; LC–qToF–MS; metamorphosis arbuscular mycorrhizal fungi; Trichoderma; Manduca sexta; Solanum lycopersicum; LC–qToF–MS; metamorphosis
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MDPI and ACS Style

Papantoniou, D.; Vergara, F.; Weinhold, A.; Quijano, T.; Khakimov, B.; Pattison, D.I.; Bak, S.; van Dam, N.M.; Martínez-Medina, A. Cascading Effects of Root Microbial Symbiosis on the Development and Metabolome of the Insect Herbivore Manduca sexta L. Metabolites 2021, 11, 731. https://doi.org/10.3390/metabo11110731

AMA Style

Papantoniou D, Vergara F, Weinhold A, Quijano T, Khakimov B, Pattison DI, Bak S, van Dam NM, Martínez-Medina A. Cascading Effects of Root Microbial Symbiosis on the Development and Metabolome of the Insect Herbivore Manduca sexta L. Metabolites. 2021; 11(11):731. https://doi.org/10.3390/metabo11110731

Chicago/Turabian Style

Papantoniou, Dimitra, Fredd Vergara, Alexander Weinhold, Teresa Quijano, Bekzod Khakimov, David I. Pattison, Søren Bak, Nicole M. van Dam, and Ainhoa Martínez-Medina. 2021. "Cascading Effects of Root Microbial Symbiosis on the Development and Metabolome of the Insect Herbivore Manduca sexta L." Metabolites 11, no. 11: 731. https://doi.org/10.3390/metabo11110731

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