TY - JOUR

T1 - Cascading effects of root microbial symbiosis on the development and metabolome of the insect herbivore Manduca sexta L.

AU - Papantoniou, Dimitra

AU - Vergara, Fredd

AU - Weinhold, Alexander

AU - Quijano, Teresa

AU - Khakimov, Bekzod

AU - Pattison, David I.

AU - Bak, Søren

AU - van Dam, Nicole M.

AU - Martínez-Medina, Ainhoa

N1 - Funding Information: Acknowledgments: The work of D.P. was supported by the European Union’s Horizon 2020 research and innovation program (Microbe-Induced Resistance, MiRA project), grant agreement no. 765290. D.P., F.V., A.W., N.M.v.D. and A.M.-M. gratefully acknowledge the support of iDiv funded by the German Research Foundation (DFG–FZT 118, 202548816). A.M.-M. acknowledges funding from the program for attracting talent to Salamanca from the Fundación Salamanca Ciudad de Cultura y Saberes and Ayuntamiento de Salamanca; the program to support junior researchers to obtain third-party funding from Friedrich-Schiller-Universität Jena (DRM/2015-02); Junta de Castilla y León and European Union (ERDF “Europe drives our growth”; CLU-2019-05—IRNASA/CSIC Unit of Excellence); and the research network RED2018-102407-T from the Spanish Ministry of Science and Innovation and Feder funds. Publisher Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland.

PY - 2021

Y1 - 2021

N2 - 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.

AB - 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.

KW - Arbuscular mycorrhizal fungi

KW - LC–qToF–MS

KW - Manduca sexta

KW - Metamorphosis

KW - Solanum lycopersicum

KW - Trichoderma

U2 - 10.3390/metabo11110731

DO - 10.3390/metabo11110731

M3 - Review

C2 - 34822389

AN - SCOPUS:85118228500

VL - 11

JO - Metabolites

JF - Metabolites

SN - 2218-1989

IS - 11

M1 - 731

ER -