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

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 me...

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Autores principales: Dimitra Papantoniou, Fredd Vergara, Alexander Weinhold, Teresa Quijano, Bekzod Khakimov, David I. Pattison, Søren Bak, Nicole M. van Dam, Ainhoa Martínez-Medina
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Acceso en línea:https://doaj.org/article/6329eb0ade3c47dca3ed429745a9c255
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spelling oai:doaj.org-article:6329eb0ade3c47dca3ed429745a9c2552021-11-25T18:20:31ZCascading Effects of Root Microbial Symbiosis on the Development and Metabolome of the Insect Herbivore <i>Manduca sexta</i> L.10.3390/metabo111107312218-1989https://doaj.org/article/6329eb0ade3c47dca3ed429745a9c2552021-10-01T00:00:00Zhttps://www.mdpi.com/2218-1989/11/11/731https://doaj.org/toc/2218-1989Root 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 (<i>Solanum lycopersicum</i>), we analyzed the impact of the arbuscular mycorrhizal fungus <i>Rhizophagus irregularis</i> and the growth-promoting fungus <i>Trichoderma harzianum</i> on the plant interaction with the specialist insect herbivore <i>Manduca sexta</i>. 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.Dimitra PapantoniouFredd VergaraAlexander WeinholdTeresa QuijanoBekzod KhakimovDavid I. PattisonSøren BakNicole M. van DamAinhoa Martínez-MedinaMDPI AGarticlearbuscular mycorrhizal fungi<i>Trichoderma</i><i>Manduca sexta</i><i>Solanum lycopersicum</i>LC–qToF–MSmetamorphosisMicrobiologyQR1-502ENMetabolites, Vol 11, Iss 731, p 731 (2021)
institution DOAJ
collection DOAJ
language EN
topic arbuscular mycorrhizal fungi
<i>Trichoderma</i>
<i>Manduca sexta</i>
<i>Solanum lycopersicum</i>
LC–qToF–MS
metamorphosis
Microbiology
QR1-502
spellingShingle arbuscular mycorrhizal fungi
<i>Trichoderma</i>
<i>Manduca sexta</i>
<i>Solanum lycopersicum</i>
LC–qToF–MS
metamorphosis
Microbiology
QR1-502
Dimitra Papantoniou
Fredd Vergara
Alexander Weinhold
Teresa Quijano
Bekzod Khakimov
David I. Pattison
Søren Bak
Nicole M. van Dam
Ainhoa Martínez-Medina
Cascading Effects of Root Microbial Symbiosis on the Development and Metabolome of the Insect Herbivore <i>Manduca sexta</i> L.
description 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 (<i>Solanum lycopersicum</i>), we analyzed the impact of the arbuscular mycorrhizal fungus <i>Rhizophagus irregularis</i> and the growth-promoting fungus <i>Trichoderma harzianum</i> on the plant interaction with the specialist insect herbivore <i>Manduca sexta</i>. 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.
format article
author Dimitra Papantoniou
Fredd Vergara
Alexander Weinhold
Teresa Quijano
Bekzod Khakimov
David I. Pattison
Søren Bak
Nicole M. van Dam
Ainhoa Martínez-Medina
author_facet Dimitra Papantoniou
Fredd Vergara
Alexander Weinhold
Teresa Quijano
Bekzod Khakimov
David I. Pattison
Søren Bak
Nicole M. van Dam
Ainhoa Martínez-Medina
author_sort Dimitra Papantoniou
title Cascading Effects of Root Microbial Symbiosis on the Development and Metabolome of the Insect Herbivore <i>Manduca sexta</i> L.
title_short Cascading Effects of Root Microbial Symbiosis on the Development and Metabolome of the Insect Herbivore <i>Manduca sexta</i> L.
title_full Cascading Effects of Root Microbial Symbiosis on the Development and Metabolome of the Insect Herbivore <i>Manduca sexta</i> L.
title_fullStr Cascading Effects of Root Microbial Symbiosis on the Development and Metabolome of the Insect Herbivore <i>Manduca sexta</i> L.
title_full_unstemmed Cascading Effects of Root Microbial Symbiosis on the Development and Metabolome of the Insect Herbivore <i>Manduca sexta</i> L.
title_sort cascading effects of root microbial symbiosis on the development and metabolome of the insect herbivore <i>manduca sexta</i> l.
publisher MDPI AG
publishDate 2021
url https://doaj.org/article/6329eb0ade3c47dca3ed429745a9c255
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