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Plant‐phenotypic changes induced by parasitoid ichnoviruses enhance the performance of both unparasitized and parasitized caterpillars

There is increasing awareness that interactions between plants and insects can be mediated by microbial symbionts. Nonetheless, evidence showing that symbionts associated with organisms beyond the second trophic level affect plant‐insect interactions are restricted to a few cases belonging to parasi...

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Autores principales: Cusumano, Antonino, Urbach, Serge, Legeai, Fabrice, Ravallec, Marc, Dicke, Marcel, Poelman, Erik H., Volkoff, Anne‐Nathalie
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8518489/
https://www.ncbi.nlm.nih.gov/pubmed/34245612
http://dx.doi.org/10.1111/mec.16072
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author Cusumano, Antonino
Urbach, Serge
Legeai, Fabrice
Ravallec, Marc
Dicke, Marcel
Poelman, Erik H.
Volkoff, Anne‐Nathalie
author_facet Cusumano, Antonino
Urbach, Serge
Legeai, Fabrice
Ravallec, Marc
Dicke, Marcel
Poelman, Erik H.
Volkoff, Anne‐Nathalie
author_sort Cusumano, Antonino
collection PubMed
description There is increasing awareness that interactions between plants and insects can be mediated by microbial symbionts. Nonetheless, evidence showing that symbionts associated with organisms beyond the second trophic level affect plant‐insect interactions are restricted to a few cases belonging to parasitoid‐associated bracoviruses. Insect parasitoids harbour a wide array of symbionts which, like bracoviruses, can be injected into their herbivorous hosts to manipulate their physiology and behaviour. Yet, the function of these symbionts in plant‐based trophic webs remains largely overlooked. Here, we provide the first evidence of a parasitoid‐associated symbiont belonging to the group of ichnoviruses which affects the strength of plant‐insect interactions. A comparative proteomic analysis shows that, upon parasitoid injection of calyx fluid containing ichnovirus particles, the composition of salivary glands of caterpillars changes both qualitatively (presence of two viral‐encoded proteins) and quantitatively (abundance of several caterpillar‐resident enzymes, including elicitors such as glucose oxidase). In turn, plant phenotypic changes triggered by the altered composition of caterpillar oral secretions affect the performance of herbivores. Ichnovirus manipulation of plant responses to herbivory leads to benefits for their parasitoid partners in terms of reduced developmental time within the parasitized caterpillar. Interestingly, plant‐mediated ichnovirus‐induced effects also enhance the performances of unparasitized herbivores which in natural conditions may feed alongside parasitized ones. We discuss these findings in the context of ecological costs imposed to the plant by the viral symbiont of the parasitoid. Our results provide intriguing novel findings about the role played by carnivore‐associated symbionts on plant‐insect‐parasitoid systems and underline the importance of placing mutualistic associations in an ecological perspective.
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spelling pubmed-85184892021-10-21 Plant‐phenotypic changes induced by parasitoid ichnoviruses enhance the performance of both unparasitized and parasitized caterpillars Cusumano, Antonino Urbach, Serge Legeai, Fabrice Ravallec, Marc Dicke, Marcel Poelman, Erik H. Volkoff, Anne‐Nathalie Mol Ecol Original Articles There is increasing awareness that interactions between plants and insects can be mediated by microbial symbionts. Nonetheless, evidence showing that symbionts associated with organisms beyond the second trophic level affect plant‐insect interactions are restricted to a few cases belonging to parasitoid‐associated bracoviruses. Insect parasitoids harbour a wide array of symbionts which, like bracoviruses, can be injected into their herbivorous hosts to manipulate their physiology and behaviour. Yet, the function of these symbionts in plant‐based trophic webs remains largely overlooked. Here, we provide the first evidence of a parasitoid‐associated symbiont belonging to the group of ichnoviruses which affects the strength of plant‐insect interactions. A comparative proteomic analysis shows that, upon parasitoid injection of calyx fluid containing ichnovirus particles, the composition of salivary glands of caterpillars changes both qualitatively (presence of two viral‐encoded proteins) and quantitatively (abundance of several caterpillar‐resident enzymes, including elicitors such as glucose oxidase). In turn, plant phenotypic changes triggered by the altered composition of caterpillar oral secretions affect the performance of herbivores. Ichnovirus manipulation of plant responses to herbivory leads to benefits for their parasitoid partners in terms of reduced developmental time within the parasitized caterpillar. Interestingly, plant‐mediated ichnovirus‐induced effects also enhance the performances of unparasitized herbivores which in natural conditions may feed alongside parasitized ones. We discuss these findings in the context of ecological costs imposed to the plant by the viral symbiont of the parasitoid. Our results provide intriguing novel findings about the role played by carnivore‐associated symbionts on plant‐insect‐parasitoid systems and underline the importance of placing mutualistic associations in an ecological perspective. John Wiley and Sons Inc. 2021-07-20 2021-09 /pmc/articles/PMC8518489/ /pubmed/34245612 http://dx.doi.org/10.1111/mec.16072 Text en © 2021 The Authors. Molecular Ecology published by John Wiley & Sons Ltd. https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Articles
Cusumano, Antonino
Urbach, Serge
Legeai, Fabrice
Ravallec, Marc
Dicke, Marcel
Poelman, Erik H.
Volkoff, Anne‐Nathalie
Plant‐phenotypic changes induced by parasitoid ichnoviruses enhance the performance of both unparasitized and parasitized caterpillars
title Plant‐phenotypic changes induced by parasitoid ichnoviruses enhance the performance of both unparasitized and parasitized caterpillars
title_full Plant‐phenotypic changes induced by parasitoid ichnoviruses enhance the performance of both unparasitized and parasitized caterpillars
title_fullStr Plant‐phenotypic changes induced by parasitoid ichnoviruses enhance the performance of both unparasitized and parasitized caterpillars
title_full_unstemmed Plant‐phenotypic changes induced by parasitoid ichnoviruses enhance the performance of both unparasitized and parasitized caterpillars
title_short Plant‐phenotypic changes induced by parasitoid ichnoviruses enhance the performance of both unparasitized and parasitized caterpillars
title_sort plant‐phenotypic changes induced by parasitoid ichnoviruses enhance the performance of both unparasitized and parasitized caterpillars
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8518489/
https://www.ncbi.nlm.nih.gov/pubmed/34245612
http://dx.doi.org/10.1111/mec.16072
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