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Under fire-simultaneous volatilome and transcriptome analysis unravels fine-scale responses of tansy chemotypes to dual herbivore attack

BACKGROUND: Tansy plants (Tanacetum vulgare L.) are known for their high intraspecific chemical variation, especially of volatile organic compounds (VOC) from the terpenoid compound group. These VOCs are closely involved in plant-insect interactions and, when profiled, can be used to classify plants...

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Autores principales: Clancy, Mary V., Haberer, Georg, Jud, Werner, Niederbacher, Bishu, Niederbacher, Simon, Senft, Matthias, Zytynska, Sharon E., Weisser, Wolfgang W., Schnitzler, Jörg-Peter
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7724791/
https://www.ncbi.nlm.nih.gov/pubmed/33297957
http://dx.doi.org/10.1186/s12870-020-02745-1
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author Clancy, Mary V.
Haberer, Georg
Jud, Werner
Niederbacher, Bishu
Niederbacher, Simon
Senft, Matthias
Zytynska, Sharon E.
Weisser, Wolfgang W.
Schnitzler, Jörg-Peter
author_facet Clancy, Mary V.
Haberer, Georg
Jud, Werner
Niederbacher, Bishu
Niederbacher, Simon
Senft, Matthias
Zytynska, Sharon E.
Weisser, Wolfgang W.
Schnitzler, Jörg-Peter
author_sort Clancy, Mary V.
collection PubMed
description BACKGROUND: Tansy plants (Tanacetum vulgare L.) are known for their high intraspecific chemical variation, especially of volatile organic compounds (VOC) from the terpenoid compound group. These VOCs are closely involved in plant-insect interactions and, when profiled, can be used to classify plants into groups known as chemotypes. Tansy chemotypes have been shown to influence plant-aphid interactions, however, to date no information is available on the response of different tansy chemotypes to simultaneous herbivory by more than one insect species. RESULTS: Using a multi-cuvette system, we investigated the responses of five tansy chemotypes to feeding by sucking and/or chewing herbivores (aphids and caterpillars; Metopeurum fuscoviride Stroyan and Spodoptera littoralis Boisduval). Herbivory by caterpillars following aphid infestation led to a plant chemotype-specific change in the patterns of terpenoids stored in trichome hairs and in VOC emissions. The transcriptomic analysis of a plant chemotype represents the first de novo assembly of a transcriptome in tansy and demonstrates priming effects of aphids on a subsequent herbivory. Overall, we show that the five chemotypes do not react in the same way to the two herbivores. As expected, we found that caterpillar feeding increased VOC emissions, however, a priori aphid infestation only led to a further increase in VOC emissions for some chemotypes. CONCLUSIONS: We were able to show that different chemotypes respond to the double herbivore attack in different ways, and that pre-treatment with aphids had a priming effect on plants when they were subsequently exposed to a chewing herbivore. If neighbouring chemotypes in a field population react differently to herbivory/dual herbivory, this could possibly have effects from the individual level to the group level. Individuals of some chemotypes may respond more efficiently to herbivory stress than others, and in a group environment these “louder” chemotypes may affect the local insect community, including the natural enemies of herbivores, and other neighbouring plants. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-020-02745-1.
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spelling pubmed-77247912020-12-09 Under fire-simultaneous volatilome and transcriptome analysis unravels fine-scale responses of tansy chemotypes to dual herbivore attack Clancy, Mary V. Haberer, Georg Jud, Werner Niederbacher, Bishu Niederbacher, Simon Senft, Matthias Zytynska, Sharon E. Weisser, Wolfgang W. Schnitzler, Jörg-Peter BMC Plant Biol Research Article BACKGROUND: Tansy plants (Tanacetum vulgare L.) are known for their high intraspecific chemical variation, especially of volatile organic compounds (VOC) from the terpenoid compound group. These VOCs are closely involved in plant-insect interactions and, when profiled, can be used to classify plants into groups known as chemotypes. Tansy chemotypes have been shown to influence plant-aphid interactions, however, to date no information is available on the response of different tansy chemotypes to simultaneous herbivory by more than one insect species. RESULTS: Using a multi-cuvette system, we investigated the responses of five tansy chemotypes to feeding by sucking and/or chewing herbivores (aphids and caterpillars; Metopeurum fuscoviride Stroyan and Spodoptera littoralis Boisduval). Herbivory by caterpillars following aphid infestation led to a plant chemotype-specific change in the patterns of terpenoids stored in trichome hairs and in VOC emissions. The transcriptomic analysis of a plant chemotype represents the first de novo assembly of a transcriptome in tansy and demonstrates priming effects of aphids on a subsequent herbivory. Overall, we show that the five chemotypes do not react in the same way to the two herbivores. As expected, we found that caterpillar feeding increased VOC emissions, however, a priori aphid infestation only led to a further increase in VOC emissions for some chemotypes. CONCLUSIONS: We were able to show that different chemotypes respond to the double herbivore attack in different ways, and that pre-treatment with aphids had a priming effect on plants when they were subsequently exposed to a chewing herbivore. If neighbouring chemotypes in a field population react differently to herbivory/dual herbivory, this could possibly have effects from the individual level to the group level. Individuals of some chemotypes may respond more efficiently to herbivory stress than others, and in a group environment these “louder” chemotypes may affect the local insect community, including the natural enemies of herbivores, and other neighbouring plants. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-020-02745-1. BioMed Central 2020-12-09 /pmc/articles/PMC7724791/ /pubmed/33297957 http://dx.doi.org/10.1186/s12870-020-02745-1 Text en © The Author(s) 2020 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Clancy, Mary V.
Haberer, Georg
Jud, Werner
Niederbacher, Bishu
Niederbacher, Simon
Senft, Matthias
Zytynska, Sharon E.
Weisser, Wolfgang W.
Schnitzler, Jörg-Peter
Under fire-simultaneous volatilome and transcriptome analysis unravels fine-scale responses of tansy chemotypes to dual herbivore attack
title Under fire-simultaneous volatilome and transcriptome analysis unravels fine-scale responses of tansy chemotypes to dual herbivore attack
title_full Under fire-simultaneous volatilome and transcriptome analysis unravels fine-scale responses of tansy chemotypes to dual herbivore attack
title_fullStr Under fire-simultaneous volatilome and transcriptome analysis unravels fine-scale responses of tansy chemotypes to dual herbivore attack
title_full_unstemmed Under fire-simultaneous volatilome and transcriptome analysis unravels fine-scale responses of tansy chemotypes to dual herbivore attack
title_short Under fire-simultaneous volatilome and transcriptome analysis unravels fine-scale responses of tansy chemotypes to dual herbivore attack
title_sort under fire-simultaneous volatilome and transcriptome analysis unravels fine-scale responses of tansy chemotypes to dual herbivore attack
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7724791/
https://www.ncbi.nlm.nih.gov/pubmed/33297957
http://dx.doi.org/10.1186/s12870-020-02745-1
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