Interactive Responses of <i>Solanum Dulcamara</i> to Drought and Insect Feeding are Herbivore Species-Specific

In nature, plants are frequently subjected to multiple biotic and abiotic stresses, resulting in a convergence of adaptive responses. We hypothesised that hormonal signalling regulating defences to different herbivores may interact with drought responses, causing distinct resistance phenotypes. To t...

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Main Authors: Duy Nguyen, Yvonne Poeschl, Tobias Lortzing, Rick Hoogveld, Andreas Gogol-Döring, Simona M. Cristescu, Anke Steppuhn, Celestina Mariani, Ivo Rieu, Nicole M. van Dam
Format: Article
Language:English
Published: MDPI AG 2018-12-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/19/12/3845
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spelling doaj-e70a0628d6b9425eb525d49db24a23172020-11-25T00:55:44ZengMDPI AGInternational Journal of Molecular Sciences1422-00672018-12-011912384510.3390/ijms19123845ijms19123845Interactive Responses of <i>Solanum Dulcamara</i> to Drought and Insect Feeding are Herbivore Species-SpecificDuy Nguyen0Yvonne Poeschl1Tobias Lortzing2Rick Hoogveld3Andreas Gogol-Döring4Simona M. Cristescu5Anke Steppuhn6Celestina Mariani7Ivo Rieu8Nicole M. van Dam9Molecular Interaction Ecology, Institute of Water and Wetland Research, Radboud University, P.O. Box 9010, 6500 GL Nijmegen, The NetherlandsGerman Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Deutscher Platz 5e, 04103 Leipzig, GermanyMolecular Ecology, Institute of Biology, Dahlem Centre of Plant Sciences, Freie Universität Berlin, Albrecht-Thaer-Weg 6, 14195 Berlin, GermanyMolecular Interaction Ecology, Institute of Water and Wetland Research, Radboud University, P.O. Box 9010, 6500 GL Nijmegen, The NetherlandsGerman Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Deutscher Platz 5e, 04103 Leipzig, GermanyMolecular and Laser Physics, Institute for Molecules and Materials, Radboud University, PO Box 9010, 6500 GL Nijmegen, The NetherlandsMolecular Ecology, Institute of Biology, Dahlem Centre of Plant Sciences, Freie Universität Berlin, Albrecht-Thaer-Weg 6, 14195 Berlin, GermanyMolecular Plant Physiology, Institute for Water and Wetland Research, Radboud University, PO Box 9010, 6500 GL Nijmegen, The NetherlandsMolecular Plant Physiology, Institute for Water and Wetland Research, Radboud University, PO Box 9010, 6500 GL Nijmegen, The NetherlandsMolecular Interaction Ecology, Institute of Water and Wetland Research, Radboud University, P.O. Box 9010, 6500 GL Nijmegen, The NetherlandsIn nature, plants are frequently subjected to multiple biotic and abiotic stresses, resulting in a convergence of adaptive responses. We hypothesised that hormonal signalling regulating defences to different herbivores may interact with drought responses, causing distinct resistance phenotypes. To test this, we studied the hormonal and transcriptomic responses of <i>Solanum dulcamara</i> subjected to drought and herbivory by the generalist <i>Spodoptera exigua</i> (beet armyworm; BAW) or the specialist <i>Leptinotarsa decemlineata</i> (Colorado potato beetle; CPB). Bioassays showed that the performance of BAW, but not CPB, decreased on plants under drought compared to controls. While drought did not alter BAW-induced hormonal responses, it enhanced the CPB-induced accumulation of jasmonic acid and salicylic acid (SA), and suppressed ethylene (ET) emission. Microarray analyses showed that under drought, BAW herbivory enhanced several herbivore-induced responses, including cell-wall remodelling and the metabolism of carbohydrates, lipids, and secondary metabolites. In contrast, CPB herbivory enhanced several photosynthesis-related and pathogen responses in drought-stressed plants. This may divert resources away from defence production and increase leaf nutritive value. In conclusion, while BAW suffers from the drought-enhanced defences, CPB may benefit from the effects of enhanced SA and reduced ET signalling. This suggests that the fine-tuned interaction between the plant and its specialist herbivore is sustained under drought.https://www.mdpi.com/1422-0067/19/12/3845<i>Solanum dulcamara</i><i>Spodoptera exigua</i><i>Leptinotarsa decemlineata</i>drought responseplant defencehormonal signallingtranscriptional regulation
collection DOAJ
language English
format Article
sources DOAJ
author Duy Nguyen
Yvonne Poeschl
Tobias Lortzing
Rick Hoogveld
Andreas Gogol-Döring
Simona M. Cristescu
Anke Steppuhn
Celestina Mariani
Ivo Rieu
Nicole M. van Dam
spellingShingle Duy Nguyen
Yvonne Poeschl
Tobias Lortzing
Rick Hoogveld
Andreas Gogol-Döring
Simona M. Cristescu
Anke Steppuhn
Celestina Mariani
Ivo Rieu
Nicole M. van Dam
Interactive Responses of <i>Solanum Dulcamara</i> to Drought and Insect Feeding are Herbivore Species-Specific
International Journal of Molecular Sciences
<i>Solanum dulcamara</i>
<i>Spodoptera exigua</i>
<i>Leptinotarsa decemlineata</i>
drought response
plant defence
hormonal signalling
transcriptional regulation
author_facet Duy Nguyen
Yvonne Poeschl
Tobias Lortzing
Rick Hoogveld
Andreas Gogol-Döring
Simona M. Cristescu
Anke Steppuhn
Celestina Mariani
Ivo Rieu
Nicole M. van Dam
author_sort Duy Nguyen
title Interactive Responses of <i>Solanum Dulcamara</i> to Drought and Insect Feeding are Herbivore Species-Specific
title_short Interactive Responses of <i>Solanum Dulcamara</i> to Drought and Insect Feeding are Herbivore Species-Specific
title_full Interactive Responses of <i>Solanum Dulcamara</i> to Drought and Insect Feeding are Herbivore Species-Specific
title_fullStr Interactive Responses of <i>Solanum Dulcamara</i> to Drought and Insect Feeding are Herbivore Species-Specific
title_full_unstemmed Interactive Responses of <i>Solanum Dulcamara</i> to Drought and Insect Feeding are Herbivore Species-Specific
title_sort interactive responses of <i>solanum dulcamara</i> to drought and insect feeding are herbivore species-specific
publisher MDPI AG
series International Journal of Molecular Sciences
issn 1422-0067
publishDate 2018-12-01
description In nature, plants are frequently subjected to multiple biotic and abiotic stresses, resulting in a convergence of adaptive responses. We hypothesised that hormonal signalling regulating defences to different herbivores may interact with drought responses, causing distinct resistance phenotypes. To test this, we studied the hormonal and transcriptomic responses of <i>Solanum dulcamara</i> subjected to drought and herbivory by the generalist <i>Spodoptera exigua</i> (beet armyworm; BAW) or the specialist <i>Leptinotarsa decemlineata</i> (Colorado potato beetle; CPB). Bioassays showed that the performance of BAW, but not CPB, decreased on plants under drought compared to controls. While drought did not alter BAW-induced hormonal responses, it enhanced the CPB-induced accumulation of jasmonic acid and salicylic acid (SA), and suppressed ethylene (ET) emission. Microarray analyses showed that under drought, BAW herbivory enhanced several herbivore-induced responses, including cell-wall remodelling and the metabolism of carbohydrates, lipids, and secondary metabolites. In contrast, CPB herbivory enhanced several photosynthesis-related and pathogen responses in drought-stressed plants. This may divert resources away from defence production and increase leaf nutritive value. In conclusion, while BAW suffers from the drought-enhanced defences, CPB may benefit from the effects of enhanced SA and reduced ET signalling. This suggests that the fine-tuned interaction between the plant and its specialist herbivore is sustained under drought.
topic <i>Solanum dulcamara</i>
<i>Spodoptera exigua</i>
<i>Leptinotarsa decemlineata</i>
drought response
plant defence
hormonal signalling
transcriptional regulation
url https://www.mdpi.com/1422-0067/19/12/3845
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