Cargando…

Combined biotic stresses trigger similar transcriptomic responses but contrasting resistance against a chewing herbivore in Brassica nigra

BACKGROUND: In nature, plants are frequently exposed to simultaneous biotic stresses that activate distinct and often antagonistic defense signaling pathways. How plants integrate this information and whether they prioritize one stress over the other is not well understood. RESULTS: We investigated...

Descripción completa

Detalles Bibliográficos
Autores principales: Bonnet, Christelle, Lassueur, Steve, Ponzio, Camille, Gols, Rieta, Dicke, Marcel, Reymond, Philippe
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5513356/
https://www.ncbi.nlm.nih.gov/pubmed/28716054
http://dx.doi.org/10.1186/s12870-017-1074-7
_version_ 1783250643700416512
author Bonnet, Christelle
Lassueur, Steve
Ponzio, Camille
Gols, Rieta
Dicke, Marcel
Reymond, Philippe
author_facet Bonnet, Christelle
Lassueur, Steve
Ponzio, Camille
Gols, Rieta
Dicke, Marcel
Reymond, Philippe
author_sort Bonnet, Christelle
collection PubMed
description BACKGROUND: In nature, plants are frequently exposed to simultaneous biotic stresses that activate distinct and often antagonistic defense signaling pathways. How plants integrate this information and whether they prioritize one stress over the other is not well understood. RESULTS: We investigated the transcriptome signature of the wild annual crucifer, Brassica nigra, in response to eggs and caterpillars of Pieris brassicae butterflies, Brevicoryne brassicae aphids and the bacterial phytopathogen Xanthomonas campestris pv. raphani (Xcr). Pretreatment with egg extract, aphids, or Xcr had a weak impact on the subsequent transcriptome profile of plants challenged with caterpillars, suggesting that the second stress dominates the transcriptional response. Nevertheless, P. brassicae larval performance was strongly affected by egg extract or Xcr pretreatment and depended on the site where the initial stress was applied. Although egg extract and Xcr pretreatments inhibited insect-induced defense gene expression, suggesting salicylic acid (SA)/jasmonic acid (JA) pathway cross talk, this was not strictly correlated with larval performance. CONCLUSION: These results emphasize the need to better integrate plant responses at different levels of biological organization and to consider localized effects in order to predict the consequence of multiple stresses on plant resistance. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12870-017-1074-7) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-5513356
institution National Center for Biotechnology Information
language English
publishDate 2017
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-55133562017-07-19 Combined biotic stresses trigger similar transcriptomic responses but contrasting resistance against a chewing herbivore in Brassica nigra Bonnet, Christelle Lassueur, Steve Ponzio, Camille Gols, Rieta Dicke, Marcel Reymond, Philippe BMC Plant Biol Research Article BACKGROUND: In nature, plants are frequently exposed to simultaneous biotic stresses that activate distinct and often antagonistic defense signaling pathways. How plants integrate this information and whether they prioritize one stress over the other is not well understood. RESULTS: We investigated the transcriptome signature of the wild annual crucifer, Brassica nigra, in response to eggs and caterpillars of Pieris brassicae butterflies, Brevicoryne brassicae aphids and the bacterial phytopathogen Xanthomonas campestris pv. raphani (Xcr). Pretreatment with egg extract, aphids, or Xcr had a weak impact on the subsequent transcriptome profile of plants challenged with caterpillars, suggesting that the second stress dominates the transcriptional response. Nevertheless, P. brassicae larval performance was strongly affected by egg extract or Xcr pretreatment and depended on the site where the initial stress was applied. Although egg extract and Xcr pretreatments inhibited insect-induced defense gene expression, suggesting salicylic acid (SA)/jasmonic acid (JA) pathway cross talk, this was not strictly correlated with larval performance. CONCLUSION: These results emphasize the need to better integrate plant responses at different levels of biological organization and to consider localized effects in order to predict the consequence of multiple stresses on plant resistance. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12870-017-1074-7) contains supplementary material, which is available to authorized users. BioMed Central 2017-07-17 /pmc/articles/PMC5513356/ /pubmed/28716054 http://dx.doi.org/10.1186/s12870-017-1074-7 Text en © The Author(s). 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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.
spellingShingle Research Article
Bonnet, Christelle
Lassueur, Steve
Ponzio, Camille
Gols, Rieta
Dicke, Marcel
Reymond, Philippe
Combined biotic stresses trigger similar transcriptomic responses but contrasting resistance against a chewing herbivore in Brassica nigra
title Combined biotic stresses trigger similar transcriptomic responses but contrasting resistance against a chewing herbivore in Brassica nigra
title_full Combined biotic stresses trigger similar transcriptomic responses but contrasting resistance against a chewing herbivore in Brassica nigra
title_fullStr Combined biotic stresses trigger similar transcriptomic responses but contrasting resistance against a chewing herbivore in Brassica nigra
title_full_unstemmed Combined biotic stresses trigger similar transcriptomic responses but contrasting resistance against a chewing herbivore in Brassica nigra
title_short Combined biotic stresses trigger similar transcriptomic responses but contrasting resistance against a chewing herbivore in Brassica nigra
title_sort combined biotic stresses trigger similar transcriptomic responses but contrasting resistance against a chewing herbivore in brassica nigra
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5513356/
https://www.ncbi.nlm.nih.gov/pubmed/28716054
http://dx.doi.org/10.1186/s12870-017-1074-7
work_keys_str_mv AT bonnetchristelle combinedbioticstressestriggersimilartranscriptomicresponsesbutcontrastingresistanceagainstachewingherbivoreinbrassicanigra
AT lassueursteve combinedbioticstressestriggersimilartranscriptomicresponsesbutcontrastingresistanceagainstachewingherbivoreinbrassicanigra
AT ponziocamille combinedbioticstressestriggersimilartranscriptomicresponsesbutcontrastingresistanceagainstachewingherbivoreinbrassicanigra
AT golsrieta combinedbioticstressestriggersimilartranscriptomicresponsesbutcontrastingresistanceagainstachewingherbivoreinbrassicanigra
AT dickemarcel combinedbioticstressestriggersimilartranscriptomicresponsesbutcontrastingresistanceagainstachewingherbivoreinbrassicanigra
AT reymondphilippe combinedbioticstressestriggersimilartranscriptomicresponsesbutcontrastingresistanceagainstachewingherbivoreinbrassicanigra