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Poplar stem transcriptome is massively remodelled in response to single or repeated mechanical stimuli

BACKGROUND: Trees experience mechanical stimuli -like wind- that trigger thigmomorphogenetic syndrome, leading to modifications of plant growth and wood quality. This syndrome affects tree productivity but is also believed to improve tree acclimation to chronic wind. Wind is particularly challenging...

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Autores principales: Pomiès, Lise, Decourteix, Mélanie, Franchel, Jérôme, Moulia, Bruno, Leblanc-Fournier, Nathalie
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5392906/
https://www.ncbi.nlm.nih.gov/pubmed/28412928
http://dx.doi.org/10.1186/s12864-017-3670-1
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author Pomiès, Lise
Decourteix, Mélanie
Franchel, Jérôme
Moulia, Bruno
Leblanc-Fournier, Nathalie
author_facet Pomiès, Lise
Decourteix, Mélanie
Franchel, Jérôme
Moulia, Bruno
Leblanc-Fournier, Nathalie
author_sort Pomiès, Lise
collection PubMed
description BACKGROUND: Trees experience mechanical stimuli -like wind- that trigger thigmomorphogenetic syndrome, leading to modifications of plant growth and wood quality. This syndrome affects tree productivity but is also believed to improve tree acclimation to chronic wind. Wind is particularly challenging for trees, because of their stature and perenniality. Climate change forecasts are predicting that the occurrence of high wind will worsen, making it increasingly vital to understand the mechanisms regulating thigmomorphogenesis, especially in perennial plants. By extension, this also implies factoring in the recurring nature of wind episodes. However, data on the molecular processes underpinning mechanoperception and transduction of mechanical signals, and their dynamics, are still dramatically lacking in trees. RESULTS: Here we performed a genome-wide and time-series analysis of poplar transcriptional responsiveness to transitory and recurring controlled stem bending, mimicking wind. The study revealed that 6% of the poplar genome is differentially expressed after a single transient bending. The combination of clustering, Gene Ontology categorization and time-series expression approaches revealed the diversity of gene expression patterns and biological processes affected by stem bending. Short-term transcriptomic responses entailed a rapid stimulation of plant defence and abiotic stress signalling pathways, including ethylene and jasmonic acid signalling but also photosynthesis process regulation. Late transcriptomic responses affected genes involved in cell wall organization and/or wood development. An analysis of the molecular impact of recurring bending found that the vast majority (96%) of the genes differentially expressed after a first bending presented reduced or even net-zero amplitude regulation after the second exposure to bending. CONCLUSION: This study constitutes the first dynamic characterization of the molecular processes affected by single or repeated stem bending in poplar. Moreover, the global attenuation of the transcriptional responses, observed from as early as after a second bending, indicates the existence of a mechanism governing a fine tuning of plant responsiveness. This points toward several mechanistic pathways that can now be targeted to elucidate the complex dynamics of wind acclimation. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-017-3670-1) contains supplementary material, which is available to authorized users.
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spelling pubmed-53929062017-04-17 Poplar stem transcriptome is massively remodelled in response to single or repeated mechanical stimuli Pomiès, Lise Decourteix, Mélanie Franchel, Jérôme Moulia, Bruno Leblanc-Fournier, Nathalie BMC Genomics Research Article BACKGROUND: Trees experience mechanical stimuli -like wind- that trigger thigmomorphogenetic syndrome, leading to modifications of plant growth and wood quality. This syndrome affects tree productivity but is also believed to improve tree acclimation to chronic wind. Wind is particularly challenging for trees, because of their stature and perenniality. Climate change forecasts are predicting that the occurrence of high wind will worsen, making it increasingly vital to understand the mechanisms regulating thigmomorphogenesis, especially in perennial plants. By extension, this also implies factoring in the recurring nature of wind episodes. However, data on the molecular processes underpinning mechanoperception and transduction of mechanical signals, and their dynamics, are still dramatically lacking in trees. RESULTS: Here we performed a genome-wide and time-series analysis of poplar transcriptional responsiveness to transitory and recurring controlled stem bending, mimicking wind. The study revealed that 6% of the poplar genome is differentially expressed after a single transient bending. The combination of clustering, Gene Ontology categorization and time-series expression approaches revealed the diversity of gene expression patterns and biological processes affected by stem bending. Short-term transcriptomic responses entailed a rapid stimulation of plant defence and abiotic stress signalling pathways, including ethylene and jasmonic acid signalling but also photosynthesis process regulation. Late transcriptomic responses affected genes involved in cell wall organization and/or wood development. An analysis of the molecular impact of recurring bending found that the vast majority (96%) of the genes differentially expressed after a first bending presented reduced or even net-zero amplitude regulation after the second exposure to bending. CONCLUSION: This study constitutes the first dynamic characterization of the molecular processes affected by single or repeated stem bending in poplar. Moreover, the global attenuation of the transcriptional responses, observed from as early as after a second bending, indicates the existence of a mechanism governing a fine tuning of plant responsiveness. This points toward several mechanistic pathways that can now be targeted to elucidate the complex dynamics of wind acclimation. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-017-3670-1) contains supplementary material, which is available to authorized users. BioMed Central 2017-04-17 /pmc/articles/PMC5392906/ /pubmed/28412928 http://dx.doi.org/10.1186/s12864-017-3670-1 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
Pomiès, Lise
Decourteix, Mélanie
Franchel, Jérôme
Moulia, Bruno
Leblanc-Fournier, Nathalie
Poplar stem transcriptome is massively remodelled in response to single or repeated mechanical stimuli
title Poplar stem transcriptome is massively remodelled in response to single or repeated mechanical stimuli
title_full Poplar stem transcriptome is massively remodelled in response to single or repeated mechanical stimuli
title_fullStr Poplar stem transcriptome is massively remodelled in response to single or repeated mechanical stimuli
title_full_unstemmed Poplar stem transcriptome is massively remodelled in response to single or repeated mechanical stimuli
title_short Poplar stem transcriptome is massively remodelled in response to single or repeated mechanical stimuli
title_sort poplar stem transcriptome is massively remodelled in response to single or repeated mechanical stimuli
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5392906/
https://www.ncbi.nlm.nih.gov/pubmed/28412928
http://dx.doi.org/10.1186/s12864-017-3670-1
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