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Transcriptional and metabolomic analysis of Ascophyllum nodosum mediated freezing tolerance in Arabidopsis thaliana

BACKGROUND: We have previously shown that lipophilic components (LPC) of the brown seaweed Ascophyllum nodosum (ANE) improved freezing tolerance in Arabidopsis thaliana. However, the mechanism(s) of this induced freezing stress tolerance is largely unknown. Here, we investigated LPC induced changes...

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Autores principales: Nair, Prasanth, Kandasamy, Saveetha, Zhang, Junzeng, Ji, Xiuhong, Kirby, Chris, Benkel, Bernhard, Hodges, Mark D, Critchley, Alan T, Hiltz, David, Prithiviraj, Balakrishnan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2012
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3560180/
https://www.ncbi.nlm.nih.gov/pubmed/23171218
http://dx.doi.org/10.1186/1471-2164-13-643
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author Nair, Prasanth
Kandasamy, Saveetha
Zhang, Junzeng
Ji, Xiuhong
Kirby, Chris
Benkel, Bernhard
Hodges, Mark D
Critchley, Alan T
Hiltz, David
Prithiviraj, Balakrishnan
author_facet Nair, Prasanth
Kandasamy, Saveetha
Zhang, Junzeng
Ji, Xiuhong
Kirby, Chris
Benkel, Bernhard
Hodges, Mark D
Critchley, Alan T
Hiltz, David
Prithiviraj, Balakrishnan
author_sort Nair, Prasanth
collection PubMed
description BACKGROUND: We have previously shown that lipophilic components (LPC) of the brown seaweed Ascophyllum nodosum (ANE) improved freezing tolerance in Arabidopsis thaliana. However, the mechanism(s) of this induced freezing stress tolerance is largely unknown. Here, we investigated LPC induced changes in the transcriptome and metabolome of A. thaliana undergoing freezing stress. RESULTS: Gene expression studies revealed that the accumulation of proline was mediated by an increase in the expression of the proline synthesis genes P5CS1 and P5CS2 and a marginal reduction in the expression of the proline dehydrogenase (ProDH) gene. Moreover, LPC application significantly increased the concentration of total soluble sugars in the cytosol in response to freezing stress. Arabidopsis sfr4 mutant plants, defective in the accumulation of free sugars, treated with LPC, exhibited freezing sensitivity similar to that of untreated controls. The (1)H NMR metabolite profile of LPC-treated Arabidopsis plants exposed to freezing stress revealed a spectrum dominated by chemical shifts (δ) representing soluble sugars, sugar alcohols, organic acids and lipophilic components like fatty acids, as compared to control plants. Additionally, 2D NMR spectra suggested an increase in the degree of unsaturation of fatty acids in LPC treated plants under freezing stress. These results were supported by global transcriptome analysis. Transcriptome analysis revealed that LPC treatment altered the expression of 1113 genes (5%) in comparison with untreated plants. A total of 463 genes (2%) were up regulated while 650 genes (3%) were down regulated. CONCLUSION: Taken together, the results of the experiments presented in this paper provide evidence to support LPC mediated freezing tolerance enhancement through a combination of the priming of plants for the increased accumulation of osmoprotectants and alteration of cellular fatty acid composition.
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spelling pubmed-35601802013-02-04 Transcriptional and metabolomic analysis of Ascophyllum nodosum mediated freezing tolerance in Arabidopsis thaliana Nair, Prasanth Kandasamy, Saveetha Zhang, Junzeng Ji, Xiuhong Kirby, Chris Benkel, Bernhard Hodges, Mark D Critchley, Alan T Hiltz, David Prithiviraj, Balakrishnan BMC Genomics Research Article BACKGROUND: We have previously shown that lipophilic components (LPC) of the brown seaweed Ascophyllum nodosum (ANE) improved freezing tolerance in Arabidopsis thaliana. However, the mechanism(s) of this induced freezing stress tolerance is largely unknown. Here, we investigated LPC induced changes in the transcriptome and metabolome of A. thaliana undergoing freezing stress. RESULTS: Gene expression studies revealed that the accumulation of proline was mediated by an increase in the expression of the proline synthesis genes P5CS1 and P5CS2 and a marginal reduction in the expression of the proline dehydrogenase (ProDH) gene. Moreover, LPC application significantly increased the concentration of total soluble sugars in the cytosol in response to freezing stress. Arabidopsis sfr4 mutant plants, defective in the accumulation of free sugars, treated with LPC, exhibited freezing sensitivity similar to that of untreated controls. The (1)H NMR metabolite profile of LPC-treated Arabidopsis plants exposed to freezing stress revealed a spectrum dominated by chemical shifts (δ) representing soluble sugars, sugar alcohols, organic acids and lipophilic components like fatty acids, as compared to control plants. Additionally, 2D NMR spectra suggested an increase in the degree of unsaturation of fatty acids in LPC treated plants under freezing stress. These results were supported by global transcriptome analysis. Transcriptome analysis revealed that LPC treatment altered the expression of 1113 genes (5%) in comparison with untreated plants. A total of 463 genes (2%) were up regulated while 650 genes (3%) were down regulated. CONCLUSION: Taken together, the results of the experiments presented in this paper provide evidence to support LPC mediated freezing tolerance enhancement through a combination of the priming of plants for the increased accumulation of osmoprotectants and alteration of cellular fatty acid composition. BioMed Central 2012-11-21 /pmc/articles/PMC3560180/ /pubmed/23171218 http://dx.doi.org/10.1186/1471-2164-13-643 Text en Copyright ©2012 Nair et al.; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
Nair, Prasanth
Kandasamy, Saveetha
Zhang, Junzeng
Ji, Xiuhong
Kirby, Chris
Benkel, Bernhard
Hodges, Mark D
Critchley, Alan T
Hiltz, David
Prithiviraj, Balakrishnan
Transcriptional and metabolomic analysis of Ascophyllum nodosum mediated freezing tolerance in Arabidopsis thaliana
title Transcriptional and metabolomic analysis of Ascophyllum nodosum mediated freezing tolerance in Arabidopsis thaliana
title_full Transcriptional and metabolomic analysis of Ascophyllum nodosum mediated freezing tolerance in Arabidopsis thaliana
title_fullStr Transcriptional and metabolomic analysis of Ascophyllum nodosum mediated freezing tolerance in Arabidopsis thaliana
title_full_unstemmed Transcriptional and metabolomic analysis of Ascophyllum nodosum mediated freezing tolerance in Arabidopsis thaliana
title_short Transcriptional and metabolomic analysis of Ascophyllum nodosum mediated freezing tolerance in Arabidopsis thaliana
title_sort transcriptional and metabolomic analysis of ascophyllum nodosum mediated freezing tolerance in arabidopsis thaliana
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3560180/
https://www.ncbi.nlm.nih.gov/pubmed/23171218
http://dx.doi.org/10.1186/1471-2164-13-643
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