Transcriptomic analysis of the role of carboxylic acids in metabolite signaling in Arabidopsis leaves.

The transcriptional response to metabolites is an important mechanism by which plants integrate information about cellular energy and nutrient status. Although some carboxylic acids have been implicated in the regulation of gene expression for select transcripts, it is unclear whether all carboxylic...

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Main Authors: Finkemeier, I, König, A, Heard, W, Nunes-Nesi, A, Pham, P, Leister, D, Fernie, A, Sweetlove, L
Format: Journal article
Language:English
Published: 2013
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author Finkemeier, I
König, A
Heard, W
Nunes-Nesi, A
Pham, P
Leister, D
Fernie, A
Sweetlove, L
author_facet Finkemeier, I
König, A
Heard, W
Nunes-Nesi, A
Pham, P
Leister, D
Fernie, A
Sweetlove, L
author_sort Finkemeier, I
collection OXFORD
description The transcriptional response to metabolites is an important mechanism by which plants integrate information about cellular energy and nutrient status. Although some carboxylic acids have been implicated in the regulation of gene expression for select transcripts, it is unclear whether all carboxylic acids have the same effect, how many transcripts are affected, and how carboxylic acid signaling is integrated with other metabolite signals. In this study, we demonstrate that perturbations in cellular concentrations of citrate, and to a lesser extent malate, have a major impact on nucleus-encoded transcript abundance. Functional categories of transcripts that were targeted by both organic acids included photosynthesis, cell wall, biotic stress, and protein synthesis. Specific functional categories that were only regulated by citrate included tricarboxylic acid cycle, nitrogen metabolism, sulfur metabolism, and DNA synthesis. Further quantitative real-time polymerase chain reaction analysis of specific citrate-responsive transcripts demonstrated that the transcript response to citrate is time and concentration dependent and distinct from other organic acids and sugars. Feeding of isocitrate as well as the nonmetabolizable citrate analog tricarballylate revealed that the abundance of selected marker transcripts is responsive to citrate and not downstream metabolites. Interestingly, the transcriptome response to citrate feeding was most similar to those observed after biotic stress treatments and the gibberellin biosynthesis inhibitor paclobutrazol. Feeding of citrate to mutants with defects in plant hormone signaling pathways did not completely abolish the transcript response but hinted at a link with jasmonic acid and gibberellin signaling pathways. Our results suggest that changes in carboxylic acid abundances can be perceived and signaled in Arabidopsis (Arabidopsis thaliana) by as yet unknown signaling pathways.
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spelling oxford-uuid:4ce969af-c1f7-4f71-bc38-9cb5fc87841b2022-03-26T15:52:16ZTranscriptomic analysis of the role of carboxylic acids in metabolite signaling in Arabidopsis leaves.Journal articlehttp://purl.org/coar/resource_type/c_dcae04bcuuid:4ce969af-c1f7-4f71-bc38-9cb5fc87841bEnglishSymplectic Elements at Oxford2013Finkemeier, IKönig, AHeard, WNunes-Nesi, APham, PLeister, DFernie, ASweetlove, LThe transcriptional response to metabolites is an important mechanism by which plants integrate information about cellular energy and nutrient status. Although some carboxylic acids have been implicated in the regulation of gene expression for select transcripts, it is unclear whether all carboxylic acids have the same effect, how many transcripts are affected, and how carboxylic acid signaling is integrated with other metabolite signals. In this study, we demonstrate that perturbations in cellular concentrations of citrate, and to a lesser extent malate, have a major impact on nucleus-encoded transcript abundance. Functional categories of transcripts that were targeted by both organic acids included photosynthesis, cell wall, biotic stress, and protein synthesis. Specific functional categories that were only regulated by citrate included tricarboxylic acid cycle, nitrogen metabolism, sulfur metabolism, and DNA synthesis. Further quantitative real-time polymerase chain reaction analysis of specific citrate-responsive transcripts demonstrated that the transcript response to citrate is time and concentration dependent and distinct from other organic acids and sugars. Feeding of isocitrate as well as the nonmetabolizable citrate analog tricarballylate revealed that the abundance of selected marker transcripts is responsive to citrate and not downstream metabolites. Interestingly, the transcriptome response to citrate feeding was most similar to those observed after biotic stress treatments and the gibberellin biosynthesis inhibitor paclobutrazol. Feeding of citrate to mutants with defects in plant hormone signaling pathways did not completely abolish the transcript response but hinted at a link with jasmonic acid and gibberellin signaling pathways. Our results suggest that changes in carboxylic acid abundances can be perceived and signaled in Arabidopsis (Arabidopsis thaliana) by as yet unknown signaling pathways.
spellingShingle Finkemeier, I
König, A
Heard, W
Nunes-Nesi, A
Pham, P
Leister, D
Fernie, A
Sweetlove, L
Transcriptomic analysis of the role of carboxylic acids in metabolite signaling in Arabidopsis leaves.
title Transcriptomic analysis of the role of carboxylic acids in metabolite signaling in Arabidopsis leaves.
title_full Transcriptomic analysis of the role of carboxylic acids in metabolite signaling in Arabidopsis leaves.
title_fullStr Transcriptomic analysis of the role of carboxylic acids in metabolite signaling in Arabidopsis leaves.
title_full_unstemmed Transcriptomic analysis of the role of carboxylic acids in metabolite signaling in Arabidopsis leaves.
title_short Transcriptomic analysis of the role of carboxylic acids in metabolite signaling in Arabidopsis leaves.
title_sort transcriptomic analysis of the role of carboxylic acids in metabolite signaling in arabidopsis leaves
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