Functional dissection of sugar signals affecting gene expression in Arabidopsis thaliana.

BACKGROUND: Sugars modulate expression of hundreds of genes in plants. Previous studies on sugar signaling, using intact plants or plant tissues, were hampered by tissue heterogeneity, uneven sugar transport and/or inter-conversions of the applied sugars. This, in turn, could obscure the identity of...

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Main Authors: Sabine Kunz, Edouard Pesquet, Leszek A Kleczkowski
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2014-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC4065033?pdf=render
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spelling doaj-3fcb266c8fed4ab180870ab9648399572020-11-25T01:56:02ZengPublic Library of Science (PLoS)PLoS ONE1932-62032014-01-0196e10031210.1371/journal.pone.0100312Functional dissection of sugar signals affecting gene expression in Arabidopsis thaliana.Sabine KunzEdouard PesquetLeszek A KleczkowskiBACKGROUND: Sugars modulate expression of hundreds of genes in plants. Previous studies on sugar signaling, using intact plants or plant tissues, were hampered by tissue heterogeneity, uneven sugar transport and/or inter-conversions of the applied sugars. This, in turn, could obscure the identity of a specific sugar that acts as a signal affecting expression of given gene in a given tissue or cell-type. METHODOLOGY/PRINCIPAL FINDINGS: To bypass those biases, we have developed a novel biological system, based on stem-cell-like Arabidopsis suspension culture. The cells were grown in a hormone-free medium and were sustained on xylose as the only carbon source. Using functional genomics we have identified 290 sugar responsive genes, responding rapidly (within 1 h) and specifically to low concentration (1 mM) of glucose, fructose and/or sucrose. For selected genes, the true nature of the signaling sugar molecules and sites of sugar perception were further clarified using non-metabolizable sugar analogues. Using both transgenic and wild-type A. thaliana seedlings, it was shown that the expression of selected sugar-responsive genes was not restricted to a specific tissue or cell type and responded to photoperiod-related changes in sugar availability. This suggested that sugar-responsiveness of genes identified in the cell culture system was not biased toward heterotrophic background and resembled that in whole plants. CONCLUSIONS: Altogether, our research strategy, using a combination of cell culture and whole plants, has provided an unequivocal evidence for the identity of sugar-responsive genes and the identity of the sugar signaling molecules, independently from their inter-conversions or use for energy metabolism.http://europepmc.org/articles/PMC4065033?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Sabine Kunz
Edouard Pesquet
Leszek A Kleczkowski
spellingShingle Sabine Kunz
Edouard Pesquet
Leszek A Kleczkowski
Functional dissection of sugar signals affecting gene expression in Arabidopsis thaliana.
PLoS ONE
author_facet Sabine Kunz
Edouard Pesquet
Leszek A Kleczkowski
author_sort Sabine Kunz
title Functional dissection of sugar signals affecting gene expression in Arabidopsis thaliana.
title_short Functional dissection of sugar signals affecting gene expression in Arabidopsis thaliana.
title_full Functional dissection of sugar signals affecting gene expression in Arabidopsis thaliana.
title_fullStr Functional dissection of sugar signals affecting gene expression in Arabidopsis thaliana.
title_full_unstemmed Functional dissection of sugar signals affecting gene expression in Arabidopsis thaliana.
title_sort functional dissection of sugar signals affecting gene expression in arabidopsis thaliana.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2014-01-01
description BACKGROUND: Sugars modulate expression of hundreds of genes in plants. Previous studies on sugar signaling, using intact plants or plant tissues, were hampered by tissue heterogeneity, uneven sugar transport and/or inter-conversions of the applied sugars. This, in turn, could obscure the identity of a specific sugar that acts as a signal affecting expression of given gene in a given tissue or cell-type. METHODOLOGY/PRINCIPAL FINDINGS: To bypass those biases, we have developed a novel biological system, based on stem-cell-like Arabidopsis suspension culture. The cells were grown in a hormone-free medium and were sustained on xylose as the only carbon source. Using functional genomics we have identified 290 sugar responsive genes, responding rapidly (within 1 h) and specifically to low concentration (1 mM) of glucose, fructose and/or sucrose. For selected genes, the true nature of the signaling sugar molecules and sites of sugar perception were further clarified using non-metabolizable sugar analogues. Using both transgenic and wild-type A. thaliana seedlings, it was shown that the expression of selected sugar-responsive genes was not restricted to a specific tissue or cell type and responded to photoperiod-related changes in sugar availability. This suggested that sugar-responsiveness of genes identified in the cell culture system was not biased toward heterotrophic background and resembled that in whole plants. CONCLUSIONS: Altogether, our research strategy, using a combination of cell culture and whole plants, has provided an unequivocal evidence for the identity of sugar-responsive genes and the identity of the sugar signaling molecules, independently from their inter-conversions or use for energy metabolism.
url http://europepmc.org/articles/PMC4065033?pdf=render
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