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Functional Dissection of Sugar Signals Affecting Gene Expression in Arabidopsis thaliana
Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).ORCID iD: 0000-0002-6959-3284
Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).ORCID iD: 0000-0001-8685-9665
2014 (English)In: PLoS ONE, ISSN 1932-6203, Vol. 9, no 6, e100312- p.Article in journal (Refereed) Published
Abstract [en]

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.

Place, publisher, year, edition, pages
2014. Vol. 9, no 6, e100312- p.
National Category
URN: urn:nbn:se:umu:diva-91274DOI: 10.1371/journal.pone.0100312ISI: 000338276300062OAI: diva2:735476
Available from: 2014-07-28 Created: 2014-07-28 Last updated: 2015-04-29Bibliographically approved
In thesis
1. Sugar-modulated gene expression and cell division in cell culture and seedlings of A. thaliana
Open this publication in new window or tab >>Sugar-modulated gene expression and cell division in cell culture and seedlings of A. thaliana
2014 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Throughout their life cycle, plants adjust growth in response to their developmental and environmental situation within the limits of their energetic capacities. This capacity is defined by the local sugar availability, which is constantly modulated through synthesis, transport and consumption of sugar. The monitoring of sugar presence is carried out by a complex signalling network in which simple sugars (e.g. glucose, fructose and sucrose) act as metabolic signals for the modulation of physiological processes. However, often it remains unclear whether the regulation is induced by the simple sugars themselves or by their derivatives generated during sugar metabolism. This thesis focuses on the dissection of distinct sugar signals, their generation, perception and impact on the modulation of gene expression and cell division both in cell culture and young seedlings.

Based on a stem-cell-like A. thaliana cell culture, which could be sustained in a hormone-free media, a new biological system, supplied with Xyl as the only carbon source was developed. The performance of a variety of sugar and sugar analogue treatments in this novel system allowed for the identification of sugar-responsive candidate genes, which were specifically regulated by glucose, fructose and sucrose. For several genes (e.g. bZIP63, AT5g22920, TPS9, MGD2 and BT2), this regulation required both sugar transport into the cytosol and metabolisation for the generation of the signal. Furthermore, gene expression analyses in young A. thaliana seedlings indicated the requirement for the catalytic activity of hexokinase 1 in the regulation of bZIP63, Atg22920 and BT2 under conditions of a perturbed carbohydrate balance. These findings have been combined in a proposed model for the transcriptional regulation of bZIP63, AT5g22920, TPS9, MGD2 and BT2, which further proposes a function of those genes in the regulation of cell division.

The optimisation of a protocol for long-term real-time live-cell imaging provided a valuable tool to show that, similar to gene expression, the progression of cell division depended on a sugar-type-specific regulation at the single-cell level; this regulation was most likely caused by prolongation of the interphase. Together with the observation of cell death and growth arrest of the primary root in intact seedlings in response to the glucose analogue 2dog, this led to the conclusion that sugar signals themselves were sufficient to induce cell division. However, the continuation of cell cycle progression and consequently organ growth over long-time required the availability of the energy contained in the sugar.

Place, publisher, year, edition, pages
Umeå: Umeå University, 2014. 59 p.
Arabidopsis thaliana, carbohydrates, cell culture, cell division, gene expression, homeostasis, live cell imaging, sugar-signals, sugar-analogues
National Category
Biochemistry and Molecular Biology Botany Cell Biology
Research subject
Physiological Botany
urn:nbn:se:umu:diva-96580 (URN)978-91-7601-174-4 (ISBN)
Public defence
2014-12-17, KB3A9; KBC huset, Umeå universitet, Umeå, 10:00 (English)
Available from: 2014-11-26 Created: 2014-11-24 Last updated: 2015-04-29Bibliographically approved

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Kunz, SabinePesquet, EdouardKleczkowski, Leszek A.
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