First published online November 22, 2006; 10.1104/pp.106.090431
Plant Physiology 143:312-325 (2007)
© 2007 American Society of Plant Biologists
ENVIRONMENTAL STRESS AND ADAPTATION TO STRESS
The Metabolic Response of Heterotrophic Arabidopsis Cells to Oxidative Stress1,[W]
Charles J. Baxter,
Henning Redestig,
Nicolas Schauer,
Dirk Repsilber,
Kiran R. Patil,
Jens Nielsen,
Joachim Selbig,
Junli Liu,
Alisdair R. Fernie and
Lee J. Sweetlove*
Department of Plant Sciences, University of Oxford, Oxford OX1 3RB, United Kingdom (C.J.B., L.J.S.); Max-Planck Institute for Molecular Plant Physiology, Am Mühlenberg 14476, Potsdam-Golm, Germany (H.R., N.S., D.R., J.S., A.R.F.); Center for Microbial Biotechnology, BioCentrum Technical University of Denmark, DK–2800 Kongens Lyngby, Denmark (K.R.P., J.N.); and Genetics Programme, Scottish Crop Research Institute, Dundee DD2 5DA, United Kingdom (J.L.)
To cope with oxidative stress, the metabolic network of plant cells must be reconfigured either to bypass damaged enzymes or to support adaptive responses. To characterize the dynamics of metabolic change during oxidative stress, heterotrophic Arabidopsis (Arabidopsis thaliana) cells were treated with menadione and changes in metabolite abundance and 13C-labeling kinetics were quantified in a time series of samples taken over a 6 h period. Oxidative stress had a profound effect on the central metabolic pathways with extensive metabolic inhibition radiating from the tricarboxylic acid cycle and including large sectors of amino acid metabolism. Sequential accumulation of metabolites in specific pathways indicated a subsequent backing up of glycolysis and a diversion of carbon into the oxidative pentose phosphate pathway. Microarray analysis revealed a coordinated transcriptomic response that represents an emergency coping strategy allowing the cell to survive the metabolic hiatus. Rather than attempt to replace inhibited enzymes, transcripts encoding these enzymes are in fact down-regulated while an antioxidant defense response is mounted. In addition, a major switch from anabolic to catabolic metabolism is signaled. Metabolism is also reconfigured to bypass damaged steps (e.g. induction of an external NADH dehydrogenase of the mitochondrial respiratory chain). The overall metabolic response of Arabidopsis cells to oxidative stress is remarkably similar to the superoxide and hydrogen peroxide stimulons of bacteria and yeast (Saccharomyces cerevisiae), suggesting that the stress regulatory and signaling pathways of plants and microbes may share common elements.
1 This work was supported by the Biotechnology and Biological Sciences Research Council, United Kingdom (to L.J.S.), the Bundesministerium für Bildung und Forschung in the framework of a Deutsche Israeli Project award and by the Max Planck Gesellschaft (to N.S. and A.R.F.), the Center for Microbial Biotechnology, who receive funding from the Danish Agency for Science, Technology, and Innovation (to K.P.), and the Scottish Executive Environment and Rural Affairs Department (to J.L.).
The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Lee J. Sweetlove (lee.sweetlove{at}plants.ox.ac.uk).
[W] The online version of this article contains Web-only data.
www.plantphysiol.org/cgi/doi/10.1104/pp.106.090431
* Corresponding author; e-mail lee.sweetlove{at}plants.ox.ac.uk; fax 44–1865–275074.
Received September 28, 2006;
accepted November 10, 2006;
published November 22, 2006.
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