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Published on November 22, 2006; 10.1104/pp.106.090431


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Received September 28, 2006
Accepted November 10, 2006

The Metabolic Response of Heterotrophic Arabidopsis Cells to Oxidative Stress

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, South Parks Road, Oxford, OX1 3RB, UK
Max-Planck Institute for Molecular Plant Physiology, Am Mühlenberg 14476, Potsdam-Golm, Germany
Center for Microbial Biotechnology, BioCentrum-DTU, Technical University of Denmark, Building 223, DK-2800 Kgs. Lyngby, Denmark
Genetics Programme, Scottish Crop Research Institute, Dundee DD2 5DA, UK

* Corresponding author; email: lee.sweetlove{at}plants.ox.ac.uk.

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 characterise the dynamics of metabolic change during oxidative stress, heterotrophic Arabidopsis cells were treated with menadione and changes in metabolite abundance and 13C labelling 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 defence response is mounted. In addition, a major switch from anabolic to catabolic metabolism is signalled. 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 suggesting that the stress-regulatory and signalling pathways of plants and microbes may share common elements.




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