Molecular Plant Advance Access originally published online on December 26, 2008
Molecular Plant 2009 2(3):390-406; doi:10.1093/mp/ssn080
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The Metabolic Response of Arabidopsis Roots to Oxidative Stress is Distinct from that of Heterotrophic Cells in Culture and Highlights a Complex Relationship between the Levels of Transcripts, Metabolites, and Flux
a Max-Planck Institute for Molecular Plant Physiology, Am Mühlenberg 14476, Potsdam-Golm, Germany
b Department of Plant Sciences, University of Oxford, South Parks Road, Oxford OX1 3RB, UK
c Plant Biochemistry Laboratory, Department of Plant Biology and Biotechnology and VKR Research Centre for Pro-Active Plants, University of Copenhagen, 40 Thorvaldsensvej, DK-1871 Frederiksberg C, Copenhagen, Denmark
1 To whom correspondence should be addressed. E-mail lee.sweetlove{at}plants.ox.ac.uk, fax +44 1865 275137, tel +44 1865 275000.
Metabolic adjustments are a significant, but poorly understood, part of the response of plants to oxidative stress. In a previous study (Baxter et al., 2007), the metabolic response of Arabidopsis cells in culture to induction of oxidative stress by menadione was characterized. An emergency survival strategy was uncovered in which anabolic primary metabolism was largely down-regulated in favour of catabolic and antioxidant metabolism. The response in whole plant tissues may be different and we have therefore investigated the response of Arabidopsis roots to menadione treatment, analyzing the transcriptome, metabolome and key metabolic fluxes with focus on primary as well as secondary metabolism. Using a redox-sensitive GFP, it was also shown that menadione causes redox perturbation, not just in the mitochondrion, but also in the cytosol and plastids of roots. In the first 30 min of treatment, the response was similar to the cell culture: there was a decrease in metabolites of the TCA cycle and amino acid biosynthesis and the transcriptomic response was dominated by up-regulation of DNA regulatory proteins. After 2 and 6 h of treatment, the response of the roots was different to the cell culture. Metabolite levels did not remain depressed, but instead recovered and, in the case of pyruvate, some amino acids and aliphatic glucosinolates showed a steady increase above control levels. However, no major changes in fluxes of central carbon metabolism were observed and metabolic transcripts changed largely independently of the corresponding metabolites. Together, the results suggest that root tissues can recover metabolic activity after oxidative inhibition and highlight potentially important roles for glycolysis and the oxidative pentose phosphate pathway.
Key Words: Carbon metabolism • oxidative and photo • oxidative stress • secondary metabolism; phenylpropanoids and phenolics • root biology • Arabidopsis
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