First published online April 15, 2005; 10.1104/pp.104.053793
Plant Physiology 138:304-318 (2005)
© 2005 American Society of Plant Biologists
ENVIRONMENTAL STRESS AND ADAPTATION
Systems Rebalancing of Metabolism in Response to Sulfur Deprivation, as Revealed by Metabolome Analysis of Arabidopsis Plants1,[w]
Victoria J. Nikiforova*,
Joachim Kopka,
Vladimir Tolstikov,
Oliver Fiehn,
Laura Hopkins,
Malcolm J. Hawkesford,
Holger Hesse and
Rainer Hoefgen
Max Planck Institute of Molecular Plant Physiology, Golm 14476, Germany (V.J.N., J.K., V.T., O.F., H.H., R.H.); Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, Moscow 127276, Russia (V.J.N.); and Rothamsted Research, West Common, Harpenden AL5 2JQ, United Kingdom (L.H., M.J.H.)
Sulfur is an essential macroelement in plant and animal nutrition. Plants assimilate inorganic sulfate into two sulfur-containing amino acids, cysteine and methionine. Low supply of sulfate leads to decreased sulfur pools within plant tissues. As sulfur-related metabolites represent an integral part of plant metabolism with multiple interactions, sulfur deficiency stress induces a number of adaptive responses, which must be coordinated. To reveal the coordinating network of adaptations to sulfur deficiency, metabolite profiling of Arabidopsis has been undertaken. Gas chromatography-mass spectrometry and liquid chromatography-mass spectrometry techniques revealed the response patterns of 6,023 peaks of nonredundant ion traces and relative concentration levels of 134 nonredundant compounds of known chemical structure. Here, we provide a catalogue of the detected metabolic changes and reconstruct the coordinating network of their mutual influences. The observed decrease in biomass, as well as in levels of proteins, chlorophylls, and total RNA, gives evidence for a general reduction of metabolic activity under conditions of depleted sulfur supply. This is achieved by a systemic adjustment of metabolism involving the major metabolic pathways. Sulfur/carbon/nitrogen are partitioned by accumulation of metabolites along the pathway O-acetylserine to serine to glycine, and are further channeled together with the nitrogen-rich compound glutamine into allantoin. Mutual influences between sulfur assimilation, nitrogen imbalance, lipid breakdown, purine metabolism, and enhanced photorespiration associated with sulfur-deficiency stress are revealed in this study. These responses may be assembled into a global scheme of metabolic regulation induced by sulfur nutritional stress, which optimizes resources for seed production.
1 This work was supported by the European Union commission through funding of FP5 project QLRT–2000–00103 and by the Max-Planck-Society. Rothamsted Research receives grant-aided support from the Biotechnology and Biological Sciences Research Council of the United Kingdom.
[w] The online version of this article contains Web-only data.
Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.104.053793.
* Corresponding author; e-mail nikiforova{at}mpimp-golm.mpg.de; fax 49–331–5678134.
Received September 20, 2004;
returned for revision December 30, 2004;
accepted March 4, 2005.
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