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First published online April 3, 2009; 10.1104/pp.108.133629

Plant Physiology 150:772-785 (2009)
© 2009 American Society of Plant Biologists

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ENVIRONMENTAL STRESS AND ADAPTATION TO STRESS

Multilevel Analysis of Primary Metabolism Provides New Insights into the Role of Potassium Nutrition for Glycolysis and Nitrogen Assimilation in Arabidopsis Roots1,[W],[OA]

Patrick Armengaud, Ronan Sulpice, Anthony J. Miller, Mark Stitt, Anna Amtmann* and Yves Gibon2

Plant Science Group, Faculty of Biomedical and Life Sciences, University of Glasgow, G128QQ Glasgow, United Kingdom (P.A., A.A.); Max Planck Institute of Molecular Plant Physiology, D–14476 Golm, Germany (R.S., M.S., Y.G.); and Centre for Soils and Ecosystem Function, Rothamsted Research, Harpenden, Hertfordshire AL5 2JQ, United Kingdom (A.J.M.)

Potassium (K) is required in large quantities by growing crops, but faced with high fertilizer prices, farmers often neglect K application in favor of nitrogen and phosphorus. As a result, large areas of farmland are now depleted of K. K deficiency affects the metabolite content of crops with negative consequences for nutritional quality, mechanical stability, and pathogen/pest resistance. Known functions of K in solute transport, protein synthesis, and enzyme activation point to a close relationship between K and metabolism, but it is unclear which of these are the most critical ones and should be targeted in biotechnological efforts to improve K usage efficiency. To identify metabolic targets and signaling components of K stress, we adopted a multilevel approach combining transcript profiles with enzyme activities and metabolite profiles of Arabidopsis (Arabidopsis thaliana) plants subjected to low K and K resupply. Roots and shoots were analyzed separately. Our results show that regulation of enzymes at the level of transcripts and proteins is likely to play an important role in plant adaptation to K deficiency by (1) maintaining carbon flux into amino acids and proteins, (2) decreasing negative metabolic charge, and (3) increasing the nitrogen-carbon ratio in amino acids. However, changes in transcripts and enzyme activities do not explain the strong and reversible depletion of pyruvate and accumulation of sugars observed in the roots of low-K plants. We propose that the primary cause of metabolic disorders in low-K plants resides in the direct inhibition of pyruvate kinase activity by low cytoplasmic K in root cells.


1 This work was supported by the Biotechnology and Biological Sciences Research Council (Wain travel fellowship to P.A. and grant no. BB/D006775 to A.A.) and the German Ministry of Education and Research within the German Plant Genome Initiative GABI-GNADE and GABI-GENOPLANTE (to M.S.). Rothamsted Research is grant aided by the Biotechnology and Biological Sciences Research Council.

2 Present address: INRA-Bordeaux, Université de Bordeaux, UMR619 Biologie du Fruit, 71 Avenue Edouard Bourlaux, F–33883 Villenave d'Ornon, France.

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: Anna Amtmann (a.amtmann{at}bio.gla.ac.uk).

[W] The online version of this article contains Web-only data.

[OA] Open Access articles can be viewed online without a subscription.

www.plantphysiol.org/cgi/doi/10.1104/pp.108.133629

* Corresponding author; e-mail a.amtmann{at}bio.gla.ac.uk.

Received December 3, 2008; accepted March 23, 2009; published April 3, 2009.




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