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Published on August 18, 2006; 10.1104/pp.106.086652

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Received July 12, 2006
Accepted August 9, 2006

A cytosolic Arabidopsis thaliana D-xylulose kinase catalyzes the phosphorylation of 1-deoxy-D-xylulose into a precursor of the plastidial isoprenoid pathway

Andréa Hemmerlin *, Denis Tritsch , Michael Hartmann , Karine Pacaud , Jean-François Hoeffler , Alain van Dorsselaer , Michel Rohmer , and Thomas J. Bach

Centre National de la Recherche Scientifique, UPR 2357, Institut de Biologie Moléculaire des Plantes, 28 rue Goethe, 67083 Strasbourg cedex, France
Université Louis Pasteur / CNRS, Institut de Chimie de Strasbourg, LC3-UMR 7177, 4 rue Blaise Pascal, 67070 Strasbourg Cedex, France
Université Louis Pasteur / CNRS, Laboratoire de Spectrométrie de Masse Bio-Organique, Institut Pluridisciplinaire Hubert Curien, LC4-UMR 7178, ECPM, 25 rue Becquerel F-67087 Strasbourg cedex , France
AlsaChim, ISIS, 8 allée Gaspard Monge, 67000 Strasbourg, France

* Corresponding author; email: andrea.hemmerlin{at}ibmp-ulp.u-strasbg.fr.

Plants are able to integrate exogenous 1-deoxy-D-xylulose into the 2C-methyl-D-erythritol 4-phosphate pathway, implicated in the biosynthesis of plastidial isoprenoids. Thus, the carbohydrate needs to be phosphorylated into 1-deoxy-D-xylulose 5-phosphate, and translocated into plastids, or vice versa. An enzyme capable of phosphorylating 1-deoxy-D-xylulose was partially purified from a cell-free Arabidopsis thaliana protein extract. It was identified by mass-spectrometry as a cytosolic protein bearing D-xylulose kinase signatures, already suggesting that 1-deoxy-D-xylulose is phosphorylated within the cytosol prior to translocation into the plastids. The corresponding cDNA was isolated and enzymatic properties of a recombinant protein were determined. In Arabidopsis, xylulose kinases are encoded by a small gene family, in which only two genes are putatively annotated. The additional gene is coding for a protein targeted to plastids, as was proved by co-localization experiments using GFP fusion proteins. Functional complementation assays in an E. coli strain deleted in D-xylulose kinase revealed that exclusively the cytosolic enzyme could phosphorylate xylulose in vivo, and not the enzyme that is targeted to plastids. D-xylulose kinase activities could not be detected in chloroplast protein extracts, nor in proteins isolated from its ancestral relative Synechocystis sp. PCC 6803. The gene encoding the plastidic protein annotated as "xylulose kinase" might in fact yield an enzyme having different phosphorylation specificities. The biochemical characterization and complementation experiments with 1-deoxy-D-xylulose of specific Arabidopsis knock-out mutants seedlings treated with oxo-clomazone, an inhibitor of 1-deoxy-D-xylulose 5-phosphate synthase, further confirmed that the cytosolic protein is responsible for the phosphorylation of 1-deoxy-D-xylulose in planta.




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