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J. Biol. Chem., Vol. 282, Issue 12, 8848-8859, March 23, 2007

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Identification, Expression, and Functional Analyses of a Thylakoid ATP/ADP Carrier from Arabidopsis^*

Sophie Thuswaldner, Jens O. Lagerstedt¹², Marc Rojas-Stütz^¶1, Karim Bouhidel^||, Christophe Der^||, Nathalie Leborgne-Castel^||, Arti Mishra, Francis Marty^||, Benoît Schoefs^||, Iwona Adamska^¶, Bengt L. Persson, and Cornelia Spetea³

From the Division of Cell Biology and Department of Physics, Chemistry and Biology, Linköping University, SE-581 85 Linköping, Sweden, Department of Chemistry and Biomedical Sciences, Kalmar University, SE-391 82 Kalmar, Sweden, ^¶Department of Physiology and Plant Biochemistry, University of Konstanz, D-78457 Konstanz, Germany, and ^||UMR Plante-Microbe-Environnement CNRS 5184/Institut National de la Recherche Agronomique1088, Université de Bourgogne, BP 47870, F-21078 Dijon Cedex, France

In plants the chloroplast thylakoid membrane is the site of light-dependent photosynthetic reactions coupled to ATP synthesis. The ability of the plant cell to build and alter this membrane system is essential for efficient photosynthesis. A nucleotide translocator homologous to the bovine mitochondrial ADP/ATP carrier (AAC) was previously found in spinach thylakoids. Here we have identified and characterized a thylakoid ATP/ADP carrier (TAAC) from Arabidopsis.(i) Sequence homology with the bovine AAC and the prediction of chloroplast transit peptides indicated a putative carrier encoded by the At5g01500 gene, as a TAAC. (ii) Transiently expressed TAAC-green fluorescent protein fusion construct was targeted to the chloroplast. Western blotting using a peptide-specific antibody together with immunogold electron microscopy revealed a major location of TAAC in the thylakoid membrane. Previous proteomic analyses identified this protein in chloroplast envelope preparations. (iii) Recombinant TAAC protein specifically imports ATP in exchange for ADP across the cytoplasmic membrane of Escherichia coli. Studies on isolated thylakoids from Arabidopsis confirmed these observations. (iv) The lack of TAAC in an Arabidopsis T-DNA insertion mutant caused a 30–40% reduction in the thylakoid ATP transport and metabolism. (v) TAAC is readily expressed in dark-grown Arabidopsis seedlings, and its level remains stable throughout the greening process. Its expression is highest in developing green tissues and in leaves undergoing senescence or abiotic stress. We propose that the TAAC protein supplies ATP for energy-dependent reactions during thylakoid biogenesis and turnover in plants.

Received for publication, September 26, 2006 , and in revised form, December 22, 2007.

^* This work was supported by the Swedish Research Council (to C. S. and B. L. P.), the Graduate Research School in Genomics and Bioinformatics and Hagberg Foundation (to C. S.), the Human Frontier Science Organization (to B. L. P.), Deutsche Forschungsgemeinschaft and Konstanz University (to I. A.), and the French Ministère de l'Education Nationale de l'Enseignement Supérieur et de la Recherche, the Institut National de la Recherche Agronomique, and the CNRS (Dijon group). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains supplemental material including Figs. S1–S4 and Table S1.

¹ These authors equally contributed to this work.

² Present address: Depts. of Biochemistry and Molecular Medicine, and Internal Medicine, University of California, School of Medicine, Davis, CA 95616.

³ To whom correspondence should be addressed. Tel.: 46-13-225788; Fax: 46-13-224314; E-mail: cornelia.spetea{at}ibk.liu.se.

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