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J. Biol. Chem., Vol. 281, Issue 5, 2882-2892, February 3, 2006

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HMA1, a New Cu-ATPase of the Chloro plast Envelope, Is Essential for Growth under Adverse Light Conditions^*

Daphné Seigneurin-Berny¹², Antoine Gravot¹, Pascaline Auroy, Christophe Mazard, Alexandra Kraut, Giovanni Finazzi^¶, Didier Grunwald^||, Fabrice Rappaport^¶, Alain Vavasseur, Jacques Joyard, Pierre Richaud, and Norbert Rolland³

From the Laboratoire de Physiologie Cellulaire Végétale, Unité Mixte de Recherche (UMR) 5168 CNRS/CEA/Institut National de la Recherche Agronomique, Université Joseph Fourier, Département Réponse et Dynamique Cellulaires (DRDC)/CEA-Grenoble, 17 rue des Martyrs, 38054 Grenoble-cedex 9, France, the Laboratoire des Echanges Membranaires et Signalisation, UMR 6191 CNRS/CEA/Université Aix-Marseille II, Département d'Ecophysiologie Végétale et de Microbiologie/CEA Cadarache, 13108 St Paul les Durance Cedex, France, the ^¶Institut de Biologie Physico-Chimique, UMR 7141 CNRS/Université Paris 6, 13 rue P. et M. Curie, 75005 Paris, France, and the ^||Laboratoire Canaux Ioniques, Fonctions et Pathologies, EMI 9931 CEA/INSERM/Université Joseph Fourier, DRDC/CEA-Grenoble, 17 rue des Martyrs, 38054 Grenoble-cedex 9, France

Although ions play important roles in the cell and chloroplast metabolism, little is known about ion transport across the chloroplast envelope. Using a proteomic approach specifically targeted to the Arabidopsis chloroplast envelope, we have identified HMA1, which belongs to the metal-transporting P_1B-type ATPases family. HMA1 is mainly expressed in green tissues, and we validated its chloroplast envelope localization. Yeast expression experiments demonstrated that HMA1 is involved in copper homeostasis and that deletion of its N-terminal His-domain partially affects the metal transport. Characterization of hma1 Arabidopsis mutants revealed a lower chloroplast copper content and a diminution of the total chloroplast superoxide dismutase activity. No effect was observed on the plastocyanin content in these lines. The hma1 insertional mutants grew like WT plants in standard condition but presented a photosensitivity phenotype under high light. Finally, direct biochemical ATPase assays performed on purified chloroplast envelope membranes showed that the ATPase activity of HMA1 is specifically stimulated by copper. Our results demonstrate that HMA1 offers an additional way to the previously characterized chloroplast envelope Cu-ATPase PAA1 to import copper in the chloroplast.

Received for publication, July 29, 2005 , and in revised form, October 26, 2005.

The nucleotide sequence(s) reported in this paper has been submitted to the GenBank^TM/EBI Data Bank with accession number(s) AY907350 [GenBank] .

^* This work was supported by CNRS and CEA (Toxicologie Nucléaire Environnementale) research programs. 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 Figs. S1-S3

¹ Both authors contributed equally to this work.

² To whom correspondence may be addressed. Tel.: 33-4-3878-4986; Fax: 33-4-3878-5091; E-mail: daphne.berny{at}cea.fr.

³ To whom correspondence may be addressed. Tel.: 33-4-3878-4986; Fax: 33-4-3878-5091; E-mail: nrolland{at}cea.fr.

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