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J. Biol. Chem., Vol. 282, Issue 40, 29482-29492, October 5, 2007

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Toc159- and Toc75-independent Import of a Transit Sequence-less Precursor into the Inner Envelope of Chloroplasts^*

Stéphane Miras¹, Daniel Salvi¹, Laurie Piette, Daphné Seigneurin-Berny, Didier Grunwald, Christiane Reinbothe^¶, Jacques Joyard, Steffen Reinbothe^¶, and Norbert Rolland²

From the Laboratoire de Physiologie Cellulaire Végétale, CNRS Unité Mixte de Recherche (UMR) (5168), Commissariat à l'Energie Atomique (CEA), Institut National de la Recherche Agronomique (UMR 1200), Université Joseph Fourier, Institut de Recherches en Technologies et Sciences pour le Vivant (iRTSV), CEA-Grenoble, 17 rue des Martyrs, Grenoble 38054 cedex 9, France, the Laboratoire Canaux Calciques Fonctions et Pathologies, INSERM (U-607), CEA, Université Joseph Fourier, iRTSV, CEA-Grenoble, Grenoble 38054 Cedex 9, France, and the ^¶Laboratoire Plastes et Différenciation Cellulaire, CNRS (UMR 5575), Université Joseph Fourier, Centre d'Etudes et de Recherches sur les Macromolécules Organiques (CERMO), Grenoble 38041 Cedex 9, France

Chloroplast envelope quinone oxidoreductase (ceQORH) is an inner plastid envelope protein that is synthesized without cleavable chloroplast transit sequence for import. In the present work, we studied the in vitro-import characteristics of Arabidopsis ceQORH. We demonstrate that ceQORH import requires ATP and is dependent on proteinaceous receptor components exposed at the outer plastid surface. Competition experiments using small subunit precursor of ribulose-bisphosphate carboxylase/oxygenase and precursor of ferredoxin, as well as antibody blocking experiments, revealed that ceQORH import does not involve the main receptor and translocation channel proteins Toc159 and Toc75, respectively, which operate in import of proteins into the chloroplast. Molecular dissection of the ceQORH amino acid sequence by site-directed mutagenesis and subsequent import experiments in planta and in vitro highlighted that ceQORH consists of different domains that act concertedly in regulating import. Collectively, our results provide unprecedented evidence for the existence of a specific import pathway for transit sequence-less inner plastid envelope membrane proteins into chloroplasts.

Received for publication, December 4, 2006 , and in revised form, July 17, 2007.

^* This work was supported by CNRS and Commissariat à l'Energie Atomique 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 text, Figs. S1–S4, and references.

¹ Both authors contributed equally to this work.

² To whom correspondence should be addressed: Tel.: 33-4-38-78-49-86; Fax: 33-4-38-78-50-91; E-mail: norbert.rolland{at}cea.fr.

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