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J. Biol. Chem., Vol. 278, Issue 47, 46869-46877, November 21, 2003

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Molecular Definition of the Ascorbate-Glutathione Cycle in Arabidopsis Mitochondria Reveals Dual Targeting of Antioxidant Defenses in Plants^*

Orinda Chew, James Whelan, and A. Harvey Millar¶

From the Plant Molecular Biology Group, School of Biomedical and Chemical Sciences, The University of Western Australia, Crawley 6009, Western Australia, Australia

Key components of the ascorbate-glutathione cycle in Arabidopsis cell organelles are encoded by single organellar targeted isoforms that are dual localized in the chloroplast stroma and the mitochondrion. We demonstrate the presence of the ascorbate-glutathione cycle in purified Arabidopsis mitochondria using enzymatic activity, proteomic and in vitro and in vivo subcellular targeting data that identify the gene products responsible. In vitro experiments using a dual import assay assessing mitochondrial and chloroplast imports simultaneously show dual targeting of ascorbate peroxidase, monodehydroascorbate reductase, and glutathione reductase gene products to mitochondria and chloroplasts, while a putative dehydroascorbate reductase protein is only imported into mitochondria. In vivo subcellular localization using green fluorescent protein fusion proteins show clear targeting of all gene products to mitochondria. Transcript levels show these genes are induced by oxidative chemical stresses targeted to chloroplasts and/or mitochondria and are elevated during photosynthetic operation in the light. Together these data present a model of an integrated ascorbate-glutathione antioxidant defense common to plastids and mitochondria that is linked at the level of the genome in Arabidopsis.

Received for publication, July 14, 2003 , and in revised form, September 2, 2003.

^* 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 Supplementary Materials.

Recipient of an Australian Postgraduate Award.

Recipient of funding from the Australian Research Council Discovery Program.

^¶ An ARC QEII Research Fellow and recipient of funding from the Australian Research Council Discovery Program. To whom correspondence should be addressed: Biochemistry & Molecular Biology, School of Biomedical & Chemical Sciences, Faculty of Life & Physical Sciences, The University of Western Australia, Crawley 6009, WA, Australia. Tel.: 61-8-93807245; Fax: 61-8-93801148; E-mail: hmillar{at}cyllene.uwa.edu.au.

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