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J. Biol. Chem., Vol. 279, Issue 38, 39471-39478, September 17, 2004

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Changes in the Mitochondrial Proteome during the Anoxia to Air Transition in Rice Focus around Cytochrome-containing Respiratory Complexes^*

A. Harvey Millar, Alice E. Trend, and Joshua L. Heazlewood

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

The ability of rice seedlings to grow from dry seed under anoxia provides a rare opportunity in a multicellular eukaryote to study the stages of mitochondrial biogenesis triggered by oxygen availability. The function and proteome of rice mitochondria synthesized under 6 days of anoxia following 1 day of air adaptation have been compared with mitochondria isolated from 7-day aerobically grown rice seedlings. Rice coleoptiles grown under anoxia, and the mitochondria isolated from them respired very slowly compared with air-adapted and air-grown seedlings. Immunodetection of key mitochondrial protein markers, isoelectric focusing electrophoresis followed by SDS-PAGE to make soluble mitochondria proteome maps, and shotgun sequencing of mitochondrial proteins by liquid chromatography-tandem mass spectrometry all revealed similar patterns of the major function categories of mitochondrial proteins from both anoxic and air-adapted samples. Activity analysis showed respiratory oxidases markedly increased in activity during the air adaptation of seedlings. Blue-native electrophoresis followed by SDS-PAGE of mitochondrial membrane proteins clearly showed the very low abundance of assembled b/c complex and cytochrome c₁ oxidase complex in the mitochondrial membrane in anoxic samples and the dramatic increase in the abundance of these complexes on air adaptation. Total heme content, cytochrome absorbance spectra, and the electron carrier, cytochrome c, also increased markedly on air adaptation. These results likely reflect limited heme synthesis for cytochrome assembly in the absence of oxygen and represent a discrete and reversible blockage of full mitochondrial biogenesis in this anoxia-tolerant species.

Received for publication, June 1, 2004 , and in revised form, July 7, 2004.

^* This work was supported by grants from the Australian Research Council through the Discovery Program. 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.

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

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