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BIOENERGETICS AND PHOTOSYNTHESIS

Complex I Dysfunction Redirects Cellular and Mitochondrial Metabolism in Arabidopsis^1,[W],[OA]

Australian Research Council Centre of Excellence in Plant Energy Biology M316 (M.G., A.J.C., E.D., C.V., I.D.S., A.H.M.) and School of Biomedical, Biomolecular, and Chemical Sciences M310 (A.J.C.), University of Western Australia, Crawley, Western Australia 6009, Australia; and Australian Research Council Centre of Excellence in Plant Energy Biology, School of Biological Sciences, University of Sydney, New South Wales 2006, Australia (D.A.D.)

Mitochondrial complex I is a major avenue for reduced NAD oxidation linked to oxidative phosphorylation in plants. However, the plant enzyme has structural and functional features that set it apart from its counterparts in other organisms, raising questions about the physiological significance of this complex in plants. We have developed an experimental model in which rotenone, a classic complex I inhibitor, has been applied to Arabidopsis (Arabidopsis thaliana) cell suspension cultures in order to dissect early metabolic adjustments involved in cell acclimation to mitochondrial dysfunction. Rotenone induced a transitory decrease in cellular respiration (0–4 h after treatment). Cell respiration then progressively recovered and reached a steady state at 10 to 12 h after treatment. Complex I inhibition by rotenone did not induce obvious oxidative stress or cell death but affected longer term cell growth. Integrated analyses of gene expression, the mitochondrial proteome, and changes in primary metabolism indicated that rotenone treatment caused changes in mitochondrial function via alterations in specific components. A physical disengagement of glycolytic activities associated with the mitochondrial outer membrane was observed, and the tricarboxylic acid cycle was altered. Amino acid and organic acid pools were also modified by rotenone treatment, with a marked early decrease of 2-oxoglutarate, aspartate, and glutamine pools. These data demonstrate that, in Arabidopsis cells, complex I inhibition by rotenone induces significant remodeling of metabolic pathways involving the mitochondria and other compartments and point to early metabolic changes in response to mitochondrial dysfunction.

² Present address: Institut de Biotechnologie des Plantes, Université Paris-Sud 11, CNRS, UMR 8618, Bâtiment 630, 91405 Orsay cedex, France.

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: A. Harvey Millar (hmillar{at}cyllene.uwa.edu.au).

^[W] The online version of this article contains Web-only data.

^[OA] Open Access articles can be viewed online without a subscription.

www.plantphysiol.org/cgi/doi/10.1104/pp.108.125880

^* Corresponding author; e-mail hmillar{at}cyllene.uwa.edu.au.

Received July 5, 2008; accepted September 5, 2008; published September 10, 2008.