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Published on September 10, 2008; 10.1104/pp.108.125880

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Received July 5, 2008
Accepted September 5, 2008

Complex I dysfunction redirects cellular and mitochondrial metabolism in Arabidopsis

Marie Garmier , Adam J. Carroll , Etienne Delannoy , Corinne Vallet , David. A Day , Ian D. Small , and A. Harvey Millar *

ARC Centre of Excellence in Plant Energy Biology, M316; School of Biomedical, Biomolecular and Chemical Sciences M310, University of Western Australia, 35 Stirling Highway, Crawley, 6009, WA, Australia; ARC Centre of Excellence in Plant Energy Biology, School of Biological Sciences, University of Sydney, 2006, NSW, Australia

* Corresponding author; email: hmillar{at}cyllene.uwa.edu.au.

Mitochondrial complex I is a major avenue for NADH 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 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 10-12 h after treatment. Complex I inhibition by rotenone did not induce obvious oxidative stress or cell death but impacted on 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 TCA 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 remodelling of metabolic pathways involving the mitochondria and other compartments, and point to early metabolic changes in response to mitochondrial dysfunction.




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