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First published online March 28, 2003; 10.1105/tpc.009464

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The Plant Cell, Vol. 15, 1212-1226, May 2003, Copyright © 2003,
American Society of Plant Biologists

Leaf Mitochondria Modulate Whole Cell Redox Homeostasis, Set Antioxidant Capacity, and Determine Stress Resistance through Altered Signaling and Diurnal Regulation

Christelle Dutilleul1,a, Marie Garmier1,a, Graham Noctor2,b, Chantal Mathieua, Philippe Chétrita, Christine H. Foyerb and Rosine de Paepe3,a

a Institut de Biotechnologie des Plantes, Laboratoire Mitochondries et Métabolisme, Centre National de la Recherche Scientifique Unité Mixte de Recherche 8618, Université Paris-Sud XI, Orsay 91405, France
b Crop Performance and Improvement Division, Rothamsted Research, Harpenden, Hertfordshire AL52JQ, United Kingdom

3 To whom correspondence should be addressed. E-mail depaepe{at}ibp.u-psud.fr; fax 33-169153425

To explore the role of plant mitochondria in the regulation of cellular redox homeostasis and stress resistance, we exploited a Nicotiana sylvestris mitochondrial mutant. The cytoplasmic male-sterile mutant (CMSII) is impaired in complex I function and displays enhanced nonphosphorylating rotenone-insensitive [NAD(P)H dehydrogenases] and cyanide-insensitive (alternative oxidase) respiration. Loss of complex I function is not associated with increased oxidative stress, as shown by decreased leaf H2O2 and the maintenance of glutathione and ascorbate content and redox state. However, the expression and activity of several antioxidant enzymes are modified in CMSII. In particular, diurnal patterns of alternative oxidase expression are lost, the relative importance of the different catalase isoforms is modified, and the transcripts, protein, and activity of cytosolic ascorbate peroxidase are enhanced markedly. Thus, loss of complex I function reveals effective antioxidant crosstalk and acclimation between the mitochondria and other organelles to maintain whole cell redox balance. This reorchestration of the cellular antioxidative system is associated with higher tolerance to ozone and Tobacco mosaic virus.




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