Plant Cell Advance Online Publication
Published on March 28, 2003; 10.1105/tpc.009464
Received November 22, 2002
Accepted February 21, 2003
Leaf Mitochondria Modulate Whole Cell Redox Homeostasis, Set Antioxidant Capacity,
and Determine Stress Resistance through Altered Signaling and Diurnal Regulation
Christelle Dutilleul 1, Marie Garmier 1, Graham Noctor 2, Chantal Mathieu 1, Philippe Chétrit 1, Christine H. Foyer 2, and Rosine de Paepe 1*
1
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
2
Crop Performance and Improvement Division, Rothamsted Research, Harpenden, Hertfordshire
AL52JQ, United Kingdom
* To whom correspondence should be addressed. E-mail: depaepe{at}ibp.u-psud.fr.
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 H
2O2 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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G. Noctor, C. Dutilleul, R. De Paepe, and C. H. Foyer
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O. Chew, J. Whelan, and A. H. Millar
Molecular Definition of the Ascorbate-Glutathione Cycle in Arabidopsis Mitochondria Reveals Dual Targeting of Antioxidant Defenses in Plants
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