Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signaling and diurnal regulation.
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(2)O(2) 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.
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.
Christelle
C
Dutilleul
Marie
M
Garmier
Graham
G
Noctor
Chantal
C
Mathieu
Philippe
P
Chétrit
Christine H
CH
Foyer
Rosine
R
de Paepe
D000222:Adaptation, Physiological / Q000502:physiology; D000975:Antioxidants / Q000378:metabolism*; D060387:Ascorbate Peroxidases; D019069:Cell Respiration / Q000187:drug effects; D002940:Circadian Rhythm / Q000502:physiology; D003486:Cyanides / Q000494:pharmacology; D005298:Fertility / Q000235:genetics; D018506:Gene Expression Regulation, Plant; D006706:Homeostasis; D006861:Hydrogen Peroxide / Q000378:metabolism; D008928:Mitochondria / Q000235:genetics / Q000378:metabolism*; D024101:Mitochondrial Proteins; D009154:Mutation; D009252:NADPH Dehydrogenase / Q000235:genetics / Q000378:metabolism; D010084:Oxidation-Reduction; D010088:Oxidoreductases / Q000235:genetics / Q000378:metabolism; D010544:Peroxidases / Q000235:genetics / Q000378:metabolism; D018515:Plant Leaves / Q000235:genetics / Q000502:physiology*; D010940:Plant Proteins; D012402:Rotenone / Q000494:pharmacology; D015398:Signal Transduction / Q000502:physiology*; D014026:Nicotiana / Q000235:genetics / Q000502:physiology; D000099188:Alternative Oxidase
D000975:Antioxidants; D060387:Ascorbate Peroxidases; D003486:Cyanides; D006861:Hydrogen Peroxide; D024101:Mitochondrial Proteins; D009252:NADPH Dehydrogenase; D010088:Oxidoreductases; D010544:Peroxidases; D010940:Plant Proteins; D012402:Rotenone; D000099188:Alternative Oxidase