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

Abstract

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 .

Suppression of tobacco mosaic virus-induced hypersensitive-type necrotization in tobacco at high temperature is associated with downregulation of NADPH oxidase and superoxide and stimulation of dehydroascorbate reductase

“…Thereby, AOX was shown to contribute to a slight (15 %) restriction of the size of necrotized viral lesions during TMV-induced HR-type cell death in tobacco (Ordog et al, 2002). Nicotiana sylvestris mitochondrial mutants with elevated levels of AOX protein and altered expression of antioxidant enzymes also display reduced number and size of lesions following TMV inoculation compared with control plants (Dutilleul et al, 2003). On the other hand, use of a TMV vector to produce extremely high levels of wild-type or mutant AOX protein in tobacco resulted in larger HR lesions than those produced by the empty TMV vector (Murphy et al, 2004).…”

Transcript, protein and metabolite temporal dynamics in the CAM plant Agave

“…1c). Interestingly, the diel pattern of daytime depletion and nocturnal accumulation of ascorbic acid in Agave contrasts markedly with that in Arabidopsis and other C 3 species 17,18 .…”

“…1c). Interestingly, the diel pattern of daytime depletion and nocturnal accumulation of ascorbic acid in Agave contrasts markedly with that in Arabidopsis and other C 3 species 17,18 .The reprogramming of the day/night pattern of ascorbic acid turnover in Agave is intriguing if ascorbic acid is a key component of a redox hub that integrates metabolic information and environmental stimuli to tune responses within the cellular signalling network 19 . Recent studies have shown that many organisms, including Arabidopsis, have a redox rhythm that is dictated by circadian clock components and metabolic activities such as the production and scavenging of reactive oxygen species (ROS) [20][21][22] .…”

Genomics-based dissection of the cross-talk of chloroplasts with the nucleus and mitochondria in Arabidopsis

“…In the tobacco CMSII mutant, which lacks the major mitochondrial NADH dehydrogenase (Complex I), the rate of photosynthesis is decreased, notably during dark -light transitions or when carbon fixation and photorespiration are simultaneously active (Sabar et al, 2000;Dutilleul et al, 2003a). In the same mutant, modulation of nuclear gene expression maintains whole cell redox balance (Dutilleul et al, 2003b). The analysis of the prors1 mutant of Arabidopsis, defective in an organelle-targeted tRNA synthetase, shows that nuclear photosynthetic genes are specifically down-regulated (P. Pesaresi and D. Leister, unpublished results), indicating that mitochondrion -chloroplast crosstalk might involve re-programming of the expression of nuclear chloroplast genes.…”