First published online April 9, 2002; 10.1104/pp.010999
Plant Physiol, April 2002, Vol. 128, pp. 1271-1281
Oxidative Stress Increased Respiration and Generation of Reactive
Oxygen Species, Resulting in ATP Depletion, Opening of Mitochondrial
Permeability Transition, and Programmed Cell Death1
Budhi Sagar
Tiwari,
Beatrice
Belenghi, and
Alex
Levine*
Department of Plant Sciences, Silberman Institute of Life Sciences,
The Hebrew University of Jerusalem, Givat-Ram, Jerusalem 91904, Israel
Mitochondria constitute a major source of reactive oxygen
species and have been proposed to integrate the cellular responses to
stress. In animals, it was shown that mitochondria can trigger apoptosis from diverse stimuli through the opening of MTP, which allows
the release of the apoptosis-inducing factor and translocation of
cytochrome c into the cytosol. Here, we analyzed the
role of the mitochondria in the generation of oxidative burst and
induction of programmed cell death in response to brief or continuous
oxidative stress in Arabidopsis cells. Oxidative stress increased
mitochondrial electron transport, resulting in amplification of
H2O2 production, depletion of ATP, and cell
death. The increased generation of H2O2 also
caused the opening of the MTP and the release of cytochrome c from mitochondria. The release of cytochrome
c and cell death were prevented by a serine/cysteine
protease inhibitor, Pefablock. However, addition of inhibitor only
partially inhibited the H2O2 amplification and
the MTP opening, suggesting that protease activation is a necessary
step in the cell death pathway after mitochondrial damage.
1
This work was supported by the Israel Science Foundation.
*
Corresponding author; e-mail alexlevine{at}huji.ac.il; fax
972-2-658-4425.
© 2002 American Society of Plant Physiologists
This article has been cited by other articles:

|
 |

|
 |
 
T. Ishikawa, K. Takahara, T. Hirabayashi, H. Matsumura, S. Fujisawa, R. Terauchi, H. Uchimiya, and M. Kawai-Yamada
Metabolome Analysis of Response to Oxidative Stress in Rice Suspension Cells Overexpressing Cell Death Suppressor Bax Inhibitor-1
Plant Cell Physiol.,
January 1, 2010;
51(1):
9 - 20.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. H.M. Schippers, A. Nunes-Nesi, R. Apetrei, J. Hille, A. R. Fernie, and P. P. Dijkwel
The Arabidopsis onset of leaf death5 Mutation of Quinolinate Synthase Affects Nicotinamide Adenine Dinucleotide Biosynthesis and Causes Early Ageing
PLANT CELL,
October 1, 2008;
20(10):
2909 - 2925.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
X.-Y. Wan and J.-Y. Liu
Comparative Proteomics Analysis Reveals an Intimate Protein Network Provoked by Hydrogen Peroxide Stress in Rice Seedling Leaves
Mol. Cell. Proteomics,
August 1, 2008;
7(8):
1469 - 1488.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. K. Azad, T. Ishikawa, T. Ishikawa, Y. Sawa, and H. Shibata
Intracellular energy depletion triggers programmed cell death during petal senescence in tulip
J. Exp. Bot.,
May 31, 2008;
(2008)
ern066v1.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E.-J. Kim, J.-S. Kim, I.-H. Lee, H. J. Rhee, and J. K. Lee
Superoxide Generation by Chlorophyllide a Reductase of Rhodobacter sphaeroides
J. Biol. Chem.,
February 15, 2008;
283(7):
3718 - 3730.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
I. I. Boubriak, D. M. Grodzinsky, V. P. Polischuk, V. D. Naumenko, N. P. Gushcha, A. N. Micheev, S. J. McCready, and D. J. Osborne
Adaptation and Impairment of DNA Repair Function in Pollen of Betula verrucosa and Seeds of Oenothera biennis from Differently Radionuclide-contaminated Sites of Chernobyl
Ann. Bot.,
January 1, 2008;
101(2):
267 - 276.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. Weinberger
Pathogen-Induced Defense and Innate Immunity in Macroalgae
Biol. Bull.,
December 1, 2007;
213(3):
290 - 302.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Morimoto, Y. Tanaka, K. Sasaki, H. Tanaka, T. Fukamizu, Y. Shoyama, Y. Shoyama, and F. Taura
Identification and Characterization of Cannabinoids That Induce Cell Death through Mitochondrial Permeability Transition in Cannabis Leaf Cells
J. Biol. Chem.,
July 13, 2007;
282(28):
20739 - 20751.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. J. Baxter, H. Redestig, N. Schauer, D. Repsilber, K. R. Patil, J. Nielsen, J. Selbig, J. Liu, A. R. Fernie, and L. J. Sweetlove
The Metabolic Response of Heterotrophic Arabidopsis Cells to Oxidative Stress
Plant Physiology,
January 1, 2007;
143(1):
312 - 325.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. M. Rhoads, A. L. Umbach, C. C. Subbaiah, and J. N. Siedow
Mitochondrial Reactive Oxygen Species. Contribution to Oxidative Stress and Interorganellar Signaling
Plant Physiology,
June 1, 2006;
141(2):
357 - 366.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. Van Breusegem and J. F. Dat
Reactive Oxygen Species in Plant Cell Death
Plant Physiology,
June 1, 2006;
141(2):
384 - 390.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. A. Vacca, D. Valenti, A. Bobba, R. S. Merafina, S. Passarella, and E. Marra
Cytochrome c Is Released in a Reactive Oxygen Species-Dependent Manner and Is Degraded via Caspase-Like Proteases in Tobacco Bright-Yellow 2 Cells en Route to Heat Shock-Induced Cell Death
Plant Physiology,
May 1, 2006;
141(1):
208 - 219.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. A. J. Mur, T. L. W. Carver, and E. Prats
NO way to live; the various roles of nitric oxide in plant-pathogen interactions
J. Exp. Bot.,
February 1, 2006;
57(3):
489 - 505.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F.-Q. Guo and N. M. Crawford
Arabidopsis Nitric Oxide Synthase1 Is Targeted to Mitochondria and Protects against Oxidative Damage and Dark-Induced Senescence
PLANT CELL,
December 1, 2005;
17(12):
3436 - 3450.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. YOSHINAGA, S.-I. ARIMURA, Y. NIWA, N. TSUTSUMI, H. UCHIMIYA, and M. KAWAI-YAMADA
Mitochondrial Behaviour in the Early Stages of ROS Stress Leading to Cell Death in Arabidopsis thaliana
Ann. Bot.,
August 1, 2005;
96(2):
337 - 342.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. G. Bartoli, F. Gomez, G. Gergoff, J. J. Guiamet, and S. Puntarulo
Up-regulation of the mitochondrial alternative oxidase pathway enhances photosynthetic electron transport under drought conditions
J. Exp. Bot.,
May 1, 2005;
56(415):
1269 - 1276.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
V. Casolo, E. Petrussa, J. Krajnakova, F. Macri, and A. Vianello
Involvement of the mitochondrial KATP+ channel in H2O2- or NO-induced programmed death of soybean suspension cell cultures
J. Exp. Bot.,
March 1, 2005;
56(413):
997 - 1006.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. W. Yang, S. K. Kim, and W. T. Kim
Perturbation of NgTRF1 Expression Induces Apoptosis-Like Cell Death in Tobacco BY-2 Cells and Implicates NgTRF1 in the Control of Telomere Length and Stability
PLANT CELL,
December 1, 2004;
16(12):
3370 - 3385.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Deuschle, D. Funck, G. Forlani, H. Stransky, A. Biehl, D. Leister, E. van der Graaff, R. Kunze, and W. B. Frommer
The Role of {Delta}1-Pyrroline-5-Carboxylate Dehydrogenase in Proline Degradation
PLANT CELL,
December 1, 2004;
16(12):
3413 - 3425.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. G. Bartoli, F. Gomez, D. E. Martinez, and J. J. Guiamet
Mitochondria are the main target for oxidative damage in leaves of wheat (Triticum aestivum L.)
J. Exp. Bot.,
August 1, 2004;
55(403):
1663 - 1669.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. Belenghi, M. Salomon, and A. Levine
Caspase-like activity in the seedlings of Pisum sativum eliminates weaker shoots during early vegetative development by induction of cell death
J. Exp. Bot.,
April 1, 2004;
55(398):
889 - 897.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Rea, M. C. de Pinto, R. Tavazza, S. Biondi, V. Gobbi, P. Ferrante, L. De Gara, R. Federico, R. Angelini, and P. Tavladoraki
Ectopic Expression of Maize Polyamine Oxidase and Pea Copper Amine Oxidase in the Cell Wall of Tobacco Plants
Plant Physiology,
April 1, 2004;
134(4):
1414 - 1426.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. A. Vacca, M. C. de Pinto, D. Valenti, S. Passarella, E. Marra, and L. De Gara
Production of Reactive Oxygen Species, Alteration of Cytosolic Ascorbate Peroxidase, and Impairment of Mitochondrial Metabolism Are Early Events in Heat Shock-Induced Programmed Cell Death in Tobacco Bright-Yellow 2 Cells
Plant Physiology,
March 1, 2004;
134(3):
1100 - 1112.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Kawai-Yamada, Y. Ohori, and H. Uchimiya
Dissection of Arabidopsis Bax Inhibitor-1 Suppressing Bax-, Hydrogen Peroxide-, and Salicylic Acid-Induced Cell Death
PLANT CELL,
January 1, 2004;
16(1):
21 - 32.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Mazel, Y. Leshem, B. S. Tiwari, and A. Levine
Induction of Salt and Osmotic Stress Tolerance by Overexpression of an Intracellular Vesicle Trafficking Protein AtRab7 (AtRabG3e)
Plant Physiology,
January 1, 2004;
134(1):
118 - 128.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Takahashi, T. Kawasaki, H. L. Wong, U. Suharsono, H. Hirano, and K. Shimamoto
Hyperphosphorylation of a Mitochondrial Protein, Prohibitin, Is Induced by Calyculin A in a Rice Lesion-Mimic Mutant cdr1
Plant Physiology,
August 1, 2003;
132(4):
1861 - 1869.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. VIROLAINEN, O. BLOKHINA, and K. FAGERSTEDT
Ca2+-induced High Amplitude Swelling and Cytochrome c Release From Wheat (Triticum aestivum L.) Mitochondria Under Anoxic Stress
Ann. Bot.,
October 1, 2002;
90(4):
509 - 516.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|
|