Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Subscribe

Logo for

Plant Physiology 129 (4): 1908-1920

Copyright © 2002 by the American Society of Plant Physiologists.

Plant Physiol, August 2002, Vol. 129, pp. 1908-1920

Transgenic Plant Cells Lacking Mitochondrial Alternative Oxidase Have Increased Susceptibility to Mitochondria-Dependent and -Independent Pathways of Programmed Cell Death1

Christine A. Robson and Greg C. Vanlerberghe*

Division of Life Sciences and Department of Botany, University of Toronto at Scarborough, 1265 Military Trail, Scarborough, Ontario, Canada M1C 1A4

The plant mitochondrial electron transport chain is branched such that electrons at ubiquinol can be diverted to oxygen via the alternative oxidase (AOX). This pathway does not contribute to ATP synthesis but can dampen the mitochondrial generation of reactive oxygen species. Here, we establish that transgenic tobacco (Nicotiana tabacum L. cv Petit Havana SR1) cells lacking AOX (AS8 cells) show increased susceptibility to three different death-inducing compounds (H2O2, salicylic acid [SA], and the protein phosphatase inhibitor cantharidin) in comparison with wild-type cells. The timing and extent of AS8 cell death are very similar among the three treatments and, in each case, are accompanied by the accumulation of oligonucleosomal fragments of DNA, indicative of programmed cell death. Death induced by H2O2 or SA occurs by a mitochondria-dependent pathway characterized by cytochrome c release from the mitochondrion. Conversely, death induced by cantharidin occurs by a pathway without any obvious mitochondrial involvement. The ability of AOX to attenuate these death pathways may relate to its ability to maintain mitochondrial function after insult with a death-inducing compound or may relate to its ability to prevent chronic oxidative stress within the mitochondrion. In support of the latter, long-term treatment of AS8 cells with an antioxidant compound increased the resistance of AS8 cells to SA- or cantharidin-induced death. The results indicate that plants maintain both mitochondria-dependent and -independent pathways of programmed cell death and that AOX may act as an important mitochondrial "survival protein" against such death.


1 This work was supported by a grant from the Natural Sciences and Engineering Research Council of Canada and by a Premiers Research Excellence Award of Ontario (both to G.C.V.).

* Corresponding author; e-mail gregv{at}utsc.utoronto.ca; fax 416-287-7642.

© 2002 American Society of Plant Physiologists


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Mitochondrial Phosphatidylethanolamine Level Modulates Cyt c Oxidase Activity to Maintain Respiration Capacity in Arabidopsis thaliana Rosette Leaves.
M. Otsuru, Y. Yu, J. Mizoi, M. Kawamoto-Fujioka, J. Wang, Y. Fujiki, and I. Nishida (2013)
Plant Cell Physiol. 54, 1612-1619
   Abstract »    Full Text »    PDF »
Alternative Oxidase in Resistance to Biotic Stresses: Nicotiana attenuata AOX Contributes to Resistance to a Pathogen and a Piercing-Sucking Insect But Not Manduca sexta Larvae.
L. Zhang, Y. Oh, H. Li, I. T. Baldwin, and I. Galis (2012)
Plant Physiology 160, 1453-1467
   Abstract »    Full Text »    PDF »
Photosynthetic Performance and Fertility Are Repressed in GmAOX2b Antisense Soybean.
T.-T. Chai, D. Simmonds, D. A. Day, T. D. Colmer, and P. M. Finnegan (2010)
Plant Physiology 152, 1638-1649
   Abstract »    Full Text »    PDF »
Regulation of Plant Glycine Decarboxylase by S-Nitrosylation and Glutathionylation.
M. C. Palmieri, C. Lindermayr, H. Bauwe, C. Steinhauser, and J. Durner (2010)
Plant Physiology 152, 1514-1528
   Abstract »    Full Text »    PDF »
Defining the Mitochondrial Stress Response in Arabidopsis thaliana.
O. Van Aken, B. Zhang, C. Carrie, V. Uggalla, E. Paynter, E. Giraud, and J. Whelan (2009)
Mol Plant 2, 1310-1324
   Abstract »    Full Text »    PDF »
Alternative oxidase in animals: unique characteristics and taxonomic distribution.
A. E. McDonald, G. C. Vanlerberghe, and J. F. Staples (2009)
J. Exp. Biol. 212, 2627-2634
   Abstract »    Full Text »    PDF »
Decreased Expression of Cytosolic Pyruvate Kinase in Potato Tubers Leads to a Decline in Pyruvate Resulting in an in Vivo Repression of the Alternative Oxidase.
S. N. Oliver, J. E. Lunn, E. Urbanczyk-Wochniak, A. Lytovchenko, J. T. van Dongen, B. Faix, E. Schmalzlin, A. R. Fernie, and P. Geigenberger (2008)
Plant Physiology 148, 1640-1654
   Abstract »    Full Text »    PDF »
Identification of Regulatory Pathways Controlling Gene Expression of Stress-Responsive Mitochondrial Proteins in Arabidopsis.
L. H.M. Ho, E. Giraud, V. Uggalla, R. Lister, R. Clifton, A. Glen, D. Thirkettle-Watts, O. Van Aken, and J. Whelan (2008)
Plant Physiology 147, 1858-1873
   Abstract »    Full Text »    PDF »
The Absence of ALTERNATIVE OXIDASE1a in Arabidopsis Results in Acute Sensitivity to Combined Light and Drought Stress.
E. Giraud, L. H.M. Ho, R. Clifton, A. Carroll, G. Estavillo, Y.-F. Tan, K. A. Howell, A. Ivanova, B. J. Pogson, A. H. Millar, et al. (2008)
Plant Physiology 147, 595-610
   Abstract »    Full Text »    PDF »
Intracellular energy depletion triggers programmed cell death during petal senescence in tulip.
A. K. Azad, T. Ishikawa, T. Ishikawa, Y. Sawa, and H. Shibata (2008)
J. Exp. Bot.
   Abstract »    Full Text »    PDF »
Two Zinc-Cluster Transcription Factors Control Induction of Alternative Oxidase in Neurospora crassa.
M. S. Chae, C. E. Nargang, I. A. Cleary, C. C. Lin, A. T. Todd, and F. E. Nargang (2007)
Genetics 177, 1997-2006
   Abstract »    Full Text »    PDF »
Pichia pastoris 'just in time' alternative respiration.
A. Kern, F. S. Hartner, M. Freigassner, J. Spielhofer, C. Rumpf, L. Leitner, K.-U. Frohlich, and A. Glieder (2007)
Microbiology 153, 1250-1260
   Abstract »    Full Text »    PDF »
Lack of Respiratory Chain Complex I Impairs Alternative Oxidase Engagement and Modulates Redox Signaling during Elicitor-Induced Cell Death in Tobacco.
G. Vidal, M. Ribas-Carbo, M. Garmier, G. Dubertret, A. G. Rasmusson, C. Mathieu, C. H. Foyer, and R. De Paepe (2007)
PLANT CELL 19, 640-655
   Abstract »    Full Text »    PDF »
Possible plant mitochondria involvement in cell adaptation to drought stress: A case study: durum wheat mitochondria.
D. Pastore, D. Trono, M. N. Laus, N. Di Fonzo, and Z. Flagella (2007)
J. Exp. Bot. 58, 195-210
   Abstract »    Full Text »    PDF »
Modifications to the Arabidopsis Defense Proteome Occur Prior to Significant Transcriptional Change in Response to Inoculation with Pseudomonas syringae.
A. M.E. Jones, V. Thomas, M. H. Bennett, J. Mansfield, and M. Grant (2006)
Plant Physiology 142, 1603-1620
   Abstract »    Full Text »    PDF »
Changes in Plant Mitochondrial Electron Transport Alter Cellular Levels of Reactive Oxygen Species and Susceptibility to Cell Death Signaling Molecules.
S. Amirsadeghi, C. A. Robson, A. E. McDonald, and G. C. Vanlerberghe (2006)
Plant Cell Physiol. 47, 1509-1519
   Abstract »    Full Text »    PDF »
Mitochondrial Reactive Oxygen Species. Contribution to Oxidative Stress and Interorganellar Signaling.
D. M. Rhoads, A. L. Umbach, C. C. Subbaiah, and J. N. Siedow (2006)
Plant Physiology 141, 357-366
   Full Text »    PDF »
Reactive Oxygen Species in Plant Cell Death.
F. Van Breusegem and J. F. Dat (2006)
Plant Physiology 141, 384-390
   Full Text »    PDF »
Characterization of Mitochondrial Alternative NAD(P)H Dehydrogenases in Arabidopsis: Intraorganelle Location and Expression.
D. Elhafez, M. W. Murcha, R. Clifton, K. L. Soole, D. A. Day, and J. Whelan (2006)
Plant Cell Physiol. 47, 43-54
   Abstract »    Full Text »    PDF »
Arabidopsis Nitric Oxide Synthase1 Is Targeted to Mitochondria and Protects against Oxidative Damage and Dark-Induced Senescence.
F.-Q. Guo and N. M. Crawford (2005)
PLANT CELL 17, 3436-3450
   Abstract »    Full Text »    PDF »
Characterization of Transformed Arabidopsis with Altered Alternative Oxidase Levels and Analysis of Effects on Reactive Oxygen Species in Tissue.
A. L. Umbach, F. Fiorani, and J. N. Siedow (2005)
Plant Physiology 139, 1806-1820
   Abstract »    Full Text »    PDF »
Use of mitochondrial electron transport mutants to evaluate the effects of redox state on photosynthesis, stress tolerance and the integration of carbon/nitrogen metabolism.
G. Noctor, C. Dutilleul, R. De Paepe, and C. H. Foyer (2004)
J. Exp. Bot. 55, 49-57
   Abstract »    Full Text »    PDF »
Changes in Mitochondrial Electron Partitioning in Response to Herbicides Inhibiting Branched-Chain Amino Acid Biosynthesis in Soybean.
S. Gaston, M. Ribas-Carbo, S. Busquets, J. A. Berry, A. Zabalza, and M. Royuela (2003)
Plant Physiology 133, 1351-1359
   Abstract »    Full Text »    PDF »
Enzymes of Glycolysis Are Functionally Associated with the Mitochondrion in Arabidopsis Cells.
P. Giege, J. L. Heazlewood, U. Roessner-Tunali, A. H. Millar, A. R. Fernie, C. J. Leaver, and L. J. Sweetlove (2003)
PLANT CELL 15, 2140-2151
   Abstract »    Full Text »    PDF »
Genetic Modification of Alternative Respiration Has Differential Effects on Antimycin A-Induced versus Salicylic Acid-Induced Resistance to Tobacco mosaic virus.
A. Gilliland, D. P. Singh, J. M. Hayward, C. A. Moore, A. M. Murphy, C. J. York, J. Slator, and J. P. Carr (2003)
Plant Physiology 132, 1518-1528
   Abstract »    Full Text »    PDF »
Leaf Mitochondria Modulate Whole Cell Redox Homeostasis, Set Antioxidant Capacity, and Determine Stress Resistance through Altered Signaling and Diurnal Regulation.
C. Dutilleul, M. Garmier, G. Noctor, C. Mathieu, P. Chetrit, C. H. Foyer, and R. de Paepe (2003)
PLANT CELL 15, 1212-1226
   Abstract »    Full Text »    PDF »
Ethylene Insensitivity Modulates Ozone-Induced Cell Death in Birch.
J. Vahala, R. Ruonala, M. Keinanen, H. Tuominen, and J. Kangasjarvi (2003)
Plant Physiology 132, 185-195
   Abstract »    Full Text »    PDF »
Mitochondrial Alternative Oxidase Is Not a Critical Component of Plant Viral Resistance But May Play a Role in the Hypersensitive Response.
S. H. Ordog, V. J. Higgins, and G. C. Vanlerberghe (2002)
Plant Physiology 129, 1858-1865
   Abstract »    Full Text »    PDF »

To Advertise     Find Products


Science Signaling. ISSN 1937-9145 (online), 1945-0877 (print). Pre-2008: Science's STKE. ISSN 1525-8882