Post-Transcriptional Suppression Of Cytosolic Ascorbate Peroxidase Expression During Pathogen-Induced Programmed Cell Death In Tobacco
R. Mittler, X. Feng, M. Cohen
Published 1998 · Biology, Medicine
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As a means to eliminate pathogen-infected cells and prevent diseases, programmed cell death (PCD) appears to be a defense strategy employed by most multicellular organisms. Recent studies have indicated that reactive oxygen species, such as O 2 ⋅ − and H2O2, play a central role in the activation and propagation of pathogen-induced PCD in plants. However, plants contain several mechanisms that detoxify O 2 ⋅ − and H2O2 and may inhibit PCD. We found that during viral-induced PCD in tobacco, the expression of cytosolic ascorbate peroxidase (cAPX), a key H2O2 detoxifying enzyme, is post-transcriptionally suppressed. Thus, although the steady state level of transcripts encoding cAPX was induced during PCD, as expected under conditions of elevated H2O2, the level of the cAPX protein declined. In vivo protein labeling, followed by immunoprecipitation, indicated that the synthesis of the cAPX protein was inhibited. Although transcripts encoding cAPX were found to associate with polysomes during PCD, no cAPX protein was detected after in vitro polysome run-off assays. Our findings suggest that viral-induced PCD in tobacco is accompanied by the suppression of cAPX expression, possibly at the level of translation elongation. This suppression is likely to contribute to a reduction in the capability of cells to scavenge H2O2, which in turn enables the accumulation of H2O2 and the acceleration of PCD.
This paper references
Systemin activates synthesis of wound-inducible tomato leaf polyphenol oxidase via the octadecanoid defense signaling pathway.
C. Constabel (1995)
Identification, characterization, and purification of a tobacco endonuclease activity induced upon hypersensitive response cell death.
R. Mittler (1995)
Assessment of translational regulation by run-off translation of polysomes in vitro.
M. Vayda (1995)
Hydrogen Peroxide Stimulates Salicylic Acid Biosynthesis in Tobacco
J. León (1995)
Sacrifice in the face of foes: pathogen-induced programmed cell death in plants.
R. Mittler (1996)
Death Don't Have No Mercy: Cell Death Programs in Plant-Microbe Interactions.
J. Dangl (1996)
Active Oxygen Species in Plant Defense against Pathogens
M. Mehdy (1994)
Development of necrosis and activation of disease resistance in transgenic tobacco plants with severely reduced catalase levels.
H. Takahashi (1997)
Pretreatment of Parsley (Petroselinum crispum L.) Suspension Cultures with Methyl Jasmonate Enhances Elicitation of Activated Oxygen Species
H. Kauss (1994)
Purification and characterization of pea cytosolic ascorbate peroxidase.
R. Mittler (1991)
Gene cluster of Pseudomonas syringae pv. "phaseolicola" controls pathogenicity of bean plants and hypersensitivity of nonhost plants.
P. B. Lindgren (1986)
Molecular cloning and characterization of a gene encoding pea cytosolic ascorbate peroxidase.
R. Mittler (1992)
Initiation of Runaway Cell Death in an Arabidopsis Mutant by Extracellular Superoxide
T. Jabs (1996)
Ascorbate peroxidase : a hydrogen peroxide-scavenging enzyme in plants
K. Asada (1992)
Is hydrogen peroxide a second messenger of salicylic acid in systemic acquired resistance
U. Neuenschwander (1995)
Evidence for the Presence of the Ascorbate-Glutathione Cycle in Mitochondria and Peroxisomes of Pea Leaves
A. Jiménez (1997)
Inhibition of Programmed Cell Death in Tobacco Plants during a Pathogen-Induced Hypersensitive Response at Low Oxygen Pressure.
R. Mittler (1996)
Pre-activating wounding response in tobacco prior to high-level ozone exposure prevents necrotic injury.
B. L. Orvar (1997)
Translational regulation of gene expression in plants.
Detection of ascorbate peroxidase activity in native gels by inhibition of the ascorbate-dependent reduction of nitroblue tetrazolium.
R. Mittler (1993)
Expression of arabidopsis cytosolic ascorbate peroxidase gene in response to ozone or sulfur dioxide
A. Kubo (2004)
Crystal structure of recombinant pea cytosolic ascorbate peroxidase.
W. R. Patterson (1995)
Involvement of Reactive Oxygen Species, Glutathione Metabolism, and Lipid Peroxidation in the Cf-Gene-Dependent Defense Response of Tomato Cotyledons Induced by Race-Specific Elicitors of Cladosporium fulvum
M. May (1996)
Prevention of hypoxia-induced cell death by Bcl-2 and Bcl-xL
S. Shimizu (1995)
Transgenic tobacco plants expressing antisense RNA for cytosolic ascorbate peroxidase show increased susceptibility to ozone injury
B. L. Örvar (1997)
Active oxygen in plant pathogenesis.
C. J. Baker (1995)
Salicylic Acid Is a Reducing Substrate and Not an Effective Inhibitor of Ascorbate Peroxidase*
M. Kvaratskhelia (1997)
H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response
Alex Levine (1994)
The product of the tobacco mosaic virus resistance gene N: Similarity to toll and the interleukin-1 receptor
S. Whitham (1994)
Programmed cell death: a way of life for plants.
J. Greenberg (1996)
A License to Kill
A. Fraser (1996)
UV-B-Induced PR-1 Accumulation Is Mediated by Active Oxygen Species.
R. Green (1995)
The Active Oxygen Response of Cell Suspensions to Incompatible Bacteria Is Not Sufficient to Cause Hypersensitive Cell Death
J. A. Glazener (1996)
Shigella flexneri induces apoptosis in infected macrophages
A. Zychlinsky (1992)
Jasmonate-signalled plant gene expression
C. Wasternack (1997)
Transgenic tobacco with a reduced catalase activity develops necrotic lesions and induces pathogenesis-related expression under high light
S. Chamnongpol (1996)
Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv phaseolicola.
C. Bestwick (1997)
Programmed cell death and Bcl-2 protection in very low oxygen
M. D. Jacobson (1995)
Local and Systemic Responses of Antioxidants to Tobacco Mosaic Virus Infection and to Salicylic Acid in Tobacco1
J. Fodor (1997)
Salicylic acid potentiates an agonist-dependent gain control that amplifies pathogen signals in the activation of defense mechanisms.
K. Shirasu (1997)
Stress-Induced Translational Control in Potato Tubers May Be Mediated by Polysome-Associated Proteins.
J. S. Crosby (1991)
Methyl jasmonate-regulated translation of nuclear-encoded chloroplast proteins in barley (Hordeum vulgare L. cv. salome).
S. Reinbothe (1993)
Coordinated Activation of Programmed Cell Death and Defense Mechanisms in Transgenic Tobacco Plants Expressing a Bacterial Proton Pump.
R. Mittler (1995)
Photosynthetic electron transport regulates the expression of cytosolic ascorbate peroxidase genes in Arabidopsis during excess light stress.
S. Karpiński (1997)
Resistance gene-dependent plant defense responses.
K. Hammond-Kosack (1996)
Involvement of an O2− generating system in the induction of necrotic lesions on tobacco leaves infected with tobacco mosaic virus
N. Doke (1988)
Salicylate, superoxide synthesis and cell suicide in plant defence
T. Slabas (1997)
Inhibition of ascorbate peroxidase by salicylic acid and 2,6-dichloroisonicotinic acid, two inducers of plant defense responses.
J. Durner (1995)
Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid.
Z. Chen (1993)
Signal perception and transduction in plant defense responses.
Y. Yang (1997)
A methyl jasmonate‐induced shift in the length of the 5′ untranslated region impairs translation of the plastid rbcL transcript in barley.
S. Reinbothe (1993)
Calcium-mediated apoptosis in a plant hypersensitive disease resistance response
A. Levine (1996)
Pathogen-induced programmed cell death in tobacco.
R. Mittler (1997)
Control of the appearance of ascorbate peroxidase (EC 126.96.36.199) in mustard seedling cotyledons by phytochrome and photooxidative treatments
B. Thomsen (1992)
Influence of Salicylic Acid on H2O2 Production, Oxidative Stress, and H2O2-Metabolizing Enzymes (Salicylic Acid-Mediated Oxidative Damage Requires H2O2)
M. Rao (1997)
Cotranslational Folding of Globin*
A. Komar (1997)
Hydrogen peroxide does not function downstream of salicylic acid in the induction of PR protein expression.
Y. Bi (1995)
Viral, worm and radical implications for apoptosis.
G. Häcker (1994)
Regulation of pea cytosolic ascorbate peroxidase and other antioxidant enzymes during the progression of drought stress and following recovery from drought.
R. Mittler (1994)
Salicylic Acid Is Needed in Hypersensitive Cell Death in Soybean but Does Not Act as a Catalase Inhibitor
R. Tenhaken (1997)
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Activated Oxygen Species in Multiple Stress Situations and Protective Systems
R. Mittler (2004)
Elucidating functional interactions between the Russian wheat aphid (D. noxia Kurjumov) and bread wheat (Triticum aestivum L.)
Thia Schultz (2014)
Differential gene expression in foxtail millet during interaction with the smut fungus Ustilago crameri
Lihong Hao (2020)
Arabidopsis thaliana plants overexpressing thylakoidal ascorbate peroxidase show increased resistance to Paraquat-induced photooxidative stress and to nitric oxide-induced cell death.
I. Murgia (2004)
Proteomic and genetic approaches to identifying defence-related proteins in rice challenged with the fungal pathogen Rhizoctonia solani.
Joohyun Lee (2006)
Biochemical basis of apple leaf resistance to Erwinia amylovora infection.
M. Viljevac (2008)
Analysis of proteins differentially accumulated during potato late blight resistance mediated by the RB resistance gene.
Zhenyu Liu (2009)
Responses of Castor Bean (Ricinus communis L.) to Lead Stress
Raikamal Pal (2013)
Ascorbic acid: metabolism and functions of a multi-facetted molecule.
N. Smirnoff (2000)
Expression of peroxidase-like genes, H2O2 production, and peroxidase activity during the hypersensitive response to Xanthomonas campestris pv. vesicatoria in Capsicum annuum.
Hyun Mee Do (2003)
Comparative effects of various nitric oxide donors on ferritin regulation, programmed cell death, and cell redox state in plant cells.
I. Murgia (2004)
Protective effect of nitric oxide against oxidative stress under ultraviolet-B radiation.
Suyun Shi (2005)
Synergistic interaction among begomoviruses leads to the suppression of host defense-related gene expression and breakdown of resistance in chilli
Ashish Kumar Singh (2015)
Oxidative stress and antioxidative responses in plant-virus interactions
José Antonio Hernández (2016)
Ascorbate-Glutathione Cycle and Biotic Stress Tolerance in Plants
Elzbieta Kuzniak (2017)
Rice ascorbate peroxidase gene family encodes functionally diverse isoforms localized in different subcellular compartments
F. Teixeira (2005)
Modulation of root antioxidant status to delay cassava post-harvest physiological deterioration
M. Page (2009)
The Ascorbate–Gluathione Cycle and Related Redox Signals in Plant–Pathogen Interactions
Elzbieta Kuzniak (2010)
Induction of Programmed cell death in tobacco Bright Yellow-2 cell lines and Saccharomyces cerevisiae strainYPH-500 against various apoptotic stimuli
D. L. Reddy (2008)
Fatty Acid Hydroperoxides and H2O2 in the Execution of Hypersensitive Cell Death in Tobacco Leaves1[w]
Jean-Luc Montillet (2005)
Comparison of putative nodule and seed lectin gene promoters of peanut and in situ localization of nodule lectin gene expression
I. J. Law (2000)
The influence of Cocksfoot mottle virus on antioxidant metabolism in the leaves of Dactylis glomerata L.
Zhanlin Li (2003)
Induction of H2O2 in Transgenic Rice Leads to Cell Death and Enhanced Resistance to Both Bacterial and Fungal Pathogens
Aardra Kachroo (2004)
Expression of potential defense responses of Asian and European pears to infection with Venturia nashicola
M. Faize (2004)
The developmental transition to flowering in Arabidopsis is associated with an increase in leaf chloroplastic lipoxygenase activity.
Gloria Rodriguez Bañuelos (2008)
Expression patterns of diverse genes in response to gamma irradiation inNicotiana tabacum
H. S. Cho (2009)
Molecular and biochemical mechanisms associated with dormancy and drought tolerance in the desert legume Retama raetam.
L. Pnueli (2002)
Role of Reactive Oxygen Species in Abiotic and Biotic Stresses in Plants
Miklós Pogány (2006)
Proteome and transcript analysis of Vitis vinifera cell cultures subjected to Botrytis cinerea infection.
K. Dadáková (2015)
Induction of Hairy Roots and Characterization of Peroxidase Expression as a Potential Root Growth Marker in Sesame
J. Chun (2009)
Signals controlling the expression of cytosolic ascorbate peroxidase during pathogen-induced programmed cell death in tobacco
R. Mittler (2004)
Isolation and characterization of genes rapidly induced by singlet oxygen in Arabidopsis
Christian Ochsenbein (2003)See more