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PMID: 9501118 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Post-transcriptional suppression of cytosolic ascorbate peroxidase expression during pathogen-induced programmed cell death in tobacco.

The Plant cell ·Vol. 10 ·No. 3 ·1998-03-00 ·Pages 461-73

Mittler R, Feng X, Cohen M

Abstract

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 O2.- and H2O2, play a central role in the activation and propagation of pathogen-induced PCD in plants. However, plants contain several mechanisms that detoxify O2.- 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.

MeSH Terms
Acetates/pharmacology Apoptosis Ascorbate Peroxidases Cyclopentanes/pharmacology Cytosol/enzymology Gene Expression Regulation, Enzymologic Gene Expression Regulation, Plant Hydrogen Peroxide/metabolism Isoenzymes/metabolism Oxylipins Peroxidases/metabolism Plant Diseases/virology Plant Growth Regulators/pharmacology Plants, Toxic Polyribosomes/metabolism Pseudomonas/physiology RNA, Messenger/metabolism Salicylates/pharmacology Salicylic Acid Tobacco/enzymology,microbiology,virology Tobacco Mosaic Virus/physiology Transcription, Genetic
Chemicals
Acetates Cyclopentanes Isoenzymes Oxylipins Plant Growth Regulators RNA, Messenger Salicylates methyl jasmonate Hydrogen Peroxide Peroxidases Ascorbate Peroxidases Salicylic Acid
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Mittler R
Department of Plant Sciences, Hebrew University of Jerusalem, Jerusalem 91904, Israel. ron@vms.huji.ac.il
Feng X
Cohen M
References (52)
52 references, click to expand
  1. Purification and characterization of pea cytosolic ascorbate peroxidase.
    Plant Physiol. 1991 Nov;97(3):962-8 PMID: 16668537
  2. Expression of Arabidopsis cytosolic ascorbate peroxidase gene in response to ozone or sulfur dioxide.
    Plant Mol Biol. 1995 Nov;29(3):479-89 PMID: 8534847
  3. Local and Systemic Responses of Antioxidants to Tobacco Mosaic Virus Infection and to Salicylic Acid in Tobacco (Role in Systemic Acquired Resistance).
    Plant Physiol. 1997 Aug;114(4):1443-1451 PMID: 12223782
  4. Inhibition of Programmed Cell Death in Tobacco Plants during a Pathogen-Induced Hypersensitive Response at Low Oxygen Pressure.
    Plant Cell. 1996 Nov;8(11):1991-2001 PMID: 12239372
  5. Systemin activates synthesis of wound-inducible tomato leaf polyphenol oxidase via the octadecanoid defense signaling pathway.
    Proc Natl Acad Sci U S A. 1995 Jan 17;92(2):407-11 PMID: 7831300
  6. Death Don't Have No Mercy: Cell Death Programs in Plant-Microbe Interactions.
    Plant Cell. 1996 Oct;8(10):1793-1807 PMID: 12239362
  7. Coordinated Activation of Programmed Cell Death and Defense Mechanisms in Transgenic Tobacco Plants Expressing a Bacterial Proton Pump.
    Plant Cell. 1995 Jan;7(1):29-42 PMID: 12242350
  8. Methyl jasmonate-regulated translation of nuclear-encoded chloroplast proteins in barley (Hordeum vulgare L. cv. salome).
    J Biol Chem. 1993 May 15;268(14):10606-11 PMID: 8486714
  9. Pathogen-induced programmed cell death in tobacco.
    J Cell Sci. 1997 Jun;110 ( Pt 11):1333-44 PMID: 9202394
  10. Sacrifice in the face of foes: pathogen-induced programmed cell death in plants.
    Trends Microbiol. 1996 Jan;4(1):10-15 PMID: 8824789
  11. Influence of salicylic acid on H2O2 production, oxidative stress, and H2O2-metabolizing enzymes. Salicylic acid-mediated oxidative damage requires H2O2.
    Plant Physiol. 1997 Sep;115(1):137-49 PMID: 9306697
  12. Salicylic acid potentiates an agonist-dependent gain control that amplifies pathogen signals in the activation of defense mechanisms.
    Plant Cell. 1997 Feb;9(2):261-70 PMID: 9061956
  13. Stress-Induced Translational Control in Potato Tubers May Be Mediated by Polysome-Associated Proteins.
    Plant Cell. 1991 Sep;3(9):1013-1023 PMID: 12324625
  14. Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide.
    Science. 1996 Sep 27;273(5283):1853-6 PMID: 8791589
  15. UV-B-Induced PR-1 Accumulation Is Mediated by Active Oxygen Species.
    Plant Cell. 1995 Feb;7(2):203-212 PMID: 12242373
  16. Hydrogen peroxide does not function downstream of salicylic acid in the induction of PR protein expression.
    Plant J. 1995 Aug;8(2):235-45 PMID: 7670505
  17. 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.
    Plant Physiol. 1996 Apr;110(4):1367-1379 PMID: 12226267
  18. Molecular cloning and characterization of a gene encoding pea cytosolic ascorbate peroxidase.
    J Biol Chem. 1992 Oct 25;267(30):21802-7 PMID: 1400489
  19. Identification, characterization, and purification of a tobacco endonuclease activity induced upon hypersensitive response cell death.
    Plant Cell. 1995 Nov;7(11):1951-62 PMID: 8535145
  20. Photosynthetic electron transport regulates the expression of cytosolic ascorbate peroxidase genes in Arabidopsis during excess light stress.
    Plant Cell. 1997 Apr;9(4):627-40 PMID: 9144965
  21. Pretreatment of Parsley (Petroselinum crispum L.) Suspension Cultures with Methyl Jasmonate Enhances Elicitation of Activated Oxygen Species.
    Plant Physiol. 1994 May;105(1):89-94 PMID: 12232189
  22. Resistance gene-dependent plant defense responses.
    Plant Cell. 1996 Oct;8(10):1773-91 PMID: 8914325
  23. Characterization of nuclease activities and DNA fragmentation induced upon hypersensitive response cell death and mechanical stress.
    Plant Mol Biol. 1997 May;34(2):209-21 PMID: 9207837
  24. Development of necrosis and activation of disease resistance in transgenic tobacco plants with severely reduced catalase levels.
    Plant J. 1997 May;11(5):993-1005 PMID: 9193071
  25. Viral, worm and radical implications for apoptosis.
    Trends Biochem Sci. 1994 Mar;19(3):99-100 PMID: 8203023
  26. Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid.
    Science. 1993 Dec 17;262(5141):1883-6 PMID: 8266079
  27. Evidence for the Presence of the Ascorbate-Glutathione Cycle in Mitochondria and Peroxisomes of Pea Leaves.
    Plant Physiol. 1997 May;114(1):275-284 PMID: 12223704
  28. Regulation of pea cytosolic ascorbate peroxidase and other antioxidant enzymes during the progression of drought stress and following recovery from drought.
    Plant J. 1994 Mar;5(3):397-405 PMID: 8180623
  29. A license to kill.
    Cell. 1996 Jun 14;85(6):781-4 PMID: 8681372
  30. Programmed cell death: a way of life for plants.
    Proc Natl Acad Sci U S A. 1996 Oct 29;93(22):12094-7 PMID: 8901538
  31. Active Oxygen Species in Plant Defense against Pathogens.
    Plant Physiol. 1994 Jun;105(2):467-472 PMID: 12232215
  32. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response.
    Cell. 1994 Nov 18;79(4):583-93 PMID: 7954825
  33. Detection of ascorbate peroxidase activity in native gels by inhibition of the ascorbate-dependent reduction of nitroblue tetrazolium.
    Anal Biochem. 1993 Aug 1;212(2):540-6 PMID: 8214598
  34. Gene cluster of Pseudomonas syringae pv. "phaseolicola" controls pathogenicity of bean plants and hypersensitivity of nonhost plants.
    J Bacteriol. 1986 Nov;168(2):512-22 PMID: 3023280
  35. Hydrogen Peroxide Stimulates Salicylic Acid Biosynthesis in Tobacco.
    Plant Physiol. 1995 Aug;108(4):1673-1678 PMID: 12228572
  36. Salicylic acid is a reducing substrate and not an effective inhibitor of ascorbate peroxidase.
    J Biol Chem. 1997 Aug 22;272(34):20998-1001 PMID: 9261100
  37. A methyl jasmonate-induced shift in the length of the 5' untranslated region impairs translation of the plastid rbcL transcript in barley.
    EMBO J. 1993 Apr;12(4):1505-12 PMID: 8467800
  38. Crystal structure of recombinant pea cytosolic ascorbate peroxidase.
    Biochemistry. 1995 Apr 4;34(13):4331-41 PMID: 7703247
  39. Cotranslational folding of globin.
    J Biol Chem. 1997 Apr 18;272(16):10646-51 PMID: 9099713
  40. Shigella flexneri induces apoptosis in infected macrophages.
    Nature. 1992 Jul 9;358(6382):167-9 PMID: 1614548
  41. Prevention of hypoxia-induced cell death by Bcl-2 and Bcl-xL.
    Nature. 1995 Apr 27;374(6525):811-3 PMID: 7723826
  42. Calcium-mediated apoptosis in a plant hypersensitive disease resistance response.
    Curr Biol. 1996 Apr 1;6(4):427-37 PMID: 8723347
  43. Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv phaseolicola.
    Plant Cell. 1997 Feb;9(2):209-21 PMID: 9061952
  44. Signal perception and transduction in plant defense responses.
    Genes Dev. 1997 Jul 1;11(13):1621-39 PMID: 9224713
  45. Translational control of cellular and viral mRNAs.
    Plant Mol Biol. 1996 Oct;32(1-2):145-58 PMID: 8980478
  46. Assessment of translational regulation by run-off translation of polysomes in vitro.
    Methods Cell Biol. 1995;50:349-59 PMID: 8531807
  47. Programmed cell death and Bcl-2 protection in very low oxygen.
    Nature. 1995 Apr 27;374(6525):814-6 PMID: 7536895
  48. Pre-activating wounding response in tobacco prior to high-level ozone exposure prevents necrotic injury.
    Plant J. 1997 Feb;11(2):203-12 PMID: 9076988
  49. Inhibition of ascorbate peroxidase by salicylic acid and 2,6-dichloroisonicotinic acid, two inducers of plant defense responses.
    Proc Natl Acad Sci U S A. 1995 Nov 21;92(24):11312-6 PMID: 7479986
  50. Salicylic Acid Is Needed in Hypersensitive Cell Death in Soybean but Does Not Act as a Catalase Inhibitor.
    Plant Physiol. 1997 Sep;115(1):291-298 PMID: 12223807
  51. The Active Oxygen Response of Cell Suspensions to Incompatible Bacteria Is Not Sufficient to Cause Hypersensitive Cell Death.
    Plant Physiol. 1996 Mar;110(3):759-763 PMID: 12226215
  52. The product of the tobacco mosaic virus resistance gene N: similarity to toll and the interleukin-1 receptor.
    Cell. 1994 Sep 23;78(6):1101-15 PMID: 7923359
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
Published
1998-03-00
Pages
461-73
Language
English
Region
England
NLM ID
9208688
PMCID
PMC144004
Subset
IM
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