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PMID: 18685041 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Generation of hydrogen peroxide in chloroplasts of Arabidopsis overexpressing glycolate oxidase as an inducible system to study oxidative stress.

Plant physiology ·Vol. 148 ·No. 2 ·2008-10-00 ·Pages 719-29

Fahnenstich H, Scarpeci TE, Valle EM, Flügge UI, Maurino VG

Abstract

Arabidopsis (Arabidopsis thaliana) overexpressing glycolate oxidase (GO) in chloroplasts accumulates both hydrogen peroxide (H(2)O(2)) and glyoxylate. GO-overexpressing lines (GO plants) grown at 75 micromol quanta m(-2) s(-1) show retarded development, yellowish rosettes, and impaired photosynthetic performance, while at 30 micromol quanta m(-2) s(-1), this phenotype virtually disappears. The GO plants develop oxidative stress lesions under photorespiratory conditions but grow like wild-type plants under nonphotorespiratory conditions. GO plants coexpressing enzymes that further metabolize glyoxylate but still accumulate H(2)O(2) show all features of the GO phenotype, indicating that H(2)O(2) is responsible for the GO phenotype. The GO plants can complete their life cycle, showing that they are able to adapt to the stress conditions imposed by the accumulation of H(2)O(2) during the light period. Moreover, the data demonstrate that a response to oxidative stress is installed, with increased expression and/or activity of known oxidative stress-responsive components. Hence, the GO plants are an ideal noninvasive model system in which to study the effects of H(2)O(2) directly in the chloroplasts, because H(2)O(2) accumulation is inducible and sustained perturbations can reproducibly be provoked by exposing the plants to different ambient conditions.

MeSH Terms
Alcohol Oxidoreductases/genetics,metabolism Anthocyanins/metabolism Antioxidants/metabolism Arabidopsis/enzymology,genetics Arabidopsis Proteins/genetics,metabolism Chloroplasts/enzymology,genetics Gene Expression Regulation, Plant Genes, Plant Genetic Vectors Glyoxylates/metabolism Hydrogen Peroxide/metabolism Light Oxidative Stress Phenotype Plants, Genetically Modified/enzymology,genetics RNA, Plant/genetics Recombinant Proteins/genetics,metabolism Starch/metabolism Transgenes
Chemicals
Anthocyanins Antioxidants Arabidopsis Proteins Glyoxylates RNA, Plant Recombinant Proteins Starch Hydrogen Peroxide Alcohol Oxidoreductases glycollate oxidase glyoxylic acid
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Fahnenstich Holger
Botanisches Institut, Universität zu Köln, Cologne, Germany.
Scarpeci Telma E
Valle Estela M
Flügge Ulf-Ingo
Maurino Verónica G
References (51)
51 references, click to expand
  1. Alteration of organic acid metabolism in Arabidopsis overexpressing the maize C4 NADP-malic enzyme causes accelerated senescence during extended darkness.
    Plant Physiol. 2007 Nov;145(3):640-52 PMID: 17885087
  2. Production and scavenging of reactive oxygen species in chloroplasts and their functions.
    Plant Physiol. 2006 Jun;141(2):391-6 PMID: 16760493
  3. Genome-wide analysis of hydrogen peroxide-regulated gene expression in Arabidopsis reveals a high light-induced transcriptional cluster involved in anthocyanin biosynthesis.
    Plant Physiol. 2005 Oct;139(2):806-21 PMID: 16183842
  4. Hydroperoxide reduction by thioredoxin-specific glutathione peroxidase isoenzymes of Arabidopsis thaliana.
    FEBS J. 2006 Dec;273(24):5589-97 PMID: 17096689
  5. Photorespiration: metabolic pathways and their role in stress protection.
    Philos Trans R Soc Lond B Biol Sci. 2000 Oct 29;355(1402):1517-29 PMID: 11128005
  6. Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis.
    Science. 1999 Apr 23;284(5414):654-7 PMID: 10213690
  7. Generation of superoxide anion in chloroplasts of Arabidopsis thaliana during active photosynthesis: a focus on rapidly induced genes.
    Plant Mol Biol. 2008 Mar;66(4):361-78 PMID: 18158584
  8. Physiological significance of anthocyanins during autumnal leaf senescence.
    Tree Physiol. 2001 Jan;21(1):1-8 PMID: 11260818
  9. Ascorbate biosynthesis and function in photoprotection.
    Philos Trans R Soc Lond B Biol Sci. 2000 Oct 29;355(1402):1455-64 PMID: 11127999
  10. Changes in hydrogen peroxide homeostasis trigger an active cell death process in tobacco.
    Plant J. 2003 Feb;33(4):621-32 PMID: 12609037
  11. A comprehensive analysis of hydrogen peroxide-induced gene expression in tobacco.
    Proc Natl Acad Sci U S A. 2003 Dec 23;100(26):16113-8 PMID: 14671332
  12. Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis.
    Plant Physiol. 2006 Jun;141(2):436-45 PMID: 16603662
  13. Altered regulation of lipid biosynthesis in a mutant of Arabidopsis deficient in chloroplast glycerol-3-phosphate acyltransferase activity.
    Proc Natl Acad Sci U S A. 1988 Jun;85(12):4143-7 PMID: 16593939
  14. Superoxide dismutase in Arabidopsis: an eclectic enzyme family with disparate regulation and protein localization.
    Plant Physiol. 1998 Oct;118(2):637-50 PMID: 9765550
  15. The role of photosynthetic electron transport in the oxidative degradation of chloroplastic glutamine synthetase
    Plant Physiol. 1999 Oct;121(2):471-8 PMID: 10517838
  16. Superoxide dismutase: improved assays and an assay applicable to acrylamide gels.
    Anal Biochem. 1971 Nov;44(1):276-87 PMID: 4943714
  17. Impact of chloroplastic- and extracellular-sourced ROS on high light-responsive gene expression in Arabidopsis.
    J Exp Bot. 2008;59(2):121-33 PMID: 18212028
  18. Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life.
    Plant Physiol. 2006 Jun;141(2):312-22 PMID: 16760481
  19. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  20. An Analysis of Phytochrome-mediated Anthocyanin Synthesis.
    Plant Physiol. 1971 May;47(5):649-55 PMID: 16657678
  21. Growth suppression, altered stomatal responses, and augmented induction of heat shock proteins in cytosolic ascorbate peroxidase (Apx1)-deficient Arabidopsis plants.
    Plant J. 2003 Apr;34(2):187-203 PMID: 12694594
  22. Regulation of the Arabidopsis transcriptome by oxidative stress.
    Plant Physiol. 2001 Sep;127(1):159-72 PMID: 11553744
  23. Alterations in Growth, Photosynthesis, and Respiration in a Starchless Mutant of Arabidopsis thaliana (L.) Deficient in Chloroplast Phosphoglucomutase Activity.
    Plant Physiol. 1985 Sep;79(1):11-7 PMID: 16664354
  24. Conditional oxidative stress responses in the Arabidopsis photorespiratory mutant cat2 demonstrate that redox state is a key modulator of daylength-dependent gene expression, and define photoperiod as a crucial factor in the regulation of H2O2-induced cell death.
    Plant J. 2007 Nov;52(4):640-57 PMID: 17877712
  25. The metabolic response of heterotrophic Arabidopsis cells to oxidative stress.
    Plant Physiol. 2007 Jan;143(1):312-25 PMID: 17122072
  26. Plant nutritional status modulates glutamine synthetase levels in ripe tomatoes (Solanum lycopersicum cv. Micro-Tom).
    J Plant Physiol. 2007 Feb;164(2):137-45 PMID: 16513209
  27. Levels of active oxygen species are controlled by ascorbic acid and anthocyanin in Arabidopsis.
    J Agric Food Chem. 2003 May 7;51(10):2992-9 PMID: 12720382
  28. pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation.
    Plant Mol Biol. 2000 Apr;42(6):819-32 PMID: 10890530
  29. Control of Ascorbate Peroxidase 2 expression by hydrogen peroxide and leaf water status during excess light stress reveals a functional organisation of Arabidopsis leaves.
    Plant J. 2003 Feb;33(4):691-705 PMID: 12609042
  30. Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer.
    Photosynth Res. 1986 Jan;10(1-2):51-62 PMID: 24435276
  31. Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate.
    Plant Cell. 2001 Jan;13(1):179-91 PMID: 11158538
  32. Biochemical and structural studies of malate synthase from Mycobacterium tuberculosis.
    J Biol Chem. 2003 Jan 17;278(3):1735-43 PMID: 12393860
  33. Reactive oxygen species: metabolism, oxidative stress, and signal transduction.
    Annu Rev Plant Biol. 2004;55:373-99 PMID: 15377225
  34. Redox regulation: a broadening horizon.
    Annu Rev Plant Biol. 2005;56:187-220 PMID: 15862094
  35. Induction of ASCORBATE PEROXIDASE 2 expression in wounded Arabidopsis leaves does not involve known wound-signalling pathways but is associated with changes in photosynthesis.
    Plant J. 2004 May;38(3):499-511 PMID: 15086807
  36. The water-water cycle is essential for chloroplast protection in the absence of stress.
    J Biol Chem. 2003 Oct 3;278(40):38921-5 PMID: 12885779
  37. Detection of singlet oxygen and superoxide with fluorescent sensors in leaves under stress by photoinhibition or UV radiation.
    Plant Cell Physiol. 2002 Oct;43(10):1154-64 PMID: 12407195
  38. Rapid inactivation of plant aconitase by hydrogen peroxide.
    Biochem J. 1991 Jun 15;276 ( Pt 3):643-8 PMID: 1648348
  39. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method.
    Methods. 2001 Dec;25(4):402-8 PMID: 11846609
  40. Purification and characterization of glycolate oxidase from pumpkin cotyledons.
    Arch Biochem Biophys. 1983 Apr 15;222(2):397-402 PMID: 6342538
  41. Signal transduction in response to excess light: getting out of the chloroplast.
    Curr Opin Plant Biol. 2002 Feb;5(1):43-8 PMID: 11788307
  42. Spatial dependence for hydrogen peroxide-directed signaling in light-stressed plants.
    Plant Physiol. 2006 Jun;141(2):346-50 PMID: 16760486
  43. Antisense reduction of thylakoidal ascorbate peroxidase in Arabidopsis enhances paraquat-induced photooxidative stress and nitric oxide-induced cell death.
    Planta. 2005 Aug;221(6):757-65 PMID: 15744494
  44. ASCORBATE AND GLUTATHIONE: Keeping Active Oxygen Under Control.
    Annu Rev Plant Physiol Plant Mol Biol. 1998 Jun;49:249-279 PMID: 15012235
  45. Investigation of the energy requirement and targeting signal for the import of glycolate oxidase into glyoxysomes.
    Eur J Biochem. 1995 May 15;230(1):157-63 PMID: 7601095
  46. Reduction to below threshold levels of glycolate oxidase activities in transgenic tobacco enhances photoinhibition during irradiation.
    Plant Cell Physiol. 2000 Dec;41(12):1397-406 PMID: 11134426
  47. Catalase deficiency drastically affects gene expression induced by high light in Arabidopsis thaliana.
    Plant J. 2004 Jul;39(1):45-58 PMID: 15200641
  48. Overexpression of Superoxide Dismutase Protects Plants from Oxidative Stress (Induction of Ascorbate Peroxidase in Superoxide Dismutase-Overexpressing Plants).
    Plant Physiol. 1993 Dec;103(4):1067-1073 PMID: 12232001
  49. THE WATER-WATER CYCLE IN CHLOROPLASTS: Scavenging of Active Oxygens and Dissipation of Excess Photons.
    Annu Rev Plant Physiol Plant Mol Biol. 1999 Jun;50:601-639 PMID: 15012221
  50. Dual action of the active oxygen species during plant stress responses.
    Cell Mol Life Sci. 2000 May;57(5):779-95 PMID: 10892343
  51. THE C2 OXIDATIVE PHOTOSYNTHETIC CARBON CYCLE.
    Annu Rev Plant Physiol Plant Mol Biol. 1997 Jun;48:1-25 PMID: 15012254
Article Info
Journal
Plant physiology
Abbr.
Plant Physiol
ISSN
0032-0889
Published
2008-10-00
Epub
2008-00-06
Pages
719-29
Language
English
Region
United States
NLM ID
0401224
PMCID
PMC2556821
Subset
IM
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