Skip to main content
NCBI home page
The Plant Cell logoLink to The Plant Cell
. 1997 Apr;9(4):627–640. doi: 10.1105/tpc.9.4.627

Photosynthetic electron transport regulates the expression of cytosolic ascorbate peroxidase genes in Arabidopsis during excess light stress.

S Karpinski 1, C Escobar 1, B Karpinska 1, G Creissen 1, P M Mullineaux 1
PMCID: PMC156944  PMID: 9144965

Abstract

Exposure of Arabidopsis plants that were maintained under low light (200 mumol of photons m-2 sec-1) to excess light (2000 mumol of photons m-2 sec-1) for 1 hr caused reversible photoinhibition of photosynthesis. Measurements of photosynthetic parameters and the use of electron transport inhibitors indicated that a novel signal transduction pathway was initiated at plastoquinone and regulated, at least in part, by the redox status of the plastoquinone pool. This signal, which preceded the photooxidative burst of hydrogen peroxide (H2O2) associated with photoinhibition of photosynthesis, resulted in a rapid increase (within 15 min) in mRNA levels of two cytosolic ascorbate peroxidase genes (APX1 and APX2). Treatment of leaves with exogenous reduced glutathione abolished this signal, suggesting that glutathione or the redox status of the glutathione pool has a regulatory impact on this signaling pathway. During recovery from photooxidative stress, transcripts for cytosolic glutathione reductase (GOR2) increased, emphasizing the role of glutathione in this stress.

Full Text

The Full Text of this article is available as a PDF (2.2 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aro E. M., Virgin I., Andersson B. Photoinhibition of Photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta. 1993 Jul 5;1143(2):113–134. doi: 10.1016/0005-2728(93)90134-2. [DOI] [PubMed] [Google Scholar]
  2. Bartling D., Radzio R., Steiner U., Weiler E. W. A glutathione S-transferase with glutathione-peroxidase activity from Arabidopsis thaliana. Molecular cloning and functional characterization. Eur J Biochem. 1993 Sep 1;216(2):579–586. doi: 10.1111/j.1432-1033.1993.tb18177.x. [DOI] [PubMed] [Google Scholar]
  3. Bi Y. M., Kenton P., Mur L., Darby R., Draper J. Hydrogen peroxide does not function downstream of salicylic acid in the induction of PR protein expression. Plant J. 1995 Aug;8(2):235–245. doi: 10.1046/j.1365-313x.1995.08020235.x. [DOI] [PubMed] [Google Scholar]
  4. Bowler C., Alliotte T., De Loose M., Van Montagu M., Inzé D. The induction of manganese superoxide dismutase in response to stress in Nicotiana plumbaginifolia. EMBO J. 1989 Jan;8(1):31–38. doi: 10.1002/j.1460-2075.1989.tb03345.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bunkelmann J. R., Trelease R. N. Ascorbate peroxidase. A prominent membrane protein in oilseed glyoxysomes. Plant Physiol. 1996 Feb;110(2):589–598. doi: 10.1104/pp.110.2.589. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Campbell D., Zhou G., Gustafsson P., Oquist G., Clarke A. K. Electron transport regulates exchange of two forms of photosystem II D1 protein in the cyanobacterium Synechococcus. EMBO J. 1995 Nov 15;14(22):5457–5466. doi: 10.1002/j.1460-2075.1995.tb00232.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chen Z., Silva H., Klessig D. F. Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science. 1993 Dec 17;262(5141):1883–1886. doi: 10.1126/science.8266079. [DOI] [PubMed] [Google Scholar]
  8. Conklin P. L., Last R. L. Differential accumulation of antioxidant mRNAs in Arabidopsis thaliana exposed to ozone. Plant Physiol. 1995 Sep;109(1):203–212. doi: 10.1104/pp.109.1.203. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dear S., Staden R. A sequence assembly and editing program for efficient management of large projects. Nucleic Acids Res. 1991 Jul 25;19(14):3907–3911. doi: 10.1093/nar/19.14.3907. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gupta A. S., Webb R. P., Holaday A. S., Allen R. D. 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. doi: 10.1104/pp.103.4.1067. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hérouart D., Van Montagu M., Inzé D. Redox-activated expression of the cytosolic copper/zinc superoxide dismutase gene in Nicotiana. Proc Natl Acad Sci U S A. 1993 Apr 1;90(7):3108–3112. doi: 10.1073/pnas.90.7.3108. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Ishikawa T., Sakai K., Yoshimura K., Takeda T., Shigeoka S. cDNAs encoding spinach stromal and thylakoid-bound ascorbate peroxidase, differing in the presence or absence of their 3'-coding regions. FEBS Lett. 1996 Apr 22;384(3):289–293. doi: 10.1016/0014-5793(96)00332-8. [DOI] [PubMed] [Google Scholar]
  14. Jansson S., Gustafsson P. Type I and type II genes for the chlorophyll a/b-binding protein in the gymnosperm Pinus sylvestris (Scots pine): cDNA cloning and sequence analysis. Plant Mol Biol. 1990 Mar;14(3):287–296. doi: 10.1007/BF00028766. [DOI] [PubMed] [Google Scholar]
  15. Karpinski S., Wingsle G., Karpinska B., Hallgren J. E. Molecular Responses to Photooxidative Stress in Pinus sylvestris (L.) (II. Differential Expression of CuZn-Superoxide Dismutases and Glutathione Reductase. Plant Physiol. 1993 Dec;103(4):1385–1391. doi: 10.1104/pp.103.4.1385. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Karpinski S., Wingsle G., Olsson O., Hällgren J. E. Characterization of cDNAs encoding CuZn-superoxide dismutases in Scots pine. Plant Mol Biol. 1992 Feb;18(3):545–555. doi: 10.1007/BF00040670. [DOI] [PubMed] [Google Scholar]
  17. Kubo A., Saji H., Tanaka K., Kondo N. Expression of Arabidopsis cytosolic ascorbate peroxidase gene in response to ozone or sulfur dioxide. Plant Mol Biol. 1995 Nov;29(3):479–489. doi: 10.1007/BF00020979. [DOI] [PubMed] [Google Scholar]
  18. Kubo A., Saji H., Tanaka K., Kondo N. Genomic DNA structure of a gene encoding cytosolic ascorbate peroxidase from Arabidopsis thaliana. FEBS Lett. 1993 Jan 11;315(3):313–317. doi: 10.1016/0014-5793(93)81185-3. [DOI] [PubMed] [Google Scholar]
  19. Kubo A., Saji H., Tanaka K., Tanaka K., Kondo N. Cloning and sequencing of a cDNA encoding ascorbate peroxidase from Arabidopsis thaliana. Plant Mol Biol. 1992 Feb;18(4):691–701. doi: 10.1007/BF00020011. [DOI] [PubMed] [Google Scholar]
  20. Levine A., Tenhaken R., Dixon R., Lamb C. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell. 1994 Nov 18;79(4):583–593. doi: 10.1016/0092-8674(94)90544-4. [DOI] [PubMed] [Google Scholar]
  21. MEHLER A. H. Studies on reactions of illuminated chloroplasts. I. Mechanism of the reduction of oxygen and other Hill reagents. Arch Biochem Biophys. 1951 Aug;33(1):65–77. doi: 10.1016/0003-9861(51)90082-3. [DOI] [PubMed] [Google Scholar]
  22. Martin C., Prescott A., Mackay S., Bartlett J., Vrijlandt E. Control of anthocyanin biosynthesis in flowers of Antirrhinum majus. Plant J. 1991 Jul;1(1):37–49. doi: 10.1111/j.1365-313x.1991.00037.x. [DOI] [PubMed] [Google Scholar]
  23. Millar A. J., Straume M., Chory J., Chua N. H., Kay S. A. The regulation of circadian period by phototransduction pathways in Arabidopsis. Science. 1995 Feb 24;267(5201):1163–1166. doi: 10.1126/science.7855596. [DOI] [PubMed] [Google Scholar]
  24. Mittler R., Zilinskas B. A. Molecular cloning and characterization of a gene encoding pea cytosolic ascorbate peroxidase. J Biol Chem. 1992 Oct 25;267(30):21802–21807. [PubMed] [Google Scholar]
  25. Mittler R., Zilinskas B. A. 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. doi: 10.1111/j.1365-313x.1994.00397.x. [DOI] [PubMed] [Google Scholar]
  26. Monroy A. F., Dhindsa R. S. Low-temperature signal transduction: induction of cold acclimation-specific genes of alfalfa by calcium at 25 degrees C. Plant Cell. 1995 Mar;7(3):321–331. doi: 10.1105/tpc.7.3.321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Neuhaus G., Bowler C., Kern R., Chua N. H. Calcium/calmodulin-dependent and -independent phytochrome signal transduction pathways. Cell. 1993 Jun 4;73(5):937–952. doi: 10.1016/0092-8674(93)90272-r. [DOI] [PubMed] [Google Scholar]
  28. Prasad T. K., Anderson M. D., Martin B. A., Stewart C. R. Evidence for Chilling-Induced Oxidative Stress in Maize Seedlings and a Regulatory Role for Hydrogen Peroxide. Plant Cell. 1994 Jan;6(1):65–74. doi: 10.1105/tpc.6.1.65. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Price A. H., Taylor A., Ripley S. J., Griffiths A., Trewavas A. J., Knight M. R. Oxidative Signals in Tobacco Increase Cytosolic Calcium. Plant Cell. 1994 Sep;6(9):1301–1310. doi: 10.1105/tpc.6.9.1301. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Russell A. W., Critchley C., Robinson S. A., Franklin L. A., Seaton GGR., Chow W. S., Anderson J. M., Osmond C. B. Photosystem II Regulation and Dynamics of the Chloroplast D1 Protein in Arabidopsis Leaves during Photosynthesis and Photoinhibition. Plant Physiol. 1995 Mar;107(3):943–952. doi: 10.1104/pp.107.3.943. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Storz G., Tartaglia L. A., Farr S. B., Ames B. N. Bacterial defenses against oxidative stress. Trends Genet. 1990 Nov;6(11):363–368. doi: 10.1016/0168-9525(90)90278-e. [DOI] [PubMed] [Google Scholar]
  32. Tsang E. W., Bowler C., Hérouart D., Van Camp W., Villarroel R., Genetello C., Van Montagu M., Inzé D. Differential regulation of superoxide dismutases in plants exposed to environmental stress. Plant Cell. 1991 Aug;3(8):783–792. doi: 10.1105/tpc.3.8.783. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Willekens H., Villarroel R., Van Montagu M., Inzé D., Van Camp W. Molecular identification of catalases from Nicotiana plumbaginifolia (L.). FEBS Lett. 1994 Sep 19;352(1):79–83. doi: 10.1016/0014-5793(94)00923-6. [DOI] [PubMed] [Google Scholar]
  34. Williamson J. D., Scandalios J. G. Differential response of maize catalases and superoxide dismutases to the photoactivated fungal toxin cercosporin. Plant J. 1992 May;2(3):351–358. doi: 10.1111/j.1365-313x.1992.00351.x. [DOI] [PubMed] [Google Scholar]
  35. Wingate V. P., Lawton M. A., Lamb C. J. Glutathione causes a massive and selective induction of plant defense genes. Plant Physiol. 1988 May;87(1):206–210. doi: 10.1104/pp.87.1.206. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. del Río L. A., Sandalio L. M., Palma J. M., Bueno P., Corpas F. J. Metabolism of oxygen radicals in peroxisomes and cellular implications. Free Radic Biol Med. 1992 Nov;13(5):557–580. doi: 10.1016/0891-5849(92)90150-f. [DOI] [PubMed] [Google Scholar]

Articles from The Plant Cell are provided here courtesy of Oxford University Press

RESOURCES