Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis

Plant Cell

Volumn 17, Issue 1, 2005, Pages 268-281

  Davletova, Sholpan ^a   Rizhsky, Ludmila ^b   Liang, Hongjian ^b   Shengqiang, Zhong ^b   Oliver, David J ^b   Coutu, Jesse ^a   Shulaev, Vladimir ^c   Schlauch, Karen ^d   Mittler, Ron ^a  

^a UNIVERSITY OF NEVADA   (United States)

^b IOWA STATE UNIVERSITY   (United States)

^c VIRGINIA BIOINFORMATICS INSTITUTE   (United States)

^d GEORGE MASON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

METABOLISM; OXIDATION; OXYGEN; PLANTS (BOTANY); PROTEINS;

FOCAL POINT; PLANT METABOLISM; REACTIVE OXYGEN SPECIES (ROS);

ENZYMES;

ENZYMES; METABOLISM; OXIDATION; OXYGEN; PLANTS; PROTEINS;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ARABIDOPSIS PROTEIN; ASCORBATE PEROXIDASE, ARABIDOPSIS; HYDROGEN PEROXIDE; PEROXIDASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ARABIDOPSIS; ARTICLE; CHLOROPLAST; CYTOSOL; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; LIGHT; METABOLISM; MITOCHONDRION; PHOTOSTIMULATION; PLANT LEAF; THYLAKOID;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHLOROPLASTS; CYTOSOL; GENE EXPRESSION REGULATION, PLANT; HYDROGEN PEROXIDE; LIGHT; MITOCHONDRIA; NADPH OXIDASE; PEROXIDASES; PHOTIC STIMULATION; PLANT LEAVES; REACTIVE OXYGEN SPECIES; THYLAKOIDS;

EID: 20044375371     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.104.026971     Document Type: Article

References (64)

1. Ahn, S.G., and Thiele, D.J. (2003). Redox regulation of mammalian heat shock factor 1 is essential for Hsp gene activation and protection from stress. Genes Dev. 17, 516-528.
2. Akenov, M.Y., Aksenova, M.V., Butterfield, D.A., Geddes, J.W., and Markesbery, W.R. (2001). Protein oxidation in the brain in Alzheimer's disease. Neuroscience 103, 373-383.
3. Apel, K., and Hirt, H. (2004). Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55, 373-399.
4. Asada, K. (1999). The water-water cycle in chloroplasts: Scavenging of active oxygen and dissipation of excess photons. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 601-639.
5. Asada, K. (2000). The water-water cycle as alternative photon and electron sinks. Philos. Trans. R. Soc. Lond. B Biol. Sci. 355, 1419-1431.
6. Asada, K., and Takahashi, M. (1987). Production and scavenging of active oxygen in photosynthesis. In Photoinhibition, D.J. Kyle, C.B. Osmond, and C.J. Arntzen, eds (Amsterdam: Elsevier), pp. 227-287.
7. Bechtold, U., Murphy, D.J., and Mullineaux, P.M. (2004). Arabidopsis peptide methionine sulfoxide reductase2 prevents cellular oxidative damage in long nights. Plant Cell 16, 908-919.
8. Benjamini, Y., and Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R. Stat. Soc. B 57, 289-300.
9. Bowler, C., and Fluhr, R. (2000). The role of calcium and activated oxygens as signals for controlling cross-tolerance. Trends Plant Sci. 5, 241-246.
10. Chew, O., Whelan, J., and Millar, A.H. (2003). Molecular definition of the ascorbate-glutathione cycle in Arabidopsis mitochondria reveals dual targeting of antioxidant defenses in plants. J. Biol. Chem. 278, 46869-46877.
11. Corpas, F.J., Barroso, J.B., and del Rio, L.A. (2001). Peroxisomes as a source of reactive oxygen species and nitric oxide signal molecules in plant cells. Trends Plant Sci. 6, 145-150.
12. Danna, C.H., Bartoli, C.G., Sacco, F., Ingala, L.R., Santa-Maria, G.E., Guiamet, J.J., and Ugalde, R.A. (2003). Thylakoid-bound ascorbate peroxidase mutant exhibits impaired electron transport and photosynthetic activity. Plant Physiol. 132, 2116-2125.
13. Dat, J., Vandenabeele, S., Vranova, E., Van Montagu, M., Inze, D., and Van Breusegem, F. (2000). Dual action of the active oxygen species during plant stress responses. Cell. Mol. Life Sci. 57, 779-795.
14. Dat, J.F., Pellinen, R., Beeckman, T., Van De Cotte, B., Langebartels, C., Kangasjarvi, J., Inze, D., and Van Breusegem, F. (2003). Changes in hydrogen peroxide homeostasis trigger an active cell death process in tobacco. Plant J. 33, 621-632.
15. Desikan, R., Cheung, M.K., Bright, J., Henson, D., Hancock, J.T., and Neill, S.J. (2004). ABA, hydrogen peroxide and nitric oxide signalling in stomatal guard cells. J. Exp. Bot. 55, 205-212.
16. Dietz, K.J. (2003). Plant peroxiredoxins. Annu. Rev. Plant Biol. 54, 93-107.
17. Foreman, J., Demidchik, V., Bothwell, J.H., Mylona, P., Miedema, H., Torres, M.A., Linstead, P., Costa, S., Brownlee, C., Jones, J.D., Davies, J.M., and Dolan, L. (2003). Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422, 442-446.
18. Gautier, L., Cope, L., Bolstad, B., and Irizarry, R.A. (2004). Affy - Analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20, 307-315.
19. Halliwell, B., and Gutteridge, J.M.C. (1989). Free Radicals in Biology and Medicine. (Oxford: Clarendon Press).
20. Henzler, T., and Steudle, E. (2000). Transport and metabolic degradation of hydrogen peroxide in Chara corallina: Model calculations and measurements with the pressure probe suggest transport of H(2)O(2) across water channels. J. Exp. Bot. 51, 2053-2066.
21. Iida, A., Kazuoka, T., Torikai, S., Kikuchi, H., and Oeda, K. (2000). A zinc finger protein RHL41 mediates the light acclimatization response in Arabidopsis. Plant J. 24, 191-203.
22. Irizarry, R.A., Hobbs, R., Collin, R., Beazer-Barclay, Y.D., Antonellis, K.J., Scherf, U., and Speed, T.P. (2003). Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4, 249-264.
23. Johansson, E., Olsson, O., and Nystrom, T. (2004). Progression and specificity of protein oxidation in the life cycle of Arabidopsis thaliana. J. Biol. Chem. 279, 22204-22208.
24. Karpinski, S., Escobar, C., Karpinska, B., Creissen, G., and Mullineaux, P.M. (1997). Photosynthetic electron transport regulates the expression of cytosolic ascorbate peroxidase genes in Arabidopsis during excess light stress. Plant Cell 9, 627-640.
25. Karpinski, S., Reynolds, H., Karpinska, B., Wingsle, G., Creissen, G., and Mullineaux, P. (1999). Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 284, 654-657.
26. Kerr, M.K., Martin, M., and Churchill, G.A. (2000). Analysis of variance for gene expression microarray data. J. Comput. Biol. 7, 819-837.
27. Kwak, J.M., Mori, I.C., Pei, Z.M., Leonhardt, N., Torres, M.A., Dangl, J.L., Bloom, R.E., Bodde, S., Jones, J.D., and Schroeder, J.I. (2003). NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J. 22, 2623-2633.
28. Mach, J.M., Castillo, A.R., Hoogstraten, R., and Greenberg, J.T. (2001). The Arabidopsis-accelerated cell death gene ACD2 encodes red chlorophyll catabolite reductase and suppresses the spread of disease symptoms. Proc. Natl. Acad. Sci. USA 98, 771-776.
29. Mano, J., Ohno, C., Domae, Y., and Asada, K. (2001). Chloroplastic ascorbate peroxidase is the primary target of methylviologen-induced photooxidative stress in spinach leaves: Its relevance to monodehydroascorbate radical detected with in vivo ESR. Biochim. Biophys. Acta 1504, 275-287.
30. Mehta, R.A., Fawcett, T.W., Porath, D., and Mattoo, A.K. (1992). Oxidative stress causes rapid membrane translocation and in vivo degradation of ribulose-1,5-bisphosphate carboxylase/oxygenase. J. Biol. Chem. 267, 2810-2816.
31. Mittler, R. (2002). Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 7, 405-410.
32. Mittler, R., Feng, X., and Cohen, M. (1998). Post-transcriptional suppression of cytosolic ascorbate peroxidase expression during pathogen-induced programmed cell death in tobacco. Plant Cell 10, 461-474.
33. Mittler, R., Hallak-Herr, E., Orvar, B.L., Van Camp, W., Willekens, H., Inze, D., and Ellis, B. (1999). Transgenic tobacco plants with reduced capability to detoxify reactive oxygen intermediates are hyperresponsive to pathogen infection. Proc. Natl. Acad. Sci. USA 96, 14165-14170.
34. Mittler, R., Vanderauwera, S., Gollery, M., and Van Breusegem, F. (2004). The reactive oxygen gene network of plants. Trends Plant Sci. 9, 490-498.
35. Mittler, R., and Zilinskas, B. (1991). Purification and characterization of pea cytosolic ascorbate peroxidase. Plant Physiol. 97, 962-968.
36. Mittler, R., and Zilinskas, B. (1992). Molecular cloning and characterization of a gene encoding pea cytosolic ascorbate peroxidase. J. Biol. Chem. 267, 21802-21807.
37. Muller-Moule, P., Golan, T., and Niyogi, K.K. (2004). Ascorbate-deficient mutants of Arabidopsis grow in high light despite chronic photooxidative stress. Plant Physiol. 134, 1163-1172.
38. Mullineaux, P., and Karpinski, S. (2002). Signal transduction in response to excess light: getting out of the chloroplast. Curr. Opin. Plant Biol. 5, 43-48.
39. Neill, S., Desikan, R., and Hancock, J. (2002). Hydrogen peroxide signalling. Curr. Opin. Plant Biol. 5, 388-395.
40. Noctor, G., and Foyer, C. (1998). Ascorbate and glutathione: Keeping active oxygen under control. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 249-279.
41. Nover, L., Bharti, K., Doring, P., Mishra, S.K., Ganguli, A., and Scharf, K.D. (2001). Arabidopsis and the heat stress transcription factor world: How many heat stress transcription factors do we need? Cell Stress Chaperones 6, 177-189.
42. Panchuk, I.I., Volkov, R.A., and Schoffl, F. (2002). Heat stress- and heat shock transcription factor-dependent expression and activity of ascorbate peroxidase in Arabidopsis. Plant Physiol. 129, 838-853.
43. Pnueli, L., Hongjian, L., and Mittler, R. (2003). Growth suppression, abnormal guard cell response, and augmented induction of heat shock proteins in cytosolic ascorbate peroxidase (Apx1)-deficient Arabidopsis plants. Plant J. 34, 187-203.
44. Polle, A. (2001). Dissecting the superoxide dismutase-ascorbate peroxidase-glutathione pathway in chloroplasts by metabolic modeling. Computer simulations as a step towards flux analysis. Plant Physiol. 126, 445-462.
45. Porubleva, L., Vander Velden, K., Kothari, S., Oliver, D.J., and Chitnis, P.R. (2001). The proteome of maize leaves: Use of gene sequences and EST data for identification of proteins with peptide mass fingerprints. Electrophoresis 22, 1724-1783.
46. Rentel, M.C., and Knight, M.R. (2004). Oxidative stress-induced calcium signaling in Arabidopsis. Plant Physiol. 135, 1471-1479.
47. Rizhsky, L., Davletova, S., Liang, H., and Mittler, R. (2004). The zinc-finger protein Zat12 is required for cytosolic ascorbate peroxidase 1 expression during oxidative stress in Arabidopsis. J. Biol. Chem. 279, 11736-11743.
48. Rizhsky, L., Hallak-Herr, E., Van Breusegem, F., Rachmilevitch, S., Rodermel, S., Inze, D., and Mittler, R. (2002). Double antisense plants with suppressed expression of ascorbate peroxidase and catalase are less sensitive to oxidative stress than single antisense plants with suppressed expression of ascorbate peroxidase or catalase. Plant J. 32, 329-342.
49. Rizhsky, L., Liang, H., and Mittler, R. (2003). The water-water cycle is essential for chloroplast protection in the absence of stress. J. Biol. Chem. 278, 38921-38925.
50. Rodermel, S. (2001). Pathways of plastid-to-nucleus signaling. Trends Plant Sci. 6, 471-478.
51. Rodriguez-Milla, M.A., Maurer, A., Rodriguez-Huete, A., and Gustafson, J.P. (2003). Glutathione peroxidase genes in Arabidopsis are ubiquitous and regulated by abiotic stresses through diverse signaling pathways. Plant J. 36, 602-615.
52. Shigeoka, S., Ishikawa, T., Tamoi, M., Miyagawa, Y., Takeda, T., Yabuta, Y., and Yoshimura, K. (2002). Regulation and function of ascorbate peroxidase isoenzymes. J. Exp. Bot. 53, 1305-1319.
53. Stadtman, E.R. (1992). Protein oxidation and aging. Science 257, 1220-1224.
54. Storey, J.D., and Tibshirani, R. (2003). Statistical significance for genome-wide experiments. Proc. Natl. Acad. Sci. USA 100, 9440-9445.
55. Storozhenko, S., De Pauw, P., Van Montagu, M., Inze, D., and Kushnir, S. (1998). The heat-shock element is a functional component of the Arabidopsis APX1 gene promoter. Plant Physiol. 118, 1005-1014.
56. Torres, M.A., Dangl, J.L., and Jones, J.D. (2002). Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc. Natl. Acad. Sci. USA 99, 517-522.
57. Ulker, B., and Somssich, I.E. (2004). WRKY transcription factors: From DNA binding towards biological function. Curr. Opin. Plant Biol. 7, 491-498.
58. Vandenabeele, S., Vanderauwera, S., Vuylsteke, M., Rombauts, S., Langebartels, C., Seidlitz, H.K., Zabeau, M., Van Montagu, M., Inze, D., and Van Breusegem, F. (2004). Catalase deficiency drastically affects gene expression induced by high light in Arabidopsis thaliana. Plant J. 39, 45-58.
59. 2 and is indispensable for stress defence in C-3 plants. EMBO J. 16, 4806-4816.
60. Yabuta, Y., Motoki, T., Yoshimura, K., Takeda, T., Ishikawa, T., and Shigeoka, S. (2002). Thylakoid membrane-bound ascorbate peroxidase is a limiting factor of antioxidative systems under photooxidative stress. Plant J. 32, 915-925.
61. Yoo, B.S., and Regnier, F.E. (2004). Proteomic analysis of carbonylated proteins in two-dimensional gel electrophoresis using avidin-fluorescein affinity staining. Electrophoresis 25, 1334-1341.
62. Yoshimura, K., Yabuta, Y., Ishikawa, T., and Shigeoka, S. (2002). Identification of a cis element for tissue-specific alternative splicing of chloroplast ascorbate peroxidase pre-mRNA in higher plants. J. Biol. Chem. 277, 40623-40632.
63. Zhang, S., and Klessig, D.F. (2001). MAPK cascades in plant defense signaling. Trends Plant Sci. 6, 520-527.
64. Zhong, M., Orosz, A., and Wu, C. (1998). Direct sensing of heat shock and oxidation by Drosophila heat shock transcription factor. Mol. Cell 2, 101-108.