Recent advances in ascorbate biosynthesis and the physiological significance of ascorbate peroxidase in photosynthesizing organisms

Bioscience, Biotechnology and Biochemistry

Volumn 72, Issue 5, 2008, Pages 1143-1154

  Ishikawa, Takahiro ^a   Shigeoka, Shigeru ^b  

^a SHIMANE UNIVERSITY   (Japan)

^b KINKI UNIVERSITY   (Japan)

Author keywords

Ascorbate biosynthesis; Ascorbate peroxidase; Environmental stress; Gene expression; Reactive oxygen species

Indexed keywords

BIOCHEMISTRY; BIOSYNTHESIS; FOOD ADDITIVES; TELLURIUM COMPOUNDS;

ANTIOXIDATIVE DEFENSE; ASCORBATE PEROXIDASE (APOX); EUKARYOTIC ALGAE; GALACTOSE (GLCN); IN PLANTS; MULTIPLE FUNCTIONS; PEROXIDASE (POD); PHYSIOLOGICAL SIGNIFICANCE;

BIOCHEMICAL ENGINEERING;

ASCORBATE PEROXIDASE; ASCORBIC ACID; ISOENZYME; PEROXIDASE;

BIOSYNTHESIS; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHOTOSYNTHESIS; PLANT; REVIEW;

ASCORBIC ACID; GENE EXPRESSION REGULATION, PLANT; ISOENZYMES; PEROXIDASES; PHOTOSYNTHESIS; PLANTS;

ALGAE; EUKARYOTA;

EID: 45749125984     PISSN: 09168451     EISSN: 13476947     Source Type: Journal    
DOI: 10.1271/bbb.80062     Document Type: Review

References (102)

1. Noctor, G., and Foyer, C. H., Ascorbate and glutathione: keeping active oxygen under control. Ann. Rev. Plant Physiol. Plant Mol. Biol., 49, 249-279 (1998).
2. Smirnoff, N., Ascorbic acid: metabolism and functions of a multi-facetted molecule. Curr. Opin. Plant Biol., 3, 229-235 (2000).
3. Davey, M. W., Van Montagu, M., Inzé, D., Sanmartin, M., Kanellis, A., Smirnoff, N., Benzie, I. J. J., Strain, J. J., Favell, D., and Fletcher, J., Plant L-ascorbic acid: chemistry, function, metabolism, bioavailability and effects of processing. J. Sci. Food Agric., 80, 825-860 (2000).
4. 2 scavenging in plants. In "Oxidative Stress and the Molecular Biology of Antioxidant Defenses," ed. Scandalios, J. G., Cold Spring Harbor Laboratory Press, New York, pp. 715-735 (1997).
5. Shigeoka, S., Ishikawa, T., Tamoi, M., Miyagawa, Y., Takeda, T., Yabuta, Y., and Yoshimura, K., Regulation and function of ascorbate peroxidase isoenzymes. J. Exp. Bot., 53, 1305-1319 (2002).
6. Asada, K., The water-water cycle in chloroplasts: scavenging of active oxygen species and dissipation of excess photons. Ann. Rev. Plant Physiol. Plant Mol. Biol., 50, 601-639 (1999).
7. Ishikawa, T., Morimoto, Y., Rapolu, M., Sawa, Y., Shibata, H., Yabuta, Y., Nishizawa, A., and Shigeoka, S., Acclimation to diverse environmental stresses caused by a suppression of cytosolic ascorbate peroxidase in tobacco BY-2 cells. Plant Cell Physiol., 46, 1264-1271 (2005).
8. Davletova, S., Rizhsky, L., Liang, H., Shengqiang, Z., Oliver, D. J., Coutu, J., Shulaev, V., Schlauch, K., and Mittler, R., Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell, 17, 268-281 (2005).
9. Wheeler, G. L., Jones, M. A., and Smirnoff, N., The biosynthetic pathway of vitamin C in higher plants. Nature, 393, 365-369 (1998).
10. Smirnoff, N., Conklin, P. L., and Loewus, F. A., Biosynthesis of ascorbic acid in plants: a renaissance. Annu. Rev. Plant Physiol. Plant Mol. Biol., 52, 437-467 (2001).
11. Ishikawa, T., Dowdle, J., and Smirnoff, N., Progress in manipulating ascorbic acid biosynthesis and accumulation in plants. Physiol. Plant., 126, 343-355 (2006).
12. Ostergaard, J., Persiau, G., Davey, M. W., Bauw, G., and Van Montagu, M., Isolation of a cDNA coding for L-galactono-gamma-lactone dehydrogenase, an enzyme involved in the biosynthesis of ascorbic acid in plants: purification, characterization, cDNA cloning, and expression in yeast. J. Biol. Chem., 272, 30009-30016 (1997).
13. Yabuta, Y., Yoshimura, K., Takeda, T., and Shigeoka, S., Molecular characterization of tobacco mitochondrial L-galactono-gamma-lactone dehydrogenase and its expression in Escherichia coli. Plant Cell Physiol., 41, 666-675 (2000).
14. Bartoli, C. G., Pastori, G. M., and Foyer, C. H., Ascorbate biosynthesis in mitochondria is linked to the electron transport chain between complexes III and IV. Plant Physiol., 123, 335-344 (2000).
15. Gatzek, S., Wheeler, G. L., and Smirnoff, N., Antisense suppression of L-galactose dehydrogenase in Arabidopsis thaliana provides evidence for its role in ascorbate synthesis and reveals light modulated L-galactose synthesis. Plant J., 30, 541-553 (2002).
16. Conklin, P. L., Norris, S. R., Wheeler, G. L., Williams, E. H., Smirnoff, N., and Last, R. L., Genetic evidence for the role of GDP-mannose in plant ascorbic acid (vitamin C) biosynthesis. Proc. Natl. Acad. Sci. USA, 96, 4198-4203 (1999).
17. Wolucka, B. A., Persiau, G., Van Doorsselaere, J., Davey, M. W., Demol, H., Vandekerckhove, J., Van Montagu, M., Zabeau, M., and Boerjan, W., Partial purification and identification of GDP-mannose 3″,5″-epimerase of Arabidopsis thaliana, a key enzyme of the plant vitamin C pathway. Proc. Natl. Acad. Sci. USA, 98, 14843-14848 (2001).
18. Laing, W. A., Bulley, S., Wright, M., Cooney, J., Jensen, D., Barraclough, D., and MacRae, E. A., highly specific L-galactose-1- phosphate phosphatase on the path to ascorbate biosynthesis. Proc. Natl. Acad. Sci. USA, 101, 16976-16981 (2004).
19. Conklin, P. L., Gatzek, S., Wheeler, G. L., Dowdle, J., Raymond, M. J., Rolinski, S., Isupov, M., Littlechild, J. A., and Smirnoff, N., Arabidopsis thaliana VTC4 encodes L-galactose-1-P phosphatase, a plant ascorbic acid biosynthetic enzyme. J. Biol. Chem., 281, 15662-15670 (2006).
20. Dowdle, J., Ishikawa, T., Gatzek, S., Rolinski, S., and Smirnoff, N., Two genes in Arabidopsis thaliana encoding GDP-L-galactose phosphorylase are required for ascorbate biosynthesis and seedling viability. Plant J., 52, 673-689 (2007).
21. Laing, W. A., Wright, M. A., Cooney, J., and Bulley, S. M., The missing step of the L-galactose pathway of ascorbate biosynthesis in plants, an L-galactose guanyltransferase, increases leaf ascorbate content. Proc. Natl. Acad. Sci. USA, 104, 9534-9539 (2007).
22. Major, L. L., Wolucka, B. A., and Naismith, J. H., Structure and function of GDP-mannose-3″,5″-epimerase: an enzyme which performs three chemical reactions at the same active site. J. Am. Chem. Soc., 127, 18309-18320 (2005).
23. Agius, F., González-Lamothe, R., Caballero, J. L., Muñoz-Blanco, J., Botella, M. A., and Valpuesta, V., Engineering increased vitamin C levels in plants by overexpression of a D-galacturonic acid reductase. Nat. Biotechnol., 21, 177-181 (2003).
24. Lorence, A., Chevone, B. I., Mendes, P., and Nessler, C. L., myo-inositol oxygenase offers a possible entry point into plant ascorbate biosynthesis. Plant Physiol., 134, 1200-1205 (2004).
25. Shigeoka, S., Nakano, Y., and Kitaoka, S., The biosynthetic pathway of L-ascorbic acid in Euglena gracilis Z. J. Nutr. Sci. Vitaminol. (Tokyo), 25, 299-307 (1979).
26. Ishikawa, T., Masumoto, I., Iwasa, N., Nishikawa, H., Sawa, Y., Shibata, H., Nakamura, A., Yabuta, Y., and Shigeoka, S., Functional characterization of D-galacturonic acid reductase, a key enzyme of the ascorbate biosynthesis pathway, from Euglena gracilis. Biosci. Biotechnol. Biochem., 70, 2720-2726 (2006).
27. Wolucka, B. A., and Van Montagu, M., GDP-mannose 3′,5′- epimerase forms GDP-L-gulose, a putative intermediate for the de novo biosynthesis of vitamin C in plants. J. Biol. Chem., 278, 47483-47490 (2003).
28. Conklin, P. L., Saracco, S. A., Norris, S. R., and Last, R. L., Identification of ascorbic acid-deficient Arabidopsis thaliana mutants. Genetics, 154, 847-856 (2000).
29. Carrari, F., Baxter, C., Usadel, B., Urbanczyk-Wochniak, E., Zanor, M. I., Nunes-Nesi, A., Nikiforova, V., Centero, D., Ratzka, A., Pauly, M., Sweetlove, L. J., and Fernie, A. R., Integrated analysis of metabolite and transcript levels reveals the metabolic shifts that underlie tomato fruit development and highlight regulatory aspects of metabolic network behavior. Plant Physiol., 142, 1380-1396 (2006).
30. Tamaoki, M., Mukai, F., Asai, N., Nakajima, N., Kubo, A., Aono, M., and Saji, H., Light-controlled expression of a gene encoding L-galactono- γ-lactone dehydrogenase which affects ascorbate pool size in Arabidopsis thaliana. Plant Sci., 164, 1111-1117 (2003).
31. Yabuta, Y., Mieda, T., Rapolu, M., Nakamura, A., Motoki, T., Maruta, T., Yoshimura, K., Ishikawa, T., and Shigeoka, S., Light regulation of ascorbate biosynthesis is dependent on the photosynthetic electron transport chain but independent of sugars in Arabidopsis. J. Exp. Bot., 58, 2661-2671 (2007).
32. Barth, C., Moeder, W., Klessig, D. F., and Conklin, P. L., The timing of senescence and response to pathogens is altered in the ascorbate-deficient Arabidopsis mutant vitamin c-1. Plant Physiol., 134, 1784-1792 (2004).
33. Pavet, V., Olmos, E., Kiddle, G., Mowla, S., Kumar, S., Antoniw, J., Alvarez, M. E., and Foyer, C. H., Ascorbic acid deficiency activates cell death and disease resistance responses in Arabidopsis. Plant Physiol., 139, 1291-1303 (2005).
34. Smirnoff, N., and Pallanca, J. E., Ascorbate metabolism in relation to oxidative stress. Biochem. Soc. Trans., 24, 472-478 (1996).
35. Pallanca, J. E., and Smirnoff, N., Ascorbic acid metabolism in pea seedlings: a comparison of D-glucosone, L-sorbosone, and L-galactono-1,4-lactone as ascorbate precursors. Plant Physiol., 120, 453-462 (1999).
36. Pateraki, I., Sanmartin, M., Kalamaki, M. S., Gerasopoulos, D., and Kanellis, A. K., Molecular characterization and expression studies during melon fruit development and ripening of L-galactono-1,4-lactone dehydrogenase. J. Exp. Bot., 55, 1623-1633 (2004).
37. Pallanca, J. E., and Smirnoff, N., The control of ascorbic acid synthesis and turnover in pea seedlings. J. Exp. Bot., 51, 669-674 (2000).
38. Mieda, T., Yabuta, Y., Rapolu, M., Motoki, T., Takeda, T., Yoshimura, K., Ishikawa, T., and Shigeoka, S., Feedback inhibition of spinach L-galactose dehydrogenase by L-ascorbate. Plant Cell Physiol., 45, 1271-1279 (2004).
39. Millar, A. H., Mittova, V., Kiddle, G., Heazlewood, J. L., Bartoli, C. G., Theodoulou, F. L., and Foyer, C. H., Control of ascorbate synthesis by respiration and its implications for stress responses. Plant Physiol., 133, 443-447 (2003).
40. Sasaki-Sekimoto, Y., Taki, N., Obayashi, T., Aono, M., Matsumoto, F., Sakurai, N., Suzuki, H., Hirai, M. Y., Noji, M., Saito, K., Masuda, T., Takamiya, K., Shibata, D., and Ohta, H., Coordinated activation of metabolic pathways for antioxidants and defense compounds by jasmonates and their roles in stress tolerance in Arabidopsis. Plant J., 44, 653-668 (2005).
41. Wolucka, B. A., Goossens, A., and Inzé, D., Methyl jasmonate stimulates the de novo biosynthesis of vitamin C in plant cell suspensions. J. Exp. Bot., 56, 2527-2538 (2005).
42. Welinder, K. G., Superfamily of plant, fungal and bacterial peroxidases. Curr. Opin. Struct. Biol., 2, 388-393 (1992).
43. Chew, O., Whelan, J., and Millar, A. H., Molecular definition of the ascorbate-glutathione cycle in Arabidopsis mitochondria reveals dual targeting of antioxidant defenses in plants. J. Biol. Chem., 278, 46869-46877 (2003).
44. Teixeira, F. K., Menezes-Benavente, L., Margis, R., and Margis-Pinheiro, M., Analysis of the molecular evolutionary history of the ascorbate peroxidase gene family: inferences from the rice genome. J. Mol. Evol., 59, 761-770 (2004).
45. Najami, N., Janda, T., Barriah, W., Kayam, G., Tal, M., Guy, M., and Volokita, M., Ascorbate peroxidase gene family in tomato: its identification and characterization. Mol. Genet. Genomics, 279, 171-182 (2008).
46. Peltier, J. B., Emanuelsson, O., Kalume, D. E., Ytterberg, J., Friso, G., Rudella, A., Liberles, D. A., Söderberg, L., Roepstorff, P., von Heijne, G., and van Wijk, K. J., Central functions of the lumenal and peripheral thylakoid proteome of Arabidopsis determined by experimentation and genome-wide prediction. Plant Cell, 14, 211-236 (2002).
47. Schubert, M., Petersson, U. A., Haas, B. J., Funk, C., Schröder, W. P., and Kieselbach, T., Proteome map of the chloroplast lumen of Arabidopsis thaliana. J. Biol. Chem., 277, 8354-8365 (2002).
48. Ishikawa, T., Yoshimura, K., Sakai, K., Tamoi, M., Takeda, T., and Shigeoka, S., Molecular characterization and physiological role of a glyoxysome-bound ascorbate peroxidase from spinach. Plant Cell Physiol., 39, 23-34 (1998).
49. Narendra, S., Venkataramani, S., Shen, G., Wang, J., Pasapula, V., Lin, Y., Kornyeyev, D., Holaday, A. S., and Zhang, H., The Arabidopsis ascorbate peroxidase 3 is a peroxisomal membrane-bound antioxidant enzyme and is dispensable for Arabidopsis growth and development. J. Exp. Bot., 57, 3033-3042 (2006).
50. Rapolu, M., Ishikawa, T., Sawa, Y., Shigeoka, S., and Shibata, H., Characterization of an ascorbate peroxidase in plastids of tobacco BY-2 cells. Physiol. Plant., 117, 550-557 (2003).
51. Shigeoka, S., Nakano, Y., and Kitaoka, S., Purification and some properties of L-ascorbic-acid-specific peroxidase in Euglena gracilis Z. Arch. Biochem. Biophys., 201, 121-127 (1980).
52. Ishikawa, T., Takeda, T., Kohno, H., and Shigeoka, S., Molecular characterization of Euglena ascorbate peroxidase using monoclonal antibody. Biochim. Biophys. Acta, 1290, 69-75 (1996).
53. Sano, S., Ueda, M., Kitajima, S., Takeda, T., Shigeoka, S., Kurano, N., Miyachi, S., Miyake, C., and Yokota, A., Characterization of ascorbate peroxidases from unicellular red alga Galdieria partita. Plant Cell Physiol., 42, 433-440 (2001).
54. Oesterhelt, C., Vogelbein, S., Shrestha, R. P., Stanke, M., and Weber, A. P., The genome of the thermoacidophilic red microalga Galdieria sulphuraria encodes a small family of secreted class III peroxidases that might be involved in cell wall modification. Planta, 227, 353-362 (2008).
55. Takeda, T., Yoshimura, K., Yoshii, M., Kanahoshi, H., Miyasaka, H., and Shigeoka, S., Molecular characterization and physiological role of ascorbate peroxidase from halotolerant Chlamydomonas sp. W80 strain. Arch. Biochem. Biophys., 376, 82-90 (2000).
56. Wilkinson, S. R., Obado, S. O., Mauricio, I. L., and Kelly, J. M., Trypanosoma cruzi expresses a plant-like ascorbate-dependent hemoperoxidase localized to the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA, 99, 13453-13458 (2002).
57. Adak, S., and Datta, A. K., Leishmania major encodes an unusual peroxidase that is a close homologue of plant ascorbate peroxidase: a novel role of the transmembrane domain. Biochem. J., 390, 465-474 (2005).
58. Sharp, K. H., Mewies, M., Moody, P. C., and Raven, E. L., Crystal structure of the ascorbate peroxidase-ascorbate complex. Nat. Struct. Biol., 10, 303-307 (2003).
59. Wada, K., Tada, T., Nakamura, Y., Ishikawa, T., Yabuta, Y., Yoshimura, K., Shigeoka, S., and Nishimura, K., Crystal structure of chloroplastic ascorbate peroxidase from tobacco plants and structural insights into its instability. J. Biochem. (Tokyo), 134, 239-244 (2003).
60. Macdonald, I. K., Badyal, S. K., Ghamsari, L., Moody, P. C., and Raven, E. L., Interaction of ascorbate peroxidase with substrates: a mechanistic and structural analysis. Biochemistry, 45, 7808-7817 (2006).
61. Chen, G.-X., and Asada, K., Ascorbate peroxidase in tea leaves: occurrence of two isozymes and the differences in their enzymatic and molecular properties. Plant Cell Physiol., 30, 987-998 (1989).
62. Kitajima, S., Tomizawa, K., Shigeoka, S., and Yokota, A., An inserted loop region of stromal ascorbate peroxidase is involved in its hydrogen peroxide-mediated inactivation. FEBS J., 273, 2704-2710 (2006).
63. Mittler, R., and Zilinskas, B. A., Molecular cloning and characterization of a gene encoding pea cytosolic ascorbate peroxidase. J. Biol. Chem., 267, 21802-21807 (1992).
64. Yoshimura, K., Yabuta, Y., Ishikawa, T., and Shigeoka, S., Expression of spinach ascorbate peroxidase isoenzymes in response to oxidative stresses. Plant Physiol., 123, 223-234 (2000).
65. Kim, D. W., Shibato, J., Agrawal, G. K., Fujihara, S., Iwahashi, H., Kim, D. H., Shim, I. S., and Rakwal, R., Gene transcription in the leaves of rice undergoing salt-induced morphological changes (Oryza sativa L.). Mol. Cells, 24, 45-59 (2007).
66. Karpinski, S., Escobar, C., Karpinska, B., Creissen, G., and Mullineaux, P. M., Photosynthetic electron transport regulates the expression of cytosolic ascorbate peroxidase genes in Arabidopsis during excess light stress. Plant Cell, 9, 627-640 (1997).
67. Yabuta, Y., Maruta, T., Yoshimura, K., Ishikawa, T., and Shigeoka, S., Two distinct redox signaling pathways for cytosolic APX induction under photo-oxidative stress. Plant Cell Physiol., 45, 1586-1594 (2004).
68. Miyagawa, Y., Tamoi, M., and Shigeoka, S., Evaluation of the defense system in chloroplasts to photooxidative stress caused by paraquat using transgenic tobacco plants expressing catalase from Escherichia coli. Plant Cell Physiol., 41, 311-320 (2000).
69. Yabuta, Y., Motoki, T., Yoshimura, K., Takeda, T., Ishikawa, T., and Shigeoka, S., Thylakoid membrane-bound ascorbate peroxidase is a limiting factor of antioxidative systems under photo-oxidative stress. Plant J., 32, 915-925 (2002).
70. Nishizawa, A., Yabuta, Y., Yoshida, E., Maruta, T., Yoshimura, K., and Shigeoka, S., Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress. Plant J., 48, 535-547 (2006).
71. Panchuk, I. I., Volkov, R. A., and Schöffl, F., Heat stress- and heat shock transcription factor-dependent expression and activity of ascorbate peroxidase in Arabidopsis. Plant Physiol., 129, 838-853 (2002).
72. Suzuki, N., and Mittler, R., Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. Physiol. Plant., 126, 45-51 (2006).
73. Rossel, J. B., Walter, P. B., Hendrickson, L., Chow, W. S., Poole, A., Mullineaux, P. M., and Pogson, B. J., A mutation affecting ASCORBATE PEROXIDASE 2 gene expression reveals a link between responses to high light and drought tolerance. Plant Cell Environ., 29, 269-281 (2006).
74. Ishikawa, T., Sakai, K., Yoshimura, K., Takeda, T., and Shigeoka, S., cDNAs encoding spinach stromal and thylakoid-bound ascorbate peroxidase, differing in the presence or absence of their 3′-coding regions. FEBS Lett., 384, 289-293 (1996).
75. Ishikawa, T., Yoshimura, K., Tamoi, M., Takeda, T., and Shigeoka, S., Alternative mRNA splicing of 3′-terminal exons generates ascorbate peroxidase isoenzymes in spinach (Spinacia oleracea) chloroplasts. Biochem. J., 328, 795-800 (1997).
76. Yoshimura, K., Yabuta, Y., Tamoi, M., Ishikawa, T., and Shigeoka, S., Alternatively spliced mRNA variants of chloroplast ascorbate peroxidase isoenzymes in spinach leaves. Biochem. J., 338, 41-48 (1999).
77. Yoshimura, K., Yabuta, Y., Ishikawa, T., and Shigeoka, S., 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 (2002).
78. Wang, B. B., and Brendel, V., Genome-wide comparative analysis of alternative splicing in plants. Proc. Natl. Acad. Sci. USA, 103, 7175-7180 (2006).
79. Savaldi-Goldstein, S., Aviv, D., Davydov, O., and Fluhr, R., Alternative splicing modulation by a LAMMER kinase impinges on developmental and transcriptome expression. Plant Cell, 15, 926-938 (2003).
80. Macknight, R., Duroux, M., Laurie, R., Dijkwel, P., Simpson, G., and Dean, C., Functional significance of the alternative transcript processing of the Arabidopsis floral promoter FCA. Plant Cell, 14, 877-888 (2002).
81. Tanabe, N., Yoshimura, K., Kimura, A., Yabuta, Y., and Shigeoka, S., Differential expression of alternatively spliced mRNAs of Arabidopsis SR protein homologs, atSR30 and atSR45a, in response to environmental stress. Plant Cell Physiol., 48, 1036-1049 (2007).
82. Shigeoka, S., Takeda, T., and Hanaoka, T., Characterization and immunological properties of selenium-containing glutathione peroxidase induced by selenite in Chlamydomonas reinhardtii. Biochem. J., 275, 623-627 (1991).
83. Takeda, T., Nakano, Y., and Shigeoka, S., Effect of selenite, CO2, and illumination on the induction of selenium-dependent glutathione peroxidase in Chlamydomonas reinharditii. Plant Sci., 94, 81-88 (1993).
84. Ishikawa, T., Takeda, T., Shigeoka, S., Hirayama, O., and Mitsunaga, T., Requirement for iron and its effect on ascorbate peroxidase in Euglena gracilis. Plant Sci., 93, 25-29 (1993).
85. Ishikawa, T., Rapolu, M., and Shigeoka, S., Effect of iron on the expression of ascorbate peroxidase in Euglena gracilis. Plant Sci., 165, 1363-1376 (2003).
86. Rapolu, M., Ishikawa, T., Sawa, Y., Shigeoka, S., and Shibata, H., Post-transcritional regulation of ascorbate peroxidase during light adaptation of Euglena gracilis. Plant Sci., 165, 233-238 (2003).
87. Asada, K., and Takahashi, M., Production and scavenging of active oxygen in photosynthesis. In "Photoinhibition," eds. Kyle, D. L., Osmond, C. B., and Arntzen, C. J., Elsevier Scientific Publishers, Oxford, pp. 227-287 (1987).
88. 2 fixation of isolated intact chloroplasts. Biochem. Biophys. Acta, 440, 476-482 (1976).
89. Takeda, T., Yokota, A., and Shigeoka, S., Resistance of photosynthesis to hydrogen peroxide in algae. Plant Cell Physiol., 36, 1089-1095 (1995).
90. Murgia, I., Tarantino, D., Vannini, C., Bracale, M., Carravieri, S., and Soave, C., Arabidopsis thaliana plants overexpressing thylakoidal ascorbate peroxidase show increased resistance to paraquat-induced photooxidative stress and to nitric oxide-induced cell death. Plant J., 38, 940-953 (2004).
91. Tarantino, D., Vannini, C., Bracale, M., Campa, M., Soave, C., and Murgia, I., Antisense reduction of thylakoidal ascorbate peroxidase in Arabidopsis enhances paraquat-induced photo-oxidative stress and nitric oxide-induced cell death. Planta, 221, 757-765 (2005).
92. Giacomelli, L., Masi, A., Ripoll, D. R., Lee, M. J., and van Wijk, K. J., Arabidopsis thaliana deficient in two chloroplast ascorbate peroxidases shows accelerated light-induced necrosis when levels of cellular ascorbate are low. Plant Mol. Biol., 65, 627-644 (2007).
93. Shikanai, T., Takeda, T., Yamauchi, H., Sano, S., Tomizawa, K., Yokota, A., and Shigeoka, S., Inhibition of ascorbate peroxidase under oxidative stress in tobacco having bacterial catalase in chloroplasts. FEBS Lett., 428, 47-51 (1998).
94. Mittler, R., Feng, X., and Cohen, M., Post-transcriptional suppression of cytosolic ascorbate peroxidase expression during pathogen-induced programmed cell death in tobacco. Plant Cell, 10, 461-473 (1998).
95. Pnueli, L., Liang, H., Rozenberg, M., and Mittler, R., Growth suppression, altered stomatal responses, and augmented induction of heat shock proteins in cytosolic ascorbate peroxidase (Apx1)-deficient Arabidopsis plants. Plant J., 34, 187-203 (2003).
96. Pastori, G. M., Kiddle, G., Antoniw, J., Bernard, S., Veljovic-Jovanovic, S., Verrier, P. J., Noctor, G., and Foyer, C. H., Leaf vitamin C contents modulate plant defense transcripts and regulate genes that control development through hormone signaling. Plant Cell, 15, 939-951 (2003).
97. Lange, T., Purification and partial amino-acid sequence of gibberellin 20-oxidase from Cucurbita maxima L. endosperm. Planta, 195, 108-115 (1994).
98. Rouhier, N., and Jacquot, J. P., The plant multigenic family of thiol peroxidases. Free Radic. Biol. Med., 38, 1413-1421 (2005).
99. Dietz, K. J., Jacob, S., Oelze, M. L., Laxa, M., Tognetti, V., de Miranda, S. M., Baier, M., and Finkemeier, I., The function of peroxiredoxins in plant organelle redox metabolism. J. Exp. Bot., 57, 1697-1709 (2006).
100. Monteiro, G., Horta, B. B., Pimenta, D. C., Augusto, O., and Netto, L. E., Reduction of 1-Cys peroxiredoxins by ascorbate changes the thiol-specific antioxidant paradigm, revealing another function of vitamin C. Proc. Natl. Acad. Sci. USA, 104, 4886-4891 (2007).
101. Yamazaki, D., Motohashi, K., Kasama, T., Hara, Y., and Hisabori, T., Target proteins of the cytosolic thioredoxins in Arabidopsis thaliana. Plant Cell Physiol., 45, 18-27 (2004).
102. Rouhier, N., Villarejo, A., Srivastava, M., Gelhaye, E., Keech, O., Droux, M., Finkemeier, I., Samuelsson, G., Dietz, K. J., Jacquot, J. P., and Wingsle, G., Identification of plant glutaredoxin targets. Antioxid. Redox Signal., 7, 919-929 (2005).