Changes in the ascorbate metabolism of apoplastic and symplastic spaces are associated with cell differentiation

Journal of Experimental Botany

Volumn 55, Issue 408, 2004, Pages 2559-2569

  De Pinto, Maria Concetta ^a   De Gara, Laura ^a,b,c  

^a UNIVERSITY OF BARI   (Italy)

^b UNIVERSITY CAMPUS BIO MEDICO   (Italy)

^c NONE

Author keywords

Ascorbate; Cell wall; Class III peroxidases; Dehydroascorbate; Galactono lactone dehydrogenase; Plant cell differentiation; Reactive oxygen species

Indexed keywords

ASCORBATE METABOLISM; CELLULAR DIFFERENTIATION; ETIOLATED PEA; REDOX ENZYMES;

ENZYMES; FREE RADICALS; METABOLISM; OXIDATION;

CELLS;

ASCORBATE OXIDASE; ASCORBATE PEROXIDASE; ASCORBIC ACID; ISOENZYME; PEROXIDASE;

ARTICLE; CELL DIFFERENTIATION; CELL FRACTIONATION; CYTOLOGY; ENZYMOLOGY; METABOLISM; PEA; PHYSIOLOGY; PLANT; SEEDLING;

ASCORBATE OXIDASE; ASCORBIC ACID; CELL DIFFERENTIATION; ISOENZYMES; PEAS; PEROXIDASE; PEROXIDASES; PLANT SHOOTS; SEEDLING; SUBCELLULAR FRACTIONS;

PISUM; PISUM SATIVUM;

EID: 11144275232     PISSN: 00220957     EISSN: None     Source Type: Journal    
DOI: 10.1093/jxb/erh253     Document Type: Article

References (66)

1. Agrawal GK, Rakwal R, Yonekura M, Kubo A, Saji H. 2002. Proteome analysis of differentially displayed proteins as a tool for investigating ozone stress in rice (Oryza sativa L.) seedlings. Proteomics 2, 947-959.
2. Amako K, Chen G-X, Asada K. 1994. Separate assays specific for ascorbate peroxidase and guaiacol peroxidase and for chloroplastic and cytosolic isoenzymes of ascorbate peroxidase in plants. Plant Cell Physiology 35, 497-504.
3. Arrigoni O. 1994. Ascorbate system in plant development. Journal of Bioenergetics and Biomembranes 26, 407-419.
4. Arrigoni O, Calabrese G, De Gara L, Bitonti MB, Liso R. 1997. Correlation between changes in cell ascorbate and growth of Lupinus albus seedlings. Journal of Plant Physiology 150, 302-308.
5. Arrigoni O, De Gara L, Tommasi F, Liso R. 1992. Changes in the ascorbate system during seed development of Vicia faba L. Plant Physiology 99, 235-238.
6. Asada K. 1999. The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annual Review of Plant Physiology and Plant Molecular Biology 50, 601-639.
7. Borraccino G, Mastropasqua L, De Leonardis S, Dipierro S. 1994. The role of the ascorbic acid system in delaying the senescence of oat (Avena sativa L.) leaf segments. Journal of Plant Physiology 144, 161-166.
8. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248-254.
9. Córdoba F, Gonzáles-Reyes JA. 1994. Ascorbate and plant cell growth. Journal of Bioenergetics and Biomembranes 26, 399-405.
10. Córdoba-Pedregosa MC, Córdoba F, Villalba JM, Gonzáles-Reyes JA. 2003a. Zonal changes in ascorbate and hydrogen peroxide contents, peroxidase, and ascorbate-related enzymes activities in onion roots. Plant Physiology 131, 1-10.
11. Córdoba-Pedregosa MC, Córdoba F, Villalba JM, Gonzáles-Reyes JA. 2003b. Differential distribution of ascorbic acid, peroxidase activity, and hydrogen peroxide along the root axis in Allium cepa L. and its possible relationship with cell growth and differentiation. Protoplasma 221, 57-65.
12. Córdoba-Pedregosa MC, Gonzáles-Reyes JA, Cañadillas MS, Navas P, Córdoba F. 1996. Role of apoplastic and cell wall peroxidases on the stimulation of root elongation by ascorbate. Plant Physiology 112, 1119-1125.
13. De Gara L. 2003. Ascorbate metabolism and plant growth - from germination to cell death. In: Asard H, May J, Smirnoff N, eds. Vitamin C: its function and biochemistry in animals and plants. Oxford: BIOS Scientific Publishers Ltd, 83-95.
14. De Gara L. 2004. Class III peroxidases and ascorbate metabolisms in plants. Phytochemistry Reviews (in press).
15. De Gara L, de Pinto MC, Arrigoni O. 1997. Ascorbate synthesis and ascorbate peroxidase activity during the early stage of wheat germination. Physiologia Plantarum 100, 894-900.
16. De Gara L, de Pinto MC, Moliterni VM, D'Egidio MG. 2003. Redox regulation and storage processes during maturation in kernels of Triticum durum. Journal of Experimental Botany 54, 249-258.
17. De Gara L, de Pinto MC, Paciolla C, Cappetti V, Arrigoni O. 1996. Is ascorbate peroxidase only a scavenger of hydrogen peroxide? In: Obinger C, Burner O, Ederman R, Penel C, Greppen H, eds. Plant peroxidases: biochemistry and physiology. Geneve: University of Geneve, 157-162.
18. De Gara L, Paciolla C, De Tullio MC, Motto M, Arrigoni O. 2000. Ascorbate-dependent hydrogen peroxide detoxification and ascorbate regeneration during germination of a highly productive maize hybrid: evidence of an improved detoxification mechanism against reactive oxygen species. Physiologia Plantarum 109, 7-13.
19. De Gara L, Paciolla C, Liso R, Stefani A, Arrigoni O. 1991. Correlation between ascorbate peroxidase and some anomalies of seedlings from aged caryopses of Dasypyrum villosum (L.) Borb. Journal of Plant Physiology 137, 697-700.
20. de Pinto MC, Francis D, De Gara L. 1999. The redox state of the ascorbate-dehydroascorbate pair as a specific sensor of cell division in tobacco BY-2 cells. Protoplasma 209, 90-97.
21. de Pinto MC, Lavermicocca P, Evidente A, Corsaro MM, Lazzaroni S, De Gara L. 2003. Exopolysaccharides produced by plant pathogenic bacteria affect ascorbate metabolism in Nicotiana tabacum. Plant Cell Physiology 44, 803-810.
22. de Pinto MC, Tommasi F, De Gara L. 2000. Enzymes of the ascorbate biosynthesis and ascorbate-glutathione cycle in cultured cells of tobacco Bright Yellow 2. Plant Physiology and Biochemistry 38, 541-550.
23. de Pinto MC, Tommasi F, De Gara L. 2002. Changes in the antioxidant systems as part of the signalling pathway responsible for the programmed cell death activated by nitric oxide and reactive oxygen species in tobacco BY-2 cells. Plant Physiology 130, 698-708.
24. De Tullio MC, Paciolla C, Della Vecchia F, Rascio N, D'Emerico S, De Gara L, Liso R, Arrigoni O. 1999. Changes in onion root development induced by the inhibition of peptidyl prolyl hydroxylase and influence of the ascorbate system on cell division and elongation. Planta 209, 424-434.
25. Feinberg AP, Vogelstein B. 1983. A technique for radiolabelling DNA-restriction endonuclease fragments to high specific activity. Analytical Biochemistry 132, 6-13.
26. Ferrer MA, Calderon AA, Munoz R, Ros Barceló A. 1990. 4-Methoxy-α-naphthol as a specific substrate for kinetic, zymographic and cytochemical studies on plant peroxidase activities. Phytochemical Analysis 1, 63-69.
27. Foyer CH, Noctor G. 2003. Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisome and mitochondria. Physiologia Plantarum 119, 355-364.
28. Francis D. 1998. Environmental control of the cell cycle in higher plants. In: Bryant JA, Chiatante D, eds. Plant cell proliferation and its regulation in growth and development. New York: Wiley, 79-98.
29. Fry SC. 1998. Oxidative scission of plant cell wall polysaccharides by ascorbate-induced hydroxyl radicals. Biochemical Journal 50, 931-937.
30. 2 production in the apoplast of pea leaves. Its relation with salt-induced necrotic lesions in minor veins. Plant Physiology 127, 817-831.
31. Hindalgo A, Gonzáles-Reyes JA, Navas P. 1989. Ascorbate free radical enhances vacuolization in onion root meristems. Plant, Cell and Environment 12, 455-460.
32. Horemans N, Foyer CH, Asard H. 2000. Transport and action of ascorbate at the plasma membrane. Trends in Plant Science 5, 263-266.
33. Horemans N, Potters G, De Wilde L, Caubergs RJ. 2003. Dehydroascorbate uptake activity correlates with cell growth and cell division of tobacco Bright Yellow 2 cell cultures. Plant Physiology 133, 361-367.
34. Iiyama K, Lam TBT, Stone BA. 1994. Covalent cross links in the cell wall. Plant Physiology 104, 315-320.
35. Kato N, Esaka M. 1999. Changes in ascorbate oxidase gene expression and ascorbate levels in cell division and cell elongation in tobacco cells. Physiologia Plantarum 105, 321-329.
36. Kato N, Esaka M. 2000. Expansion of transgenic tobacco protoplasts expressing pumpkin ascorbate oxidase is more rapid than that of wild-type protoplasts. Planta 210, 1018-1022.
37. Kerk NM, Fedman LJ. 1995. A biochemical model for initiation and maintenance of quiescent centre: implication for organization of root meristems. Development 121, 2825-2833.
38. Kubo A, Saji H, Tanaka K, Kondo N. 1995. Expression of Arabidopsis cytosolic ascorbate peroxidase gene in response to ozone and sulphur dioxide. Plant Molecular Biology 29, 479-485.
39. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
40. Lin CC, Kao CH. 2001. Cell wall peroxidase activity, hydrogen peroxide level and NaCl-inhibited root growth of rice seedlings. Plant and Soil 230, 135-143.
41. Lin L, Varner JE. 1991. Expression of ascorbic acid oxidase in zucchini squash (Cucurbita pepo L.). Plant Physiology 101, 969-976.
42. Liso R, Calabrese G, Bitonti MB, Arrigoni O. 1984. Relationship between ascorbic acid and cell division. Experimental Cell Research 150, 314-320.
43. Luwe M. 1996. Antioxidants in the apoplast and symplast of beech (Fagus sylvatica L.) leaves: seasonal variation and responses to changing ozone concentration in air. Plant, Cell and Environment 19, 321-328.
44. Noctor G, Foyer CH. 1998. Ascorbate and glutathione: keeping active oxygen under control. Annual Review of Plant Physiology and Plant Molecular Biology 49, 249-279.
45. Oakley BR, Kirsch DR, Morris NR. 1980. A simplified ultrasensitive silver stain for detecting proteins in polyacrylamide gels. Analytical Biochemistry 105, 361-363.
46. Ôba K, Ishikawa S, Nishikawa M, Mizuno H, Yamamoto T. 1995. Purification and properties of L-galactono-γ-lactone dehydrogenase, a key enzyme for ascorbic acid biosynthesis, from sweet potato roots. Journal of Biochemistry 117, 120-124.
47. Pastori C, Foyer CH. 2002. Common components, networks and pathways of cross-tolerance to stress. The central role of 'redox' and abscissic acid-mediated controls. Plant Physiology 129, 460-468.
48. Pignocchi C, Foyer CH. 2003. Apoplastic ascorbate metabolism and its role in the regulation of cell signalling. Current Opinion in Plant Biology 6, 379-389.
49. Pignocchi C, Fletcher JM, Wilkinson JE, Barnes JD, Foyer CH. 2003. The function of ascorbate oxidase in tobacco. Plant Physiology 132, 1631-1641.
50. 2 generation during the auto-oxidation of coniferyl alcohol drives the oxidase activity of a highly conserved class III peroxidase involved in lignin biosynthesis. FEBS Letters 529, 198-202.
51. Potters G, De Gara L, Asard H, Horemans N. 2002. Ascorbate and glutathione: guardians of the cell cycle, partners in crime? Plant Physiology and Biochemistry 40, 537-548.
52. Reichheld JP, Vernoux T, Lardon F, van Montagu M, Inzé D. 1999. Specific checkpoints regulate plant cell cycle progression in response to oxidative stress. The Plant Journal 17, 647-656.
53. Ros Barceló A. 1998. Hydrogen peroxide production is a general property of the lignifying xylem from vascular plants. Annals of Botany 82, 97-103.
54. Saji H, Tanaka K, Kondo N. 1990. Monoclonal antibodies to spinach ascorbate peroxidase and immunochemical detection of the enzyme in eight different plant species. Plant Science 69, 1-9.
55. Sambrook J, Fritsch T, Maniatis F. 1989. Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
56. 2 in organs of higher plants by tissue printing on nitrocellulose paper. Plant Physiology 104, 1269-1275.
57. Schützendübel A, Polle A. 2002. Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. Journal of Experimental Botany 53, 1351-1365.
58. Smirnoff N. 2000. Ascorbate biosynthesis and function in photo-protection. Philosophical Transactions of the Royal Society B 355, 1455-1464.
59. Smirnoff N, Wheeler GL. 2000. Ascorbic acid in plants: biosynthesis and function. Critical Reviews in Plant Science 19, 267-290.
60. Takahama U. 1993. Regulation of peroxidase-dependeni: oxidation of phenolic radicals by ascorbic acid: different effects of ascorbic acid on the oxidation of coniferyl alcohol by the apoplastic soluble and cell wall-bound peroxidase from epicotyls of Vigna angularis. Plant Cell Physiology 34, 809-817.
61. Tommasi F, Paciolla C, de Pinto MC, De Gara L. 2001. A comparative study of glutathione and ascorbate metabolism during germination of Pinus pinea L. seeds. Journal of Experimental Botany 52, 1647-1654.
62. Vanacker H, Carver TL, Foyer CH. 1998. Pathogen-induced changes in antioxidant status of the apoplast in barley leaves. Plant Physiology 117, 1103-1114.
63. Veljovic-Jovanovic S, Pignocchi C, Noctor G, Foyer CH. 2001. Low vitamin C in the vtc-1 mutants of Arabidospis is associated with decreases growth and intracellular redistribution of antioxidant system. Plant Physiology 127, 426-435.
64. 561 proteins. Genome Biology 4, R38.
65. Zarra I, Sanchez M, Queijero E, Peña MJ, Revilla G. 1999. The cell wall stiffening mechanism in Pinus pinaster Aiton: regulation by apoplastic levels of ascorbate and hydrogen peroxide. Journal of Science of Food Agriculture 79, 416-420.
66. Zheng X, Van Huystee RB. 1992. Peroxidase-regulated elongation of segments from peanut hypocotyls. Plant Science 81, 47-56.