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The ascorbic acid system in seeds: to protect and to serve

Published online by Cambridge University Press:  22 February 2007

Mario C. De Tullio  and
Oreste Arrigoni
Mario C. De Tullio*
Affiliation:
Dipartimento di Biologia e Patologia Vegetale, Università di Bari, Via E. Orabona 4, Bari, I-70125, Italy
Oreste Arrigoni
Affiliation:
Dipartimento di Biologia e Patologia Vegetale, Università di Bari, Via E. Orabona 4, Bari, I-70125, Italy
*
*Correspondence Fax: +39 080 5442155 Email: detullio@botanica.uniba.it
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Abstract

The ascorbic acid (ASC) system functions dynamically in seeds, although the strategies for ASC production and utilization may vary according to seed developmental and functional stages. In orthodox seeds, ASC content and ASC peroxidase activity increase during the early stages of development, then decrease during the desiccation stage, so that, at quiescence, seeds have neither ASC nor ASC peroxidase, but retain a small amount of dehydroascorbic acid (DHA) and significant activities of ASC recycling enzymes. ASC and ASC peroxidase activity re-start after a few hours from the onset of imbibition. In contrast, the ASC system is little affected during germination of recalcitrant seeds. Although the presence of the ASC system in seeds has often been considered only within the framework of seed antioxidant defences, ASC function in seeds is also likely to be related to its action as a specific co-substrate required for the activity of dioxygenases (e.g. 1-aminocyclopropane carboxylate oxidase, gibberellic acid hydroxylases and 9-cis-epoxycarotenoid dioxygenases) involved in the synthesis of ethylene, gibberellins and abscisic acid, respectively. The possible role of ASC in coordinating the activities of these key enzymes is discussed.

Keywords

ascorbic aciddioxygenasesdehydroascorbic acidembryogenesisplant hormonesseed developmentseed germination
Type
Invited Review and Research Opinion
Information
Seed Science Research , Volume 13 , Issue 4 , December 2003 , pp. 249 - 260
Copyright
Copyright © Cambridge University Press 2003

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References

Agius, F., Gonzalez-Lamothe, R., Caballero, J.L., Munoz-Blanco, J., Botella, M.A. and Valpuesta, V. (2003) Engineering increased vitamin C levels in plants by overexpression of a D -galacturonic acid reductase. Nature Biotechnology 21, 177–181.CrossRefGoogle ScholarPubMed
Arrigoni, O. (1994) Ascorbate system in plant development. Journal of Bioenergetics and Biomembranes 26, 407–419.CrossRefGoogle ScholarPubMed
Arrigoni, O. and De Tullio, M.C. (2000) The role of ascorbic acid in cell metabolism: between gene-directed functions and unpredictable chemical reactions. Journal of Plant Physiology 157, 481–488.CrossRefGoogle Scholar
Arrigoni, O. and De Tullio, M.C. (2002) Ascorbic acid: much more than just an antioxidant. Biochimica et Biophysica Acta 1569, 1–9.CrossRefGoogle ScholarPubMed
Arrigoni, O., De Gara, L., Tommasi, F. and Liso, R. (1992) Changes in the ascorbate system during seed development in Vicia faba L. Plant Physiology 99, 235–238.CrossRefGoogle ScholarPubMed
Asada, K. (1992) Ascorbate peroxidase: a hydrogen peroxide scavenging system in plants. Physiologia Plantarum 85, 235–241.CrossRefGoogle Scholar
Bailly, C., Audigier, C., Ladonne, F., Wagner, M.H., Coste, F., Corbineau, F. and Côme, D. (2001) Changes in oligosaccharide content and antioxidant enzyme activities in developing bean seeds as related to acquisition of drying tolerance and seed quality. Journal of Experimental Botany 52, 701–708.CrossRefGoogle ScholarPubMed
Bartoli, C.G., Pastori, G.M. and Foyer, C.H. (2000) Ascorbate biosynthesis in mitochondria is linked to the electron transport chain between complexes III and IV. Plant Physiology 123, 335–344.CrossRefGoogle Scholar
Bensch, K.G., Koerner, O. and Lohmann, W. (1981) On a possible mechanism of action of ascorbic acid: formation of ionic bonds with biological molecules. Biochemical and Biophysical Research Communications 101, 312–316.CrossRefGoogle ScholarPubMed
Bethke, P.C., Fath, A., Spiegel, Y.N., Hwang, Y. and Jones, R.L. (2002) Abscisic acid, gibberellin and cell viability in cereal aleurone. Euphytica 126, 3–11.CrossRefGoogle Scholar
Bielski, B.H.J., Allen, A.O. and Schwarz, H.A. (1981) Mechanism of disproportionation of ascorbate radicals. Journal of the American Chemical Society 103, 3516–3518.CrossRefGoogle Scholar
Britsch, L. (1990) Purification and characterization of flavone synthase I, a 2-oxoglutarate-dependent desaturase. Archives of Biochemistry and Biophysics 282, 152–160.CrossRefGoogle ScholarPubMed
Britsch, L., Dedio, J., Saedler, H. and Forkmann, G. (1993) Molecular characterization of flavanone 3β-hydroxylases. Consensus sequence, comparison with related enzymes and the role of conserved histidine residues. European Journal of Biochemistry 217, 745–754.CrossRefGoogle Scholar
Cakmak, I., Strbac, D. and Marschner, H. (1993) Activities of hydrogen peroxide-scavenging enzymes in germinating wheat seeds. Journal of Experimental Botany 44, 127–132.CrossRefGoogle Scholar
Citterio, S., Sgorbati, S., Scippa, S. and Sparvoli, E. (1994) Ascorbic acid effect on the onset of cell proliferation in pea root. Physiologia Plantarum 92, 601–607.CrossRefGoogle Scholar
Corbineau, F., Picard, M.A., Fougereux, J-A., Ladonne, F., Côme, D. (2000) Effects of dehydration conditions on desiccation tolerance of developing pea seeds as related to oligosaccharide content and cell membrane properties. Seed Science Research 10, 329–339.CrossRefGoogle Scholar
Davey, M.W., Gilot, C., Persiau, G., Ostergaard, J., Han, Y., Bauw, G.C., Van Montagu, M.C. (1999) Ascorbate biosynthesis in Arabidopsis cell suspension culture. Plant Physiology 121, 535–543.CrossRefGoogle ScholarPubMed
Davies, M.B., Austin, J., Partridge, D.A. (1991) Vitamin C: Its chemistry and biochemistry. Cambridge, The Royal Society of Chemistry.Google Scholar
De Gara, L., Tommasi, F., Liso, R. and Arrigoni, O. (1989) Ascorbic acid as a factor controlling ‘in vivo’ its biosynthetic pathway. Bollettino della Società Italiana di Biologia Sperimentale 65, 959–965.Google ScholarPubMed
De Gara, L., Paciolla, C., Liso, R., Stefani, A. and Arrigoni, O. (1991) Correlation between ascorbate peroxidase activity and some anomalies of seedlings from aged caryopses of Dasypyrum villosum (L.) Borb. Journal of Plant Physiology 137, 697–700.CrossRefGoogle Scholar
De Gara, L. de, Pinto, M.C. and Arrigoni, O. (1997) Ascorbate synthesis and ascorbate peroxidase activity during the early stage of wheat germination. Physiologia Plantarum 100, 894–900.CrossRefGoogle Scholar
De Gara, L., Paciolla, C., De Tullio, M.C., Motto, M. and 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.CrossRefGoogle Scholar
De Gara, L., de Pinto, M.C., Moliterni, V.M.C., D'Egidio, M.G. (2003) Redox regulation and storage processes during maturation in kernels of Triticum durum. Journal of Experimental Botany 54, 249–258.CrossRefGoogle ScholarPubMed
De Jong, L. and Kemp, A. (1984) Stoichiometry and kinetics of the prolyl 4-hydroxylase partial reaction. Biochimica et Biophysica Acta 787, 105–111.CrossRefGoogle Scholar
Del Bello, B., Maellaro, E., Sugherini, L., Santucci, A., Comporti, M., Casini, A.F. (1994) Purification of NADPH-dependent dehydroascorbate reductase from rat liver and its identification with 3 α-hydroxysteroid dehydrogenase. Biochemical Journal 304, 385–390.CrossRefGoogle ScholarPubMed
De Leonardis, S., Dipierro, N. and Dipierro, S. (2000) Purification and characterization of an ascorbate peroxidase from potato tuber mitochondria. Plant Physiology and Biochemistry 38, 773–779.CrossRefGoogle Scholar
De Tullio, M.C. (2003) How does ascorbic acid prevent scurvy? A survey of the nonantioxidant functions of vitamin C. pp. 159–171in Asard, H.;May, J.M. and Smirnoff, N. (Eds) Vitamin C, its function and biochemistry in animals and plants. Abingdon, UK, Bios Scientific Publishers.Google Scholar
De Tullio, M.C. and Arrigoni, O. (2003) Hopes, disillusions and more hopes from vitamin C. Cellular and Molecular Life Sciences (in press).CrossRefGoogle Scholar
De Tullio, M.C., De Gara, L., Paciolla, C. and Arrigoni, O. (1998) Dehydroascorbate-reducing proteins in maize are induced by the ascorbate biosynthesis inhibitor lycorine. Plant Physiology and Biochemistry 36, 433–440.CrossRefGoogle Scholar
De Tullio, M.C., Paciolla, C., Dalla Vecchia, F., Rascio, N., D'Emerico, S., De Gara, L., Liso, R. and 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.CrossRefGoogle Scholar
De Tullio, M.C., Paciolla, C. and Arrigoni, O. (2002) Identification and analysis of proteins sharing dehydroascorbate reductase activity. Biologia Plantarum 45, 145–147.CrossRefGoogle Scholar
Djoman, M.C., Neault, J.F., Hashemi-Fesharaky, S., Tajmir-Riahi, H.A. (1998) RNA–ascorbate interaction. Journal of Biomolecular Structure and Dynamics 15, 1115–1120.CrossRefGoogle ScholarPubMed
Finnie, C., Melchior, S., Roepstorff, P. and Svensson, B. (2002) Proteome analysis of grain filling and seed maturation in barley. Plant Physiology 129, 1308–1319.CrossRefGoogle ScholarPubMed
Fiorani, M., De Sanctis, R., Scarlatti, F., Vallorani, L., De Bellis, R., Serafini, G., Bianchi, M. and Stocchi, V. (2000) Dehydroascorbic acid irreversibly inhibits hexokinase activity. Molecular and Cellular Biochemistry 209, 145–153.CrossRefGoogle ScholarPubMed
Franceschi, V.R. and Tarlyn, N.M. (2002) L -ascorbic acid is accumulated in source leaf phloem and transported to sink tissues in plants. Plant Physiology 130, 649–656.CrossRefGoogle ScholarPubMed
Gatzek, S., Wheeler, G.L. and Smirnoff, N. (2002) 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 Journal 30, 541–553.CrossRefGoogle ScholarPubMed
Gawronska, H., Burza, W., Bolesta, E. and Malepszy, S. (2000) Zygotic and somatic embryos of cucumber (Cucumis sativus L.) substantially differ in their levels of abscisic acid. Plant Science 157, 129–137.CrossRefGoogle ScholarPubMed
Gobin, P., Ng, P.K.W., Buchanan, B.B. and Kobrehel, K. (1997) Sulfhydryl–disulfide changes in proteins of developing wheat grain. Plant Physiology and Biochemistry 35, 777–783.Google Scholar
Halliwell, B. and Gutteridge, J.M.C. (1985) Free radicals in biology and medicine. Oxford, Clarendon Press.Google Scholar
Hedden, P. and Kamiya, Y. (1997) Gibberellin biosynthesis: enzymes, genes and their regulation. Annual Review of Plant Physiology and Plant Molecular Biology 48, 431–460.CrossRefGoogle ScholarPubMed
Innocenti, A.M., Mazzuca, S., Bitonti, M.B., De Gara, L., Liso, R. and Arrigoni, O. (1994) Endogenous rhythm of ascorbic acid in seedling roots of broad bean. Plant Physiology and Biochemistry 32, 521–525.Google Scholar
Jiménez, A., Hernández, J.A., Barceló, A.R., Sandalio, L.M. and Sevilla, F. (1998) Mitochondrial and peroxisomal ascorbate peroxidase of pea leaves. Physiologia Plantarum 104, 687–692.CrossRefGoogle Scholar
Kende, H. (1993) Ethylene biosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 44, 283–307.CrossRefGoogle Scholar
Klapheck, S. (1988) Homoglutathione: isolation, quantification and occurrence in legumes. Physiologia Plantarum 74, 727–732.CrossRefGoogle Scholar
Klapheck, S., Zimmer, I. and Cosse, H. (1990) Scavenging of hydrogen peroxide in the endosperm of Ricinus communis by ascorbate peroxidase. Plant and Cell Physiology 31, 1005–1013.Google Scholar
Leprince, O., Hendry, G.A.F. and Atherton, N.M. (1994) Free radical processes induced by desiccation in germinating maize. The relationship with respiration and loss of desiccation tolerance. Proceedings of the Royal Society of Edinburgh 102, 211–218.Google Scholar
Leprince, O., Hendry, G.A.F., Atherton, N.M. and Walters-Vertucci, C. (1996) Free radicals and metabolism associated with the acquisition and loss of desiccation tolerance in developing seeds. Biochemical Society Transactions 24, 451–455.CrossRefGoogle ScholarPubMed
Liso, R., Calabrese, G., Bitonti, M.B. and Arrigoni, O. (1984) Relationship between ascorbic acid and cell division. Experimental Cell Research 150, 314–320.CrossRefGoogle ScholarPubMed
Liu, X., Shiomi, S., Nakatsuka, A., Kubo, Y., Nakamura, R. and Inaba, A. (1999) Characterization of ethylene biosynthesis associated with ripening in banana fruit. Plant Physiology 121, 1257–1266.CrossRefGoogle ScholarPubMed
Lukowitz, W., Nickle, T.C., Meinke, D.W., Last, R.L., Conklin, P.L. and Somerville, C.R. (2001) Arabidopsis cyt1 mutants are deficient in a mannose-1-phosphate guanylyltransferase and point to a requirement of N-linked glycosylation for cellulose biosynthesis. Proceedings of the National Academy of Sciences, USA 98, 2262–2267.CrossRefGoogle Scholar
Majewska-Sawka, A. and Nothnagel, E.A. (2000) The multiple roles of arabinogalactan proteins in plant development. Plant Physiology 122, 3–9.CrossRefGoogle ScholarPubMed
Marx, C., Wong, J.H. and Buchanan, B.B. (2003) Thioredoxin and germinating barley: targets and protein redox changes. Planta 216, 454–460.CrossRefGoogle ScholarPubMed
May, J.M., Mendiratta, S., Hill, K.E. and Burk, R.F. (1997) Reduction of dehydroascorbate to ascorbate by the selenoenzyme thioredoxin reductase. Journal of Biological Chemistry 272, 22607–22610.CrossRefGoogle ScholarPubMed
Morell, S., Follmann, H., De Tullio, M. and Häberlein, I. (1997) Dehydroascorbate and dehydroascorbate reductase are phantom indicators of oxidative stress in plants. FEBS Letters 414, 567–570.CrossRefGoogle ScholarPubMed
Müntz, K. (1981) Seed development. Encyclopedia of Plant Physiology 14A, 505–558.Google Scholar
Murthy, U.M.N., Liang, Y.H., Kumar, P.P. and Sun, W.Q. (2002) Non-enzymatic protein modification by the Maillard reaction reduces the activities of scavenging enzymes in Vigna radiata. Physiologia Plantarum 115, 213–220.CrossRefGoogle ScholarPubMed
Myllyla, R., Majamaa, K., Günzler, V., Hanauske-Abel, H.M. and Kivirikko, K.I. (1984) Ascorbate is consumed stoichiometrically in the uncoupled reactions catalyzed by prolyl 4-hydroxylase and lysyl hydroxylase. Journal of Biological Chemistry 259, 5403–5405.CrossRefGoogle ScholarPubMed
Nambara, E. and Marion-Poll, A. (2003) ABA action and interactions in seeds. Trends in Plant Science 8, 213–217.CrossRefGoogle ScholarPubMed
Navas, P., Villalba, J.M. and Cordoba, F. (1994) Ascorbate function at the plasma membrane. Biochimica et Biophysica Acta 1197, 1–13.CrossRefGoogle ScholarPubMed
Noctor, G. and Foyer, C.H. (1998) Ascorbate and glutathione: keeping active oxygen under control. Annual Review of Plant Physiology and Plant Molecular Biology 49, 249–279.CrossRefGoogle ScholarPubMed
Paciolla, C. De, Tullio, M.C., Chiappetta, A., Innocenti, A.M., Bitonti, M.B., Liso, R. and Arrigoni, O. (2001) Short- and long-term effects of dehydroascorbate on Lupinus albus and Allium cepa roots. Plant and Cell Physiology 42, 857–863.CrossRefGoogle Scholar
Pallanca, J.E. and Smirnoff, N. (1999) Ascorbic acid metabolism in pea seedlings. A comparison of D -glucosone, L -sorbosone, and L -galactono-1,4-lactone as ascorbate precursors. Plant Physiology 120, 453–461.CrossRefGoogle ScholarPubMed
Pallanca, J.E. and Smirnoff, N. (2000) The control of ascorbic acid synthesis and turnover in pea seedlings. Journal of Experimental Botany 51, 669–674.CrossRefGoogle ScholarPubMed
Pammenter, N.W. and Berjak, P. (1999) A review of recalcitrant seed physiology in relation to desiccation-tolerance mechanisms. Seed Science Research 9, 13–37.CrossRefGoogle Scholar
Pastori, G.M., Kiddle, G., Antoniw, J., Bernard, S., Veljovic-Jovanovic, S., Verrier, P.J., Noctor, G. and Foyer, C.H. (2003) Leaf vitamin C contents modulate plant defense transcripts and regulate genes that control development through hormone signaling. Plant Cell 15, 939–951.CrossRefGoogle ScholarPubMed
Peng, J.R. and Harberd, N.P. (2002) The role of GA-mediated signalling in the control of seed germination. Current Opinion in Plant Biology 5, 376–381.CrossRefGoogle ScholarPubMed
Pharis, R.P. and King, R.W. (1985) Gibberellins and reproductive development in seed plants. Annual Review of Plant Physiology 36, 517–568.CrossRefGoogle Scholar
Pinzino, C., Nanni, B. and Zandomeneghi, M. (1999) Aging, free radicals, and antioxidants in wheat seeds. Journal of Agricultural and Food Chemistry 47, 1333–1339.CrossRefGoogle ScholarPubMed
Potters, G., Horemans, N., Caubergs, R.J. and Asard, H. (2000) Ascorbate and dehydroascorbate influence cell cycle progression in a tobacco cell suspension. Plant Physiology 124, 17–20.CrossRefGoogle Scholar
Potters, G., De Gara, L., Asard, H. and Horemans, N. (2002) Ascorbate and glutathione: guardians of the cell cycle, partners in crime? Plant Physiology and Biochemistry 40, 537–548.CrossRefGoogle Scholar
Prescott, A.G. and John, P. (1996) Dioxygenases: molecular structure and role in plant metabolism. Annual Review of Plant Physiology and Plant Molecular Biology 47, 245–271.CrossRefGoogle ScholarPubMed
Rodriguez-Gacio, M.D. and Matilla, A.J. (2001) The last step of the ethylene biosynthesis pathway in turnip tops (Brassica rapa) seeds: Alterations related to development and germination and its inhibition during desiccation. Physiologia Plantarum 112, 273–279.CrossRefGoogle Scholar
Seo, M. and Koshiba, T. (2002) Complex regulation of ABA biosynthesis in plants. Trends in Plant Science 7, 41–48.CrossRefGoogle ScholarPubMed
Shigeoka, S., Ishikawa, T., Tamoi, M., Miyagawa, Y., Takeda, T., Yabuta, Y. and Yoshimura, K. (2002) Regulation and function of ascorbate peroxidase isoenzymes. Journal of Experimental Botany 53, 1305–1319.CrossRefGoogle ScholarPubMed
Shimaoka, T., Yokota, A. and Miyake, C. (2000) Purification and characterization of chloroplast dehydroascorbate reductase from spinach leaves. Plant and Cell Physiology 41, 1110–1118.CrossRefGoogle ScholarPubMed
Singh, D.P., Jermakow, A.M. and Swain, S.M. (2002) Gibberellins are required for seed development and pollen tube growth in Arabidopsis. Plant Cell 14, 3133–3147.CrossRefGoogle ScholarPubMed
Smirnoff, N. (2000) Ascorbic acid: metabolism and functions of a multi-facetted molecule. Current Opinion in Plant Biology 3, 229–235.CrossRefGoogle ScholarPubMed
Smirnoff, N., Conklin, P.L. and Loewus, F.A. (2001) Biosynthesis of ascorbic acid: A renaissance. Annual Review of Plant Physiology and Plant Molecular Biolog 52, 437–467.CrossRefGoogle ScholarPubMed
Sommer-Knudsen, J., Bacic, A. and Clarke, A.E. (1998) Hydroxyproline-rich plant glycoproteins. Phytochemistry 47, 483–497.CrossRefGoogle Scholar
Stasolla, C. and Yeung, E.C. (1999) Ascorbic acid improves conversion of white spruce somatic embryos. In Vitro Cellular and Developmental Biology – Plant 35, 316–319.CrossRefGoogle Scholar
Stasolla, C. and Yeung, E.C. (2001) Ascorbic acid metabolism during white spruce somatic embryo maturation and germination. Physiologia Plantarum 111, 196–205.CrossRefGoogle Scholar
Svirbely, J.L., Szent-Györgyi, A. (1932) Hexuronic acid as the antiscorbutic factor. Nature 129, 576.CrossRefGoogle Scholar
Thompson, A.J., Jackson, A.C., Symonds, R.C., Mulholland, B.J., Dadswell, A.R., Blake, P.S., Burbidge, A. and Taylor, I.B. (2000) Ectopic expression of a tomato 9- cis -epoxycarotenoid dioxygenase gene causes over-production of abscisic acid. Plant Journal 23, 363–374.CrossRefGoogle ScholarPubMed
Tommasi, F., Paciolla, C. and Arrigoni, O. (1999) The ascorbate system in recalcitrant and orthodox seeds. Physiologia Plantarum 105, 193–198.CrossRefGoogle Scholar
Tommasi, F., Paciolla, C., de Pinto, M.C. and 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.CrossRefGoogle ScholarPubMed
Tommasi, F., Paciolla, C., de Pinto, M.C. and De Gara, L. (2002) Relationships between water levels and ascorbate peroxidase–ascorbate recycling enzymes in recalcitrant and orthodox seeds. pp. 209–213in Acosta, M.;Rodriguez Lopez, J.N.;Pedreño, M.A. (Eds) Plant peroxidases, biochemistry and physiology. Spain, University of Murcia.Google Scholar
Trümper, S., Follmann, H. and Häberlein, I. (1994) A novel dehydroascorbate reductase from spinach chloroplasts homologous to plant trypsin inhibitor. FEBS Letters 352, 159–162.CrossRefGoogle ScholarPubMed
Tschank, G., Sanders, J., Baringhaus, K.H., Dallacker, F., Kivirikko, K. and Günzler, V. (1994) Structural requirements for the utilization of ascorbate analogs in the prolyl 4-hydroxylase reaction. Biochemical Journal 300, 75–79.CrossRefGoogle ScholarPubMed
Urano, J., Nakagawa, T., Maki, Y., Masumura, T., Tanaka, K., Murata, N. and Ushimaru, T. (2000) Molecular cloning and characterization of a rice dehydroascorbate reductase. FEBS Letters 466, 107–111.CrossRefGoogle ScholarPubMed
Vethanayagam, J.G.G., Green, E.H., Rose, R.C. and Bode, A.M. (1999) Glutathione-dependent ascorbate recycling activity of rat serum albumin. Free Radical Biology and Medicine 26, 1591–1598.CrossRefGoogle ScholarPubMed
Washburn, M.P. and Wells, W.W. (1999) Identification of the dehydroascorbic acid reductase and thioltransferase (glutaredoxin) activities of bovine erythrocyte glutathione peroxidase. Biochemical and Biophysical Research Communications 257, 567–571.CrossRefGoogle ScholarPubMed
Weber, H., Borisjuk, L. and Wobus, U. (1997) Sugar import and metabolism during seed development. Trends in Plant Science 2, 169–174.CrossRefGoogle Scholar
Wheeler, G.L., Jones, M.A. and Smirnoff, N. (1998) The biosynthetic pathway of vitamin C in higher plants. Nature 393, 365–369.CrossRefGoogle ScholarPubMed
Wilson, J.X. (2002) The physiological role of dehydroascorbic acid. FEBS Letters 527, 5–9.CrossRefGoogle ScholarPubMed
Wojtaszek, P., Smith, C.G. and Bolwell, G.P. (1999) Ultrastructural localisation and further biochemical characterisation of prolyl-4-hydroxylase from Phaseolus vulgaris: comparative analysis. International Journal of Biochemistry and Cell Biology 31, 463–477.CrossRefGoogle ScholarPubMed
Wolucka, B.A., Persiau, G., Van Doorsselaere, J., Davey, M.W., Demol, H., Vandekerckhove, J., Van Montagu, M., Zabeau, M. and Boerjan, W. (2001) Partial purification and identification of GDP-mannose 3',5'-epimerase of Arabidopsis thaliana, a key enzyme of the plant vitamin C pathway. Proceedings of the National Academy of Sciences, USA 98, 14843–14848.CrossRefGoogle ScholarPubMed
Woo, H.H. and Hawes, M.C. (1997) Cloning of genes whose expression is correlated with mitosis and localized in dividing cells in root caps of Pisum sativum L. Plant Molecular Biology 35, 1045–1051.CrossRefGoogle ScholarPubMed
Wu, M., Moon, H.S., Pirskanen, A., Myllyharju, J., Kivirikko, K.I. and Begley, T.P. (2000) Mechanistic studies on prolyl-4-hydroxylase: the vitamin C requiring uncoupled oxidation. Bioorganic and Medicinal Chemistry Letters 10, 1511–1514.CrossRefGoogle ScholarPubMed
Zacheo, G., Cappello, M.S., Gallo, A., Santino, A. and Cappello, A.R. (2000) Changes associated with post-harvest ageing in almond seeds. Food Science and Technology 33, 415–423.Google Scholar