Skip to main content
×
Home
    • Aa
    • Aa

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

  • Mario C. De Tullio (a1) and Oreste Arrigoni (a1)
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.

Copyright
Corresponding author
*Correspondence Fax: +39 080 5442155 Email: detullio@botanica.uniba.it
References
Hide All
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, 177181.
Arrigoni O. (1994) Ascorbate system in plant development. Journal of Bioenergetics and Biomembranes 26, 407419.
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, 481488.
Arrigoni O. and De Tullio M.C. (2002) Ascorbic acid: much more than just an antioxidant. Biochimica et Biophysica Acta 1569, 19.
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, 235238.
Asada K. (1992) Ascorbate peroxidase: a hydrogen peroxide scavenging system in plants. Physiologia Plantarum 85, 235241.
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, 701708.
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, 335344.
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, 312316.
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, 311.
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, 35163518.
Britsch L. (1990) Purification and characterization of flavone synthase I, a 2-oxoglutarate-dependent desaturase. Archives of Biochemistry and Biophysics 282, 152160.
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, 745754.
Cakmak I., Strbac D. and Marschner H. (1993) Activities of hydrogen peroxide-scavenging enzymes in germinating wheat seeds. Journal of Experimental Botany 44, 127132.
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, 601607.
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, 329339.
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, 535543.
Davies M.B., Austin J., Partridge D.A. (1991) Vitamin C: Its chemistry and biochemistry. Cambridge, The Royal Society of Chemistry.
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, 959965.
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, 697700.
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, 894900.
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, 713.
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, 249258.
De Jong L. and Kemp A. (1984) Stoichiometry and kinetics of the prolyl 4-hydroxylase partial reaction. Biochimica et Biophysica Acta 787, 105111.
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, 385390.
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, 773779.
De Tullio M.C. (2003) How does ascorbic acid prevent scurvy? A survey of the nonantioxidant functions of vitamin C. pp. 159171in Asard H.;May J.M. and Smirnoff N. (Eds) Vitamin C, its function and biochemistry in animals and plants. Abingdon, UK, Bios Scientific Publishers.
De Tullio M.C. and Arrigoni O. (2003) Hopes, disillusions and more hopes from vitamin C. Cellular and Molecular Life Sciences (in press).
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, 433440.
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, 424434.
De Tullio M.C., Paciolla C. and Arrigoni O. (2002) Identification and analysis of proteins sharing dehydroascorbate reductase activity. Biologia Plantarum 45, 145147.
Djoman M.C., Neault J.F., Hashemi-Fesharaky S., Tajmir-Riahi H.A. (1998) RNA–ascorbate interaction. Journal of Biomolecular Structure and Dynamics 15, 11151120.
Finnie C., Melchior S., Roepstorff P. and Svensson B. (2002) Proteome analysis of grain filling and seed maturation in barley. Plant Physiology 129, 13081319.
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, 145153.
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, 649656.
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, 541553.
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, 129137.
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, 777783.
Halliwell B. and Gutteridge J.M.C. (1985) Free radicals in biology and medicine. Oxford, Clarendon Press.
Hedden P. and Kamiya Y. (1997) Gibberellin biosynthesis: enzymes, genes and their regulation. Annual Review of Plant Physiology and Plant Molecular Biology 48, 431460.
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, 521525.
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, 687692.
Kende H. (1993) Ethylene biosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 44, 283307.
Klapheck S. (1988) Homoglutathione: isolation, quantification and occurrence in legumes. Physiologia Plantarum 74, 727732.
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, 10051013.
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, 211218.
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, 451455.
Liso R., Calabrese G., Bitonti M.B. and Arrigoni O. (1984) Relationship between ascorbic acid and cell division. Experimental Cell Research 150, 314320.
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, 12571266.
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, 22622267.
Majewska-Sawka A. and Nothnagel E.A. (2000) The multiple roles of arabinogalactan proteins in plant development. Plant Physiology 122, 39.
Marx C., Wong J.H. and Buchanan B.B. (2003) Thioredoxin and germinating barley: targets and protein redox changes. Planta 216, 454460.
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, 2260722610.
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, 567570.
Müntz K. (1981) Seed development. Encyclopedia of Plant Physiology 14A, 505558.
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, 213220.
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, 54035405.
Nambara E. and Marion-Poll A. (2003) ABA action and interactions in seeds. Trends in Plant Science 8, 213217.
Navas P., Villalba J.M. and Cordoba F. (1994) Ascorbate function at the plasma membrane. Biochimica et Biophysica Acta 1197, 113.
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, 249279.
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, 857863.
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, 453461.
Pallanca J.E. and Smirnoff N. (2000) The control of ascorbic acid synthesis and turnover in pea seedlings. Journal of Experimental Botany 51, 669674.
Pammenter N.W. and Berjak P. (1999) A review of recalcitrant seed physiology in relation to desiccation-tolerance mechanisms. Seed Science Research 9, 1337.
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, 939951.
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, 376381.
Pharis R.P. and King R.W. (1985) Gibberellins and reproductive development in seed plants. Annual Review of Plant Physiology 36, 517568.
Pinzino C., Nanni B. and Zandomeneghi M. (1999) Aging, free radicals, and antioxidants in wheat seeds. Journal of Agricultural and Food Chemistry 47, 13331339.
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, 1720.
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, 537548.
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, 245271.
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, 273279.
Seo M. and Koshiba T. (2002) Complex regulation of ABA biosynthesis in plants. Trends in Plant Science 7, 4148.
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, 13051319.
Shimaoka T., Yokota A. and Miyake C. (2000) Purification and characterization of chloroplast dehydroascorbate reductase from spinach leaves. Plant and Cell Physiology 41, 11101118.
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, 31333147.
Smirnoff N. (2000) Ascorbic acid: metabolism and functions of a multi-facetted molecule. Current Opinion in Plant Biology 3, 229235.
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, 437467.
Sommer-Knudsen J., Bacic A. and Clarke A.E. (1998) Hydroxyproline-rich plant glycoproteins. Phytochemistry 47, 483497.
Stasolla C. and Yeung E.C. (1999) Ascorbic acid improves conversion of white spruce somatic embryos. In Vitro Cellular and Developmental Biology – Plant 35, 316319.
Stasolla C. and Yeung E.C. (2001) Ascorbic acid metabolism during white spruce somatic embryo maturation and germination. Physiologia Plantarum 111, 196205.
Svirbely J.L., Szent-Györgyi A. (1932) Hexuronic acid as the antiscorbutic factor. Nature 129, 576.
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, 363374.
Tommasi F., Paciolla C. and Arrigoni O. (1999) The ascorbate system in recalcitrant and orthodox seeds. Physiologia Plantarum 105, 193198.
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, 16471654.
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. 209213in Acosta M.;Rodriguez Lopez J.N.;Pedreño M.A. (Eds) Plant peroxidases, biochemistry and physiology. Spain, University of Murcia.
Trümper S., Follmann H. and Häberlein I. (1994) A novel dehydroascorbate reductase from spinach chloroplasts homologous to plant trypsin inhibitor. FEBS Letters 352, 159162.
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, 7579.
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, 107111.
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, 15911598.
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, 567571.
Weber H., Borisjuk L. and Wobus U. (1997) Sugar import and metabolism during seed development. Trends in Plant Science 2, 169174.
Wheeler G.L., Jones M.A. and Smirnoff N. (1998) The biosynthetic pathway of vitamin C in higher plants. Nature 393, 365369.
Wilson J.X. (2002) The physiological role of dehydroascorbic acid. FEBS Letters 527, 59.
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, 463477.
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, 1484314848.
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, 10451051.
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, 15111514.
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, 415423.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Seed Science Research
  • ISSN: 0960-2585
  • EISSN: 1475-2735
  • URL: /core/journals/seed-science-research
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords:

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 33 *
Loading metrics...

Abstract views

Total abstract views: 302 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 24th October 2017. This data will be updated every 24 hours.