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
Linked references
Hide All

This list contains references from the content that can be linked to their source. For a full set of references and notes please see the PDF or HTML where available.

F. Agius , R. Gonzalez-Lamothe , J.L. Caballero , J. Munoz-Blanco , M.A. Botella and V. Valpuesta (2003) Engineering increased vitamin C levels in plants by overexpression of a D -galacturonic acid reductase. Nature Biotechnology 21, 177181.

O. Arrigoni (1994) Ascorbate system in plant development. Journal of Bioenergetics and Biomembranes 26, 407419.

O. Arrigoni and M.C. De Tullio (2000) The role of ascorbic acid in cell metabolism: between gene-directed functions and unpredictable chemical reactions. Journal of Plant Physiology 157, 481488.

O. Arrigoni and M.C. De Tullio (2002) Ascorbic acid: much more than just an antioxidant. Biochimica et Biophysica Acta 1569, 19.

O. Arrigoni , L. De Gara , F. Tommasi and R. Liso (1992) Changes in the ascorbate system during seed development in Vicia faba L. Plant Physiology 99, 235238.

K. Asada (1992) Ascorbate peroxidase: a hydrogen peroxide scavenging system in plants. Physiologia Plantarum 85, 235241.

C.G. Bartoli , G.M. Pastori and C.H. Foyer (2000) Ascorbate biosynthesis in mitochondria is linked to the electron transport chain between complexes III and IV. Plant Physiology 123, 335344.

K.G. Bensch , O. Koerner and W. Lohmann (1981) On a possible mechanism of action of ascorbic acid: formation of ionic bonds with biological molecules. Biochemical and Biophysical Research Communications 101, 312316.

P.C. Bethke , A. Fath , Y.N. Spiegel , Y. Hwang and R.L. Jones (2002) Abscisic acid, gibberellin and cell viability in cereal aleurone. Euphytica 126, 311.

B.H.J. Bielski , A.O. Allen and H.A. Schwarz (1981) Mechanism of disproportionation of ascorbate radicals. Journal of the American Chemical Society 103, 35163518.

L. Britsch (1990) Purification and characterization of flavone synthase I, a 2-oxoglutarate-dependent desaturase. Archives of Biochemistry and Biophysics 282, 152160.

L. Britsch , J. Dedio , H. Saedler and G. Forkmann (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.

I. Cakmak , D. Strbac and H. Marschner (1993) Activities of hydrogen peroxide-scavenging enzymes in germinating wheat seeds. Journal of Experimental Botany 44, 127132.

S. Citterio , S. Sgorbati , S. Scippa and E. Sparvoli (1994) Ascorbic acid effect on the onset of cell proliferation in pea root. Physiologia Plantarum 92, 601607.

M.W. Davey , C. Gilot , G. Persiau , J. Ostergaard , Y. Han , G.C. Bauw , M.C. Van Montagu (1999) Ascorbate biosynthesis in Arabidopsis cell suspension culture. Plant Physiology 121, 535543.

M.B. Davies , J. Austin , D.A. Partridge (1991) Vitamin C: Its chemistry and biochemistry. Cambridge, The Royal Society of Chemistry.

L. De Gara , C. Paciolla , R. Liso , A. Stefani and O. Arrigoni (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.

L. de De Gara , M.C. Pinto and O. Arrigoni (1997) Ascorbate synthesis and ascorbate peroxidase activity during the early stage of wheat germination. Physiologia Plantarum 100, 894900.

L. De Gara , C. Paciolla , M.C. De Tullio , M. Motto and O. Arrigoni (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.

L. De Gara , M.C. de Pinto , V.M.C. Moliterni , M.G. D'Egidio (2003) Redox regulation and storage processes during maturation in kernels of Triticum durum. Journal of Experimental Botany 54, 249258.

L. De Jong and A. Kemp (1984) Stoichiometry and kinetics of the prolyl 4-hydroxylase partial reaction. Biochimica et Biophysica Acta 787, 105111.

B. Del Bello , E. Maellaro , L. Sugherini , A. Santucci , M. Comporti , A.F. Casini (1994) Purification of NADPH-dependent dehydroascorbate reductase from rat liver and its identification with 3 α-hydroxysteroid dehydrogenase. Biochemical Journal 304, 385390.

S. De Leonardis , N. Dipierro and S. Dipierro (2000) Purification and characterization of an ascorbate peroxidase from potato tuber mitochondria. Plant Physiology and Biochemistry 38, 773779.

M.C. De Tullio , L. De Gara , C. Paciolla and O. Arrigoni (1998) Dehydroascorbate-reducing proteins in maize are induced by the ascorbate biosynthesis inhibitor lycorine. Plant Physiology and Biochemistry 36, 433440.

M.C. De Tullio , C. Paciolla , F. Dalla Vecchia , N. Rascio , S. D'Emerico , L. De Gara , R. Liso and O. Arrigoni (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.

M.C. De Tullio , C. Paciolla and O. Arrigoni (2002) Identification and analysis of proteins sharing dehydroascorbate reductase activity. Biologia Plantarum 45, 145147.

M.C. Djoman , J.F. Neault , S. Hashemi-Fesharaky , H.A. Tajmir-Riahi (1998) RNA–ascorbate interaction. Journal of Biomolecular Structure and Dynamics 15, 11151120.

C. Finnie , S. Melchior , P. Roepstorff and B. Svensson (2002) Proteome analysis of grain filling and seed maturation in barley. Plant Physiology 129, 13081319.

M. Fiorani , R. De Sanctis , F. Scarlatti , L. Vallorani , R. De Bellis , G. Serafini , M. Bianchi and V. Stocchi (2000) Dehydroascorbic acid irreversibly inhibits hexokinase activity. Molecular and Cellular Biochemistry 209, 145153.

V.R. Franceschi and N.M. Tarlyn (2002) L -ascorbic acid is accumulated in source leaf phloem and transported to sink tissues in plants. Plant Physiology 130, 649656.

S. Gatzek , G.L. Wheeler and N. Smirnoff (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.

H. Gawronska , W. Burza , E. Bolesta and S. Malepszy (2000) Zygotic and somatic embryos of cucumber (Cucumis sativus L.) substantially differ in their levels of abscisic acid. Plant Science 157, 129137.

B. Halliwell and J.M.C. Gutteridge (1985) Free radicals in biology and medicine. Oxford, Clarendon Press.

P. Hedden and Y. Kamiya (1997) Gibberellin biosynthesis: enzymes, genes and their regulation. Annual Review of Plant Physiology and Plant Molecular Biology 48, 431460.

A. Jiménez , J.A. Hernández , A.R. Barceló , L.M. Sandalio and F. Sevilla (1998) Mitochondrial and peroxisomal ascorbate peroxidase of pea leaves. Physiologia Plantarum 104, 687692.

H. Kende (1993) Ethylene biosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 44, 283307.

S. Klapheck (1988) Homoglutathione: isolation, quantification and occurrence in legumes. Physiologia Plantarum 74, 727732.

O. Leprince , G.A.F. Hendry , N.M. Atherton and C. Walters-Vertucci (1996) Free radicals and metabolism associated with the acquisition and loss of desiccation tolerance in developing seeds. Biochemical Society Transactions 24, 451455.

R. Liso , G. Calabrese , M.B. Bitonti and O. Arrigoni (1984) Relationship between ascorbic acid and cell division. Experimental Cell Research 150, 314320.

X. Liu , S. Shiomi , A. Nakatsuka , Y. Kubo , R. Nakamura and A. Inaba (1999) Characterization of ethylene biosynthesis associated with ripening in banana fruit. Plant Physiology 121, 12571266.

W. Lukowitz , T.C. Nickle , D.W. Meinke , R.L. Last , P.L. Conklin and C.R. Somerville (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.

A. Majewska-Sawka and E.A. Nothnagel (2000) The multiple roles of arabinogalactan proteins in plant development. Plant Physiology 122, 39.

J.M. May , S. Mendiratta , K.E. Hill and R.F. Burk (1997) Reduction of dehydroascorbate to ascorbate by the selenoenzyme thioredoxin reductase. Journal of Biological Chemistry 272, 2260722610.

S. Morell , H. Follmann , M. De Tullio and I. Häberlein (1997) Dehydroascorbate and dehydroascorbate reductase are phantom indicators of oxidative stress in plants. FEBS Letters 414, 567570.

U.M.N. Murthy , Y.H. Liang , P.P. Kumar and W.Q. Sun (2002) Non-enzymatic protein modification by the Maillard reaction reduces the activities of scavenging enzymes in Vigna radiata. Physiologia Plantarum 115, 213220.

E. Nambara and A. Marion-Poll (2003) ABA action and interactions in seeds. Trends in Plant Science 8, 213217.

P. Navas , J.M. Villalba and F. Cordoba (1994) Ascorbate function at the plasma membrane. Biochimica et Biophysica Acta 1197, 113.

G. Noctor and C.H. Foyer (1998) Ascorbate and glutathione: keeping active oxygen under control. Annual Review of Plant Physiology and Plant Molecular Biology 49, 249279.

C. De Paciolla , M.C. Tullio , A. Chiappetta , A.M. Innocenti , M.B. Bitonti , R. Liso and O. Arrigoni (2001) Short- and long-term effects of dehydroascorbate on Lupinus albus and Allium cepa roots. Plant and Cell Physiology 42, 857863.

J.E. Pallanca and N. Smirnoff (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.

J.E. Pallanca and N. Smirnoff (2000) The control of ascorbic acid synthesis and turnover in pea seedlings. Journal of Experimental Botany 51, 669674.

N.W. Pammenter and P. Berjak (1999) A review of recalcitrant seed physiology in relation to desiccation-tolerance mechanisms. Seed Science Research 9, 1337.

G.M. Pastori , G. Kiddle , J. Antoniw , S. Bernard , S. Veljovic-Jovanovic , P.J. Verrier , G. Noctor and C.H. Foyer (2003) Leaf vitamin C contents modulate plant defense transcripts and regulate genes that control development through hormone signaling. Plant Cell 15, 939951.

J.R. Peng and N.P. Harberd (2002) The role of GA-mediated signalling in the control of seed germination. Current Opinion in Plant Biology 5, 376381.

R.P. Pharis and R.W. King (1985) Gibberellins and reproductive development in seed plants. Annual Review of Plant Physiology 36, 517568.

C. Pinzino , B. Nanni and M. Zandomeneghi (1999) Aging, free radicals, and antioxidants in wheat seeds. Journal of Agricultural and Food Chemistry 47, 13331339.

G. Potters , N. Horemans , R.J. Caubergs and H. Asard (2000) Ascorbate and dehydroascorbate influence cell cycle progression in a tobacco cell suspension. Plant Physiology 124, 1720.

G. Potters , L. De Gara , H. Asard and N. Horemans (2002) Ascorbate and glutathione: guardians of the cell cycle, partners in crime? Plant Physiology and Biochemistry 40, 537548.

A.G. Prescott and P. John (1996) Dioxygenases: molecular structure and role in plant metabolism. Annual Review of Plant Physiology and Plant Molecular Biology 47, 245271.

M.D. Rodriguez-Gacio and A.J. Matilla (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.

M. Seo and T. Koshiba (2002) Complex regulation of ABA biosynthesis in plants. Trends in Plant Science 7, 4148.

S. Shigeoka , T. Ishikawa , M. Tamoi , Y. Miyagawa , T. Takeda , Y. Yabuta and K. Yoshimura (2002) Regulation and function of ascorbate peroxidase isoenzymes. Journal of Experimental Botany 53, 13051319.

T. Shimaoka , A. Yokota and C. Miyake (2000) Purification and characterization of chloroplast dehydroascorbate reductase from spinach leaves. Plant and Cell Physiology 41, 11101118.

D.P. Singh , A.M. Jermakow and S.M. Swain (2002) Gibberellins are required for seed development and pollen tube growth in Arabidopsis. Plant Cell 14, 31333147.

N. Smirnoff (2000) Ascorbic acid: metabolism and functions of a multi-facetted molecule. Current Opinion in Plant Biology 3, 229235.

N. Smirnoff , P.L. Conklin and F.A. Loewus (2001) Biosynthesis of ascorbic acid: A renaissance. Annual Review of Plant Physiology and Plant Molecular Biolog 52, 437467.

J. Sommer-Knudsen , A. Bacic and A.E. Clarke (1998) Hydroxyproline-rich plant glycoproteins. Phytochemistry 47, 483497.

C. Stasolla and E.C. Yeung (1999) Ascorbic acid improves conversion of white spruce somatic embryos. In Vitro Cellular and Developmental Biology – Plant 35, 316319.

C. Stasolla and E.C. Yeung (2001) Ascorbic acid metabolism during white spruce somatic embryo maturation and germination. Physiologia Plantarum 111, 196205.

J.L. Svirbely , A. Szent-Györgyi (1932) Hexuronic acid as the antiscorbutic factor. Nature 129, 576.

A.J. Thompson , A.C. Jackson , R.C. Symonds , B.J. Mulholland , A.R. Dadswell , P.S. Blake , A. Burbidge and I.B. Taylor (2000) Ectopic expression of a tomato 9- cis -epoxycarotenoid dioxygenase gene causes over-production of abscisic acid. Plant Journal 23, 363374.

F. Tommasi , C. Paciolla and O. Arrigoni (1999) The ascorbate system in recalcitrant and orthodox seeds. Physiologia Plantarum 105, 193198.

F. Tommasi , C. Paciolla , M.C. de Pinto and L. De Gara (2001) A comparative study of glutathione and ascorbate metabolism during germination of Pinus pinea L. seeds. Journal of Experimental Botany 52, 16471654.

S. Trümper , H. Follmann and I. Häberlein (1994) A novel dehydroascorbate reductase from spinach chloroplasts homologous to plant trypsin inhibitor. FEBS Letters 352, 159162.

G. Tschank , J. Sanders , K.H. Baringhaus , F. Dallacker , K. Kivirikko and V. Günzler (1994) Structural requirements for the utilization of ascorbate analogs in the prolyl 4-hydroxylase reaction. Biochemical Journal 300, 7579.

J. Urano , T. Nakagawa , Y. Maki , T. Masumura , K. Tanaka , N. Murata and T. Ushimaru (2000) Molecular cloning and characterization of a rice dehydroascorbate reductase. FEBS Letters 466, 107111.

J.G.G. Vethanayagam , E.H. Green , R.C. Rose and A.M. Bode (1999) Glutathione-dependent ascorbate recycling activity of rat serum albumin. Free Radical Biology and Medicine 26, 15911598.

M.P. Washburn and W.W. Wells (1999) Identification of the dehydroascorbic acid reductase and thioltransferase (glutaredoxin) activities of bovine erythrocyte glutathione peroxidase. Biochemical and Biophysical Research Communications 257, 567571.

H. Weber , L. Borisjuk and U. Wobus (1997) Sugar import and metabolism during seed development. Trends in Plant Science 2, 169174.

J.X. Wilson (2002) The physiological role of dehydroascorbic acid. FEBS Letters 527, 59.

P. Wojtaszek , C.G. Smith and G.P. Bolwell (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.

B.A. Wolucka , G. Persiau , J. Van Doorsselaere , M.W. Davey , H. Demol , J. Vandekerckhove , M. Van Montagu , M. Zabeau and W. Boerjan (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.

H.H. Woo and M.C. Hawes (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.

M. Wu , H.S. Moon , A. Pirskanen , J. Myllyharju , K.I. Kivirikko and T.P. Begley (2000) Mechanistic studies on prolyl-4-hydroxylase: the vitamin C requiring uncoupled oxidation. Bioorganic and Medicinal Chemistry Letters 10, 15111514.

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: 26 *
Loading metrics...

Abstract views

Total abstract views: 175 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 28th May 2017. This data will be updated every 24 hours.