Skip to main content
Log in

Ascorbate system in plant development

  • Published:
Journal of Bioenergetics and Biomembranes Aims and scope Submit manuscript

    We’re sorry, something doesn't seem to be working properly.

    Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.

Abstract

By using lycorine, a specific inhibitor of ascorbate biosynthesis, it was possible to demonstrate that plant cells consume a high quantity of ascorbate (AA). Thein vivo metabolic reactions utilizing ascorbate are the elimination of H2O2 by ascorbate peroxidase and the hydroxylation of proline residues present in the polypeptide chains by means of peptidyl-proline hydroxylase.

Ascorbate acts in the cell metabolism as an electron donor, and consequently ascorbate free radical (AFR) is continuously produced. AFR can be reconverted to AA by means of AFR reductase or can undergo spontaneous disproportion, thus generating dehydroascorbic acid (DHA).

During cell division and cell expansion ascorbate consumption is more or less the same; however, the AA/DHA ratio is 6–10 during cell division and 1–3 during cell expansion. This ratio depends essentially on the different AFR reductase activity in these cells. In meristematic cells AFR reductase is very high, and consequently a large amount of AFR is reduced to AA and a small amount of AFR undergoes disproportionation; in expanding cells the AFR reductase activity is lower, and therefore AFR is massively disproportionated, thus generating a large quantity of DHA. Since the transition from cell division to cell expansion is marked by a large drop of AFR reductase activity in the ER, it is suggested here that AFR formed in this compartment may be involved in the enlargement of the ER membranes and provacuole acidification.

DHA is a toxic compound for the cell metabolism and as such the cell has various strategies to counteract its effects: (i) meristematic cells, having an elevated AFR reductase, prevent large DHA production, limiting the quantity of AFR undergoing disproportionation. (ii) Expanding cells, which contain a lower AFR reductase, are, however, provided with a developed vacuolar system and segregate the toxic DHA in the vacuole. (iii) Chloroplast strategy against DHA toxicity is efficient DHA reduction to AA using GSH as electron donor. This strategy is usually poorly utilized by the surrounding cytoplasm.

DHA reduction does play an important role at one point in the life of the plant, that is, during the early stage of seed germination. The dry seed does not store ascorbate, but contains DHA, and several DHA-reducing proteins are detectable. In this condition, DHA reduction is necessary to form a limited AA pool in the seed for the metabolic requirements of the beginning of germination. After 30–40h ascorbateex novo synthesis starts, DHA reduction declines until a single isoform remains, as is typical in the roots, stem, and leaves of seedlings. Finally, DHA recycling also appears to be important under adverse environmental conditions and ascorbate deficiency.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Amico, A., Dalessandro, G., Stefanizzi, L., and De Leo, P. (1972).Ann. Fac. Agr. 25 1–11.

    Google Scholar 

  • Arrigoni, O. (1957).Rend. Acc. Naz. Lincei 22 77–85.

    Google Scholar 

  • Arrigoni, O., Rossi, G., and Marrè, E. (1957).Rend. Acc. Naz. Lincei 23 287–295.

    Google Scholar 

  • Arrigoni, O. (1958).Rend. Acc. Naz. Lincei 19 156–164.

    Google Scholar 

  • Arrigoni, O., Arrigoni-Liso, R., and Calabrese, G. (1975).Nature (London) 256 513–514.

    Google Scholar 

  • Arrigoni, O., Arrigoni-Liso, R., and Calabrese, G. (1976).Science 194 332–333.

    Google Scholar 

  • Arrigoni, O., Arrigoni-Liso, R., and Calabrese, G. (1977a).FEBS Lett. 82 131–138.

    Google Scholar 

  • Arrigoni, O., De Santis, A., Arrigoni-Liso, R., and Calabrese, G. (1977b).Biochem. Biophys. Res. Comm. 74 1637.

    Google Scholar 

  • Arrigoni, O., Calabrese, G., Liso, R., and Porcelli, S. (1977c).Ann. Ist. Sper. Ortic. SA,7 1–14.

    Google Scholar 

  • Arrigoni, O., Di Pierro, S., and Borraccino, G. (1981).FEBS Lett. 125 242–244.

    Google Scholar 

  • Arrigoni, O., Bitonti, M. B., Cozza, R., Innocenti, A. M., Liso, R., and Veltri, R. (1989).Caryologia 42 213–216.

    Google Scholar 

  • Arrigoni, O., De Gara, L., Tommasi, F., and Liso, R. (1992).Plant Physiol. 99 236–238.

    Google Scholar 

  • Barlow, P. W., and Macdonald, P. D. M. (1973).Proc. R. Soc. B. London 183 385–398.

    Google Scholar 

  • Bitonti, M. B., Chiappetta, A., Innocenti, A. M., Liso, R., and Arrigoni, O. (1992).New Phytol. 121 577–580.

    Google Scholar 

  • Blakely, L. M., and Evans, T. A. (1979).Plant Sci. Lett. 14 79–83.

    Google Scholar 

  • Borsook, H., Davenport, H. W., Jeffreys, C. E. P., and Warner, R. C. (1937).J. Biol. Chem. 117 237–279.

    Google Scholar 

  • Chrispeels, M. J., Sadawa, D., and Cho, Y. P. (1974).J. Exp. Bot. 25 1157–1166.

    Google Scholar 

  • Cleland, R. (1968a).Plant Physiol. 43 865–870.

    Google Scholar 

  • Cleland, R. (1968b).Plant Physiol. 43 1625–1630.

    Google Scholar 

  • Clowes, F. A. L. (1961).J. Exp. Bot. 12 283–293.

    Google Scholar 

  • Cooper, J. B., and Varner, J. E. (1983).Plant Physiol. 73 324–328.

    Google Scholar 

  • Corsi, G., and Avanzi, S. (1970).Caryologia 23 381–394.

    Google Scholar 

  • Craig, T. A., and Crane, F. L. (1982).Indiana Acad. Sci. 91 150–162.

    Google Scholar 

  • De Gara, L., Tommasi, F., Liso, R., and Arrigoni, O. (1987).Boll. Soc. It. Biol. Sper. LXIII 551–558.

    Google Scholar 

  • De Gara, L., and Tommasi, F. (1990).Boll. Soc. It. Biol. Sper. LXVI 953–960.

    Google Scholar 

  • De Gara, L., Paciolla, C., Liso, R., Stefani, A., and Arrigoni, O. (1991a).J. Plant Physiol. 137 697–700.

    Google Scholar 

  • De Gara, L., Tommasi, F., Liso, R., and Arrigoni, O. (1991b).Phytochemistry 30 1397–1399.

    Google Scholar 

  • De Gara, L., De Tullio, M., Paciolla, C., Liso, R., and Arrigoni, O. (1993a). InPlant Peroxidase and Physiology (Welinder, K. G., Rasmussen, S. K., Penel, C., and Greppin, H., eds.), University of Geneva, Geneva, Switzerland, pp. 251–255.

    Google Scholar 

  • De Gara, L., Paciolla, C., Liso, R., Stefani, A., Blanco, A., and Arrigoni, O. (1993b).J. Plant Physiol. 141 405–409.

    Google Scholar 

  • De Gara, L., Paciolla, C., Tommasi, F., Liso, R., and Arrigoni, O. (1994).J. Plant Physiol. (in press).

  • De Leo, P., Dalessandro, G., De Santis, A., and Arrigoni, O. (1972).Plant and Cell Physiol. 14 487–496.

    Google Scholar 

  • De Tullio, M., Paciolla, C., and De Gara, L. (1993).Boll. Soc. It. Biol. Sper. LXIX 231–236.

    Google Scholar 

  • Evidente, A., Cicala, M. R., Randazzo, G., Riccio, R., Calabrese, G., Liso, R., and Arrigoni, O. (1983).Phytochemistry 22 2193–2196.

    Google Scholar 

  • Evidente, A., Arrigoni, O., Liso, R., Calabrese, G., and Randazzo, G. (1986).Phytochemistry 25 2739–2743.

    Google Scholar 

  • Foerster, G. V., Weis, W., and Standinger, H. (1965).Ann. Chem. 690 166–169.

    Google Scholar 

  • Forti, G. (1958).Rend. Acc. Naz. Lincei 24 70–77.

    Google Scholar 

  • Foyer, C. H., and Halliwell, B. (1976).Planta 133 21–25.

    Google Scholar 

  • Garuccio, I., and Arrigoni, O. (1979).Boll. Soc. It. Biol. Sper. 45 501–508.

    Google Scholar 

  • Groden, D., and Beck, E. (1979).Biochem. Biophys. Acta 546 426–435.

    Google Scholar 

  • Hedge, R. R. (1985).Bot. Mag. Tokyo 98 219–223.

    Google Scholar 

  • Hidalgo, A., Gonzales-Reyes, J. A., and Navas, P. (1989).Plant Cell Environ. 12 455–460.

    Google Scholar 

  • Hutton, J. J., Tappel, A. L., and Udenfriend, S. (1967).Arch. Biochem. Biophys. 118 231–240.

    Google Scholar 

  • Innocenti, A. M., Bitonti, M. B., Arrigoni, O., and Liso, R. (1990).New Phytol. 114 507–509.

    Google Scholar 

  • Innocenti, A. M., Bitonti, B., Mazzucca, S., Liso, R., and Arrigoni, O. (1993).Caryologia 46 1–4.

    Google Scholar 

  • Innocenti, A. M., Mazzucca, S., Bitonti, B., De Gara, L., Liso, R., and Arrigoni, O. (1994).Plant Physiol. Biochemistry (in press).

  • Lamport, D. T. A. (1965). The protein component of primary cell walls. InAdvances in Botanical Researches (Preston, R. D., ed.),2 151–218.

  • Laudi, G. (1955).N. Giorn. Bot. Ital. 62 368–373.

    Google Scholar 

  • Liso, R., and Calabrese, G. (1974).Phycologia 13 205–208.

    Google Scholar 

  • Liso, R., and Calabrese, G. (1975).Phycologia 14 9–11.

    Google Scholar 

  • Liso, R., Arrigoni, O., Stomeo, G., and Porcelli, S. (1977).Ann. Ist. Sper. Ort. SA,7 1–11.

    Google Scholar 

  • Liso, R., Calabrese, G., Bitonti, M. B., and Arrigoni, O. (1984).Exp. Cell. Res. 150 314–320.

    Google Scholar 

  • Liso, R., Innocenti, A. M., Bitonti, M. B., and Arrigoni, O. (1988).New Phytol. 110 469–471.

    Google Scholar 

  • Luster, D. G., and Buckhout, T. J. (1988).Physiol. Plant. 73 339–347.

    Google Scholar 

  • Marrè, E., and Laudi, G. (1955).Rend. Acc. Naz. Lincei 20 77–82.

    Google Scholar 

  • Marrè, E., Pece, G., and Forti, G. (1956).Rend. Acc. Naz. Lincei 20 646–652.

    Google Scholar 

  • Marrè, E., and Arrigoni, O. (1958).Biochem. Biophys. Acta 30 453–457.

    Google Scholar 

  • May, M. J., and Leaver, C. J. (1993).Plant. Physiol. 103 621–627.

    Google Scholar 

  • Meister, A. (1992).Biochem. Pharmacol. 44 1905–1915.

    Google Scholar 

  • Navas, P. (1991). Ascorbate free radical (semidehydro) reductase on plant plasma membrane. InOxidoreduction at the Plasma Membrane: Relation to Growth and Transport. Vol. II (Crane, F. L., Morrè, D. J., and Low, H. E., eds.), CRC Press, Boca Raton, Florida, pp. 111–120.

    Google Scholar 

  • Pece, G., Laudi, G., and Marrè, E. (1956).Rend. Acc. Naz. Lincei 20 513–518.

    Google Scholar 

  • Pihlajaniemi, T., Helaakoski, T., Tasanen, K., Myllylä, R., Huhtala, M. L., Koivu, J., and Kivirikko, K. I. (1987).EMBO J. 6 643–649.

    Google Scholar 

  • Rhoads, R. E., and Udenfriend, S. (1970).Arch. Biochem. Biophys. 139 329–339.

    Google Scholar 

  • Ridge, I., and Osborne, D. J. (1971).Nature New. Biol. 229 205–208.

    Google Scholar 

  • Shigeoka, S., Nakano, Y., and Kitaoka, S. (1980).Arch. Biochem. Biophys. 201 121–127.

    Google Scholar 

  • Stone, N., and Meister, A. (1962).Nature 194 555–557.

    Google Scholar 

  • Sreekumari, S. B., and Shah, C. K. (1978).Acta Bot. Indica,6 (suppl. 22–31.

    Google Scholar 

  • Szent Györgyi, A. (1928).Biochem. J. 22 1387–1409.

    Google Scholar 

  • Thomas, J. E., and Davidson, D. (1982).Caryologia 35 191–203.

    Google Scholar 

  • Tommasi, F., De Gara, L., Liso, R., and Arrigoni, O. (1987).Boll. Soc. It. Biol. 43 779–786.

    Google Scholar 

  • Tommasi, F., De Gara, L., Liso, R., and Arrigoni, O. (1990).J. Plant Physiol. 135 766–768.

    Google Scholar 

  • Trezzi, F. (1956).Rend. Acc. Naz. Lincei 21 1–15.

    Google Scholar 

  • Wells, W. W., Xu, D. P., Yang, Y., and Rocque, P. A. (1990).J. Biol. Chem. 265 15361–15364.

    Google Scholar 

  • Yamaguchi, M., and Joslyn, M. A. (1951).Plant Physiol. 26 757–772.

    Google Scholar 

  • Yamaguchi, K., and Suda, S. (1952).Folia pharmacol. Japan 48 31–32.

    Google Scholar 

  • Zacheo, G., Liso, R., Bleve, T., Lamberti, F., Perrino, F., and Arrigoni, O. (1981).Nematol. Medit. 9 181–187.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Arrigoni, O. Ascorbate system in plant development. J Bioenerg Biomembr 26, 407–419 (1994). https://doi.org/10.1007/BF00762782

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00762782

Key words

Navigation