Summary
Freezing, desiccation and high-temperature stress may under certain conditions result in inactivation of electron transport (DCIP reduction) and cyclic photophosphorylation of isolated chloroplast membranes of spinach (Spinacia oleracea L.). When sugars are present during temperature and water stress, the thylakoids may be partially or completely protected. This membrane stabilization depends on the concentration of sugars and their molecular size. The trisaccharide raffinose is, on a molar basis, more effective than the disaccharide sucrose and the latter more than the monosaccharide glucose. An uncoupling effect and a stimulation of electron transport can be observed during freezing, desiccation and heat treatment, e.g. electron transport reactions are less sensitive to temperature and water stress than is photophosphorylation. As sugars are known to accumulate in winter, unspecific membrane stabilization by sugars may help to explain the often reported parallel development of frost, drought and heat resistance in many plants during winter.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alexandrov, V. Y., Lomagin, A. G., Feldman, N. L.: The responsive increase in thermostability of plant cells. Protoplasma (Wien) 69, 417–458 (1970).
Arnon, D. I.: Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol. 24, 1–15 (1949).
Duane, W. C., Krogmann, D. W.: Chloroplast storage with retention of photosynthetic activities. Biochim. biophys. Acta (Amst.) 71, 195–196 (1963).
Emmett, J. M., Walker, D. A.: Thermal uncoupling in chloroplasts. Biochim. biophys. Acta (Amst.) 180, 424–425 (1969).
Feldman, N. L.: The influence of sugars on the cell stability of some higher plants to heating and high hydrostatic pressure. Citologija (Leningrad) 4, 633–643 (1962).
Giles, C. H., McKay, R. B.: Studies in hydrogen bond formation. XI. Reactions between a variety of carbohydrates and proteins in aqueous solutions. J. biol. Chem. 237, 3388–3392 (1962).
Heber, U., Santarius, K. A.: Loss of adenosine triphosphate synthesis caused by freezing and its relationship to frost hardiness problems. Plant Physiol. 39, 712–719 (1964).
Heber, U., Santarius, K. A.: Cell death by cold and heat and resistance to extreme temperatures. Mechanisms of hardening and dehardening. In: Temperature and life, Precht, H., Christophersen, J., Hensel, H., Larcher, W., eds. (in press). Berlin-Heidelberg-New York: Springer 1973.
Heber, U., Tyankova, L., Santarius, K. A.: Stabilization and inactivation of biological membranes during freezing in the presence of amino acids. Biochim. biophys. Acta (Amst.) 241, 578–592 (1971).
Henckel, P. A.: Physiology of plants under drought. Ann. Rev. Plant Physiol. 15, 363–386 (1964).
Huggins, C. E.: Preservation of organized tissues by freezing. Fed. Proc. 24, S190-S195 (1965).
Jagendorf, A. T., Avron, M.: Cofactors and rates of photosynthetic phosphorylation by spinach chloroplasts. J. biol. Chem. 231, 277–290 (1958).
Jeremias, K.: Über die jahresperiodisch bedingten Veränderungen der Ablagerungsform der Kohlenhydrate in vegetativen Pflanzenteilen (unter besonderer Berücksichtigung der Zucker der Raffinose-Gruppe). Bot. Studien (Jena) No. 15 (1964).
Kappen, L.: Untersuchungen über den Jahresverlauf der Frost-, Hitze- und Austrocknungsresistenz von Sporophyten einheimischer Polypodiaceen (Filicinae). Flora 155, 123–166 (1964).
Kiewiet, D. Y. de, Hall, D. O., Jenner, E. L.: Effect of carbonylcyanide m-chlorophenylhydrazone on the photochemical reactions of isolated chloroplasts. Biochim. biophys. Acta (Amst.) 109, 284–292 (1965).
Lange, O. L.: Die Hitzeresistenz einheimischer immer- und wintergrüner Pflanzen im Jahresverlauf. Planta (Berl.) 56, 666–683 (1961).
Lange, O. L.: Investigations on the variability of heat-resistance in plants. In: The cell and environmental temperature, p. 131–141, Troshin, A. S., ed. Oxford: Pergamon Press 1967.
Langridge, J., McWilliam, J. R.: Heat responses of higher plants. In: Thermobiology, p. 231–292, Rose, A. H., ed. London-New York: Acad. Press 1967.
Levitt, J.: The hardiness of plants. New York: Acad. Press 1956.
Levitt, J.: Frost, drought, and heat resistance. Protoplasmatologia, vol. VIII/6, Heilbrunn, L. V., Weber, F., eds. Vienna: Springer 1958.
Levitt, J.: Responses of plants to environmental stresses. New York and London: Acad. Press 1972.
Molotkovsky, Y. G.: Hydrolysis of phospholipids and formation of free fatty acids in isolated chloroplasts. Biokhimiya 33, 961–968 (1968).
Molotkovsky, Y. G., Zhestkova, I. M.: The influence of heating on the morphology and photochemical activity of isolated chloroplasts. Biochem. biophys. Res. Commun. 20, 411–415 (1965).
Molotkovsky, Y. G., Zhestkova, I. M.: Morphological and functional changes of isolated chloroplasts during heating. Dokl. Acad. Nauk SSSR 166, 488–491 (1966).
Oku, T., Tomita, G.: Effect of polyethylene glycol on heat inactivation of the Hill reaction. Biochem. biophys. Res. Commun. 44, 958–962 (1971).
Parker, J.: Protoplasmic resistance to water deficits. In: Water deficits and plant growth, vol III, p. 125–176, Kozlowski, T. T., ed. New York-London: Acad. Press 1972.
Santarius, K. A.: Protective mechanisms in frost-hardy plants. In: Low temperature biology of foodstuffs, p. 135–151, Hawthorn, J., Rolfe, E. J., eds. New York: Pergamon Press 1968.
Santarius, K. A.: The effect of freezing on thylakoid membranes in the presence of organic acids. Plant Physiol. 48, 156–162 (1971).
Santarius, K. A.: Freezing. The effect of eutectic crystallization on biological membranes. Biochim. biophys. Acta (Amst.) 291, 38–50 (1973).
Santarius, K. A., Heber, U.: Das Verhalten von Hill-Reaktion und Photophosphorylierung isolierter Chloroplasten in Abhängigkeit vom Wassergehalt. II. Wasserentzug über CaCl2. Planta (Berl.) 73, 109–137 (1967).
Schwarz, W.: Der Einfluß der Photoperiode auf das Austreiben, die Frosthärte und die Hitzeresistenz von Zirben und Alpenrosen. Flora 159, 258–285 (1970).
Seybold, S.: Zum jahres- und tagesperiodischen Verhalten von Zuckeralkoholen in vegetativen Pflanzenteilen. Flora A 160, 561–575 (1969).
Steponkus, P. L.: Protein-sugar interactions during cold acclimatation. (Abstr.) Proc. XI Int. Bot. Congr., p. 209 (1969).
Author information
Authors and Affiliations
Additional information
Dedicated to Professor Otto Stocker, Darmstadt, on the occasion of his 85th birthday.
Rights and permissions
About this article
Cite this article
Santarius, K.A. The protective effect of sugars on chloroplast membranes during temperature and water stress and its relationship to frost, desiccation and heat resistance. Planta 113, 105–114 (1973). https://doi.org/10.1007/BF00388196
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00388196