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Cellular compartmentalization of salt ions and protective agents with respect to freezing tolerance of leaves

Investigations with the Halophyte Halimione portulacoides (L.) aellen

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Summary

Evidence was given that the freezing tolerance of Halimione portulacoides, a wintergreen halophyte, can be explained by protection of sensitive cellular membranes in vivo. Experiments were done with cloned cuttings of a plant from the German North Sea coast. One series received no NaCl (O-plants) the other 3% NaCl (NaCl-plants) in the nutrient solution. During the annual course Na+ and Cl- of the O-plant leaves remained on a nearly constant low level. In the leaves of the NaCl-plants Na+ and Cl- concentrations changed strongly during year and reached a maximum in winter. Potassium was always on a low level. The freezing tolerance curves showed a minimum in summer and a maximum in winter. The small difference between the freezing tolerance peaks of the NaCl- and O-plants indicated that the increased salt stress did not affect freezing tolerance very much. Freezing stress in cellular membranes, like thylacoids, acts in the same way as increasing salt concentration; consequently both together must amplify the stress. For the analysis of their ion contents chloroplasts of H. portulacoides were non-aqueously isolated from leaves with different freezing tolerance during the year. In midwinter, when freezing tolerance was highest, the chloroplasts of the NaCl-plants contained about 250 mM chloride (O-plants c. 150 mM), while the non-plastidic fraction of the cell contained about 1 M (O-plants c. 400 mM) chloride. On the other hand citrate reached high concentrations in the chloroplasts in winter. Non-volatile organic acids like citrate are known to compensate colligatively the injurious action of the inorganic salt ions on thylacoids in vitro (Heber and Santarius, 1976). The molar proportion between chloride and citrate in H. portulacoides chloroplasts decreased with increasing freezing tolerance and reached values which were protective on chloroplast membranes in vitro. This relationship in vivo with H. portulacoides provides evidence supplying the concept of colligative protection of cellular membranes. Besides citrate also malate may act as a colligatively protecting agent against the amplified salt stress by freezing.

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Maier, M., Kappen, L. Cellular compartmentalization of salt ions and protective agents with respect to freezing tolerance of leaves. Oecologia 38, 303–316 (1979). https://doi.org/10.1007/BF00345190

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