Aqueous Interfaces in Plant Cells

Authors

  • S. K. Asunmaa

Abstract

A subunit, 90 to 100 Å in diameter, consisting of lipid and protein components, is proposed for semipermeable plant cell membranes. The hydrocarbon chains of the lipid molecules are oriented toward the periphery, the hydrophilic molecular segments toward the center of a lipid annulus where the hydrophilic region stabilizes a 22-Å sheath of ordered water, too rich in hydrogen bonds to dissolve electrolytes. The ordered water leaves a core of ordinary water for ion transport. The subunit thus acts as an ion-gate, because of synchronized movement of the lipids for opening and closing the pore, powered by surface adsorbed proteins. The subunit model would consist of 27 galactosyl diglyceride units (mono- or di- or both) in chloroplast membranes from which Wehrmeyer (1967) isolated a 80,000-g fraction that consists of 90-Å diameter subunits.

Membrane permeability data and the Small-Bourgès (1965) phase diagram for the ternary system cholesterol-lecithin-water (in agreement with X-ray and NMR data) are discussed as supporting evidence for the ion-gate model, after a short review of the model design for the cholesterol-lecithin complexes, which in the subunit configuration may adsorb proteins such as the circular polypeptide alamethicin. The role of plant proteins requires further analysis. Electron micrographs of preparations of plant cell membranes, animal cell plasma membranes and proteolipid membranes in vitro, as published by various research groups, are presented as morphological support for the ion-gate model.

References

Asunmaa, S. K., R. D. Schultz, and F. D. Kleist. 1969. Ultrastructure of thin proteolipid membranes. In C. J. Arceneaux (ed.), Proceedings 27th Annual Meeting, Electron Microscopy Soc. of America. St. Paul, Minn., Aug. 26-29, 1969, Claitor's Publishing Division, Baton Rouge, La., p. 336.nBenedetti, E. L., and P. E. Emmelot. 1965. Electron microscopic observation of negatively stained plasma membranes isolated from rat liver. J. Cell Biol., 26: 299.nBenedetti, E. L., and P. E. Emmelot. 1968. Hexagonal array of subunits in tight junctions separated from isolated rat liver plasma membranes. J. Cell Biol., 38: 15.nBriggs, G. E., A. Hope, and R. N. Robertson. 1961. Electrolytes and plant cells, v. 1. Botanical Monographs, F. A. Davis Company, Philadelphia, Pa. Blackwell Scientific Publ. Co., Oxford.nCollander, R. 1941. Selective absorption of cations by higher plants. Plant Physiol., 16.nDrost-Hansen, W. 1969. Structure of water near solid interfaces. Ind. Eng. Chem., 61(11): 10.nFowkes, F. M. 1966. Part of general discussion on colloid stability in aqueous and nonaqueous media. Faraday Soc. Disc., 42: 140.nFrey-Wyssling, and K. Mühlethaler. 1960. Ultrastructural plant cytology. Elsevier Publ. Co., Amsterdam, London, N. Y., p. 145.nGlauert, A. M. 1966. Moiré pattern in electron micrographs of a bacteria membrane. J. Cell. Sci., 1: 425.nGlauert, A. M., N. T. Dingle, and J. A. Lucy. 1962. Action of saponin on biological cell membranes. Nature, 196: 952, 953.nGreenwood, A. D. 1968. In J. H. Burnett (ed.), Plant cells by F. A. L. Clowes and B. E. Juniper, v. 8, Botanical Monographs, Blackwell Scientific Publ. Co., Oxford, p. 135.nHicks, R. M., and B. Ketterer. 1970. Isolation of the plasma membrane of the luminal surface of rat bladder epithelium and the occurrence of a hexagonal lattice of subunits both in negatively stained whole mounts and in sectioned membranes. J. Cell Biol., 45: 542.nHohl, H. R., and A. Hepton. 1965. A globular subunit pattern in plastid membranes. J. Ultrastruct. Res., 12: 542.nHudson, J. B., and S. Ross. 1965. Adsorption and condensation processes. In D. E. Gushee (ed.), Chemistry and physics of interfaces, reprinted from Industrial and Engineering Chemistry, Sept. 1964-Sept. 1965, American Chemical Soc. Publications, Washington, D.C., p. 103.nHyde, B. B., A. J. Hodge, and M. L. Birnstiel. 1962. Phytoferritin: A plant protein discovered by electron microscopy. In S. S. Breese (ed.), Proceedings 5th International Congress for Electron Microscopy, Philadelphia, Pa., Academic Press, v. 2, T 1.nJunger, E., and H. Reinauer. 1969. Liquid crystalline phases of hydrated phosphatidyl ethanolamine. Biochem. Biophys. Acta, 183: 304.nKawasaki, K., K. Kanou, and Y. Sakita. 1958. Liquid-like layers in the adsorbed film of H2O on glass. J. Phys. Soc. Japan, 13: 222.nKubát, J., and C. Pattyranie. 1967. Transition in cellulose in the vicinity of -30 C. Nature, 215: 390.nLawson, K. D., and T. J. Flautt. 1965. Nuclear magnetic resonance studies of surfactant mesophases, presented at Internatl. Liquid Crystal Conference, Kent State Univ., Ohio, 1965, Aug. 15-20. Publ. In C. J. Diene and M. M. Labes (eds.), Molecular crystals (1966), 1 (2): 24.nMoor, H., and K. Mühlethaler. 1965. In Ultrastructural plant cytology by A. Frey-Wyssling and K. Mühlethaler. Elsevier Publ. Co., Amsterdam, London, N. Y., p. 148, 170, 184, 186, 264.nMysels, K. J. 1966. Part of general discussion on colloid stability in aqueous and nonaqueous media. Faraday Soc. Disc., 42: 138.nNorthcote, D. H. 1968. In J. H. Burnett (ed.), v. 8, Plant cells by F. A. L. Clowes and B. E. Juniper. Botanical Monographs. Blackwell Scientific Publ. Co., Oxford, p. 260.nNichols, B. W., and A. T. James. 1968. The function and metabolism of fatty acids and acyl lipids in chloroplasts. In J. B. Pridham (ed.), Plant cells. Academic Press, N. Y., p. 163.nParpart, A. K., and J. F. Hoffman. 1954. In H. T. Clark (ed.), Ion transport across membranes. Academic Press, N. Y., p. 69.nParpart, A. K., and R. Ballentine. 1952. In E. S. B. Barrow (ed.), Modern trends in physiology and biochemistry. Academic Press, N. Y., p. 135.nPinto Da Silva, P., and D. Branton. 1970. Membrane splitting in freeze-etching, covalently bound ferritin as a membrane marker. J. Cell Biol., 45: 598.nRamiah, M. V., and D. A. I. Goring. 1965. The thermal expansion of cellulose, hemicellulose and lignin. J. Polymer Sci., Pt. C No. 11; 27.nRevel, J. P., and M. J. Karnovsky. 1967. Hexagonal array of subunits in intercellular junctions of the mouse heart and liver. J. Cell Biol., 33: C7-C12 (following p. 450).nRies, H. E., Jr. 1961. Monomolecular films. Scientific Am., 204: 152nRitchie, A. E., and J. H. Bryner. 1968. A structural element in the envelope system of Vibrio fetus. In C. J. Arceneaux (ed.), Proceedings 26th Annual Meeting, Electron Microscopy Society of America, New Orleans, La., 1-9 Sept. 1968. Claitor's Publishing Division, Baton Rouge, La., p. 78.nRobertson, J. D. 1966. Current problems of unit membrane structure and contact relationships. In Proceedings of Conference on Nerve as a Tissue, Philadelphia, Pa., 12-13 Nov. 1964. Harper and Row, Publishers, N. Y., London, p. 11-48.nRobertson, J. D. 1966. Granulo-fibrillar and globular substructure in unit membranes (electron microscopy). New York Academy of Sciences, 137 (2): 421.nRobertson, J. D. 1965. Design principles of the (animal cell) unit membrane. In CIBA Foundation Symposium on principles of biomolecular organization 9-11 June 1965. London; Little Brown and Company, Boston 1966, p. 357.nSchultz, R. D., and S. K. Asunmaa. 1970. Ordered water and the ultrastructure of the cellular plasma membrane. In J. F. Danielli, A. C. Riddiford, and M. D. Rosenberg (eds.), Recent progress in surface science, v. 3, Academic Press, N. Y., p. 291.nSchultz, R. D., S. K. Asunmaa, and F. D. Kleist. 1969. Ultrastructure and variable aperture pore function of hexagonal subunits in plasma membranes, Paper 10246 McDonnell Douglas Co., Newport Beach, Calif., presented at the 2nd Internatl. Meeting of the Internatl. Society of Neurochemistry, Milan, Italy, 1-5 Sept. 1969.nSchultz, R. D., S. K. Asunmaa, G. A. Guter, and F. E. Littman. 1969. Characterization of ordered water in hydrophilic membrane pores, Paper 10247 McDonnell Douglas Co., Newport Beach, Calif., presented at the 2nd Internatl. Meeting of the Internatl. Society of Neurochemistry, Milan, Italy, 1-5 Sept. 1969.nSjöstrand, F. S. 1953. The ultrastructural organization of retinal rods and cones. In Proceedings of the Annual Meeting of the Electron Microscopy Soc. of America in Cleveland, Ohio, 6-8 Nov. 1952. J. Appl. Phys. 1953, 24: 117.nSjöstrand, F. S. 1962. Molecular architecture of cell membrane and cytoplasmic membranes. In Proceedings Internatl. Pharmacology Meeting in Stockholm, 1961, v. 4, p. 1. (Publ. 1962.)nSjöstrand, F. S. 1963. A comparison of plasma membrane, cytomembranes and mitochondrial membrane elements with respect to ultrastructural features. J. Ultrastruct. Res., 9: 561.nSjöstrand, F. S. 1963. A new repeat structural element of mitochondrial and certain cytoplasmic membranes. Nature, 199: 1262.nSjöstrand, F. S. 1963. A new ultrastructural element of the membranes in mitochondrial and some cytoplasmic membranes. J. Ultrastruct. Res., 9: 340.nSjöstrand, F. S. 1969. Morphological aspects of lipoprotein structures. In E. Tria and A. M. Scanu (eds.), Structural and functional aspects of lipoprotein structures in living systems. Academic Press, N. Y., p. 73.nSjöstrand, F. S. and L. Barajas. 1970. A new model for mitochondrial membranes based on structural and biochemical information. J. Ultrastructure Research. In press.nSjöstrand, F. S., and J. Rhodin. 1953. The ultrastructure of the proximal convoluted tubules of the mouse kidney as revealed by high resolution electron microscopy. Exp. Cell Res., 4: 426.nSmall, D. M., and M. Bourgès. 1965. Lyotropic paracrystalline phases obtained with ternary and quarternary systems of amphiphilic substances in water: Studies on aqueous systems of lecithin, bile salt and cholesterol. In G. H. Brown, G. J. Dienes, and M. M. Labes (eds.), Liquid crystals. Proceedings Internal. Conference on Liquid Crystals, Kent State Univ., Ohio, 16-20 Aug., Gordon and Breach, Science Publishers Inc., N. Y., p. 221.nVandenheuval, F. A. 1963. Biological structure at the molecular level with stereomodel projections; I, The lipids in the myelin sheath of nerve. J. Am. Oil Chemists' Soc., 40(9): 455.nWehrmeyer, O. 1967. Prolamellar bodies, structure and development. In C. Sironval (ed.), Le Chloroplaste, Croissance et Vieillissement. Masson et C1e Editeurs, Paris, p. 62.nWeier, T. E., A. H. Engelbrecht, A. Harrison, and E. B. Risley. 1965. Subunits in the membranes of chloroplasts of Phaseolus vulgaris, Pisum sativum, and Aspidistra sp. J. Ultrastruct. Res., 13: 92 and In J. T. O. Kirk and R. A. Tilney-Basset (eds.), The plastids. W. H. Freeman and Co., London, San Francisco, p. 48.nWu, T. H. 1964. A nuclear magnetic resonance study of water in clay. J. Geophys. Res., 69: 1083.n

Downloads

Published

2007-06-19

Issue

Section

Research Contributions