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Transverse heterogeneity in lipid fluidity in spinach thylakoids, photosystem II preparations, and thylakoid galactolipid vesicles

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Abstract

We have used three doxyl stearic acid spin labels to study the transverse hetero-geneity in lipid fluidity in thylakoids, photosystem II (PS II) preparations, and thylakoid galactolipid vesicles. This comparative study shows that spin labels incorporated into the membrane of the PS II preparation experience far more immobilization than do the same spin labels incorporated into either thylakoids or vesicles prepared from the polar lipids extracted from thylakoids. The spin label immobilization found in the PS II preparation is manifest even near the center of the bilayer, where lipid mobility is normally at its maximum. Analysis of the lipid content of the PS II preparation, relative to chlorophyll, suggests that the PS II preparation may be lipid depleted. This lipid depletion could explain the results presented. However, electron microscopy [Dunahay et al. (1984) Biochim. Biophys. Acta 764:179–193] has not indicated that major delipidation has occurred, and so it remains possible that the immobilization found in the PS II preparation is due primarily to the normal (but close) juxtaposition of adjacent PS II complexes and the cooperative immobilization of their surrounding lipids. Based on the results presented, we conclude that highly mobile lipids are not required for oxygen evolution, the primary photochemistry or the secondary reduction of exogenously added quinones. Unfortunately, the relationship between the plastoquinone pool and the fluidity of the membrane in the PS II preparation remains ambiguous.

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Abbreviations

PS II:

photosystem II

SDSA:

5-doxylstearic acid

12DSA:

12-doxylstearic acid

16DSA:

16-doxylstearic acid

7N14:

2-heptyl-2-hexyl-5,5-dimethyloxazolidine-N-oxyl

chromium oxalate:

potassium trioxalatochromiate

EPR:

electron paramagnetic resonance

Chl:

chlorophyll

MGDG:

monogalactosyldiacylglycerol

DGDG:

digalactosyldiacylglycerol

References

  1. Aronson H, Waggoner C, More J and Berg SP (1983) Spin-Label Studies of the Lipid Regions of Spinach Thylakoids and a Detergent-Derived Oxygen-Evolving Photosystem II Preparation. Biochim Biophys Acta 725:519–528

    Google Scholar 

  2. Berg SP and Nesbitt DM (1979) Chromium Oxalate: A New Spin Label Broadening Agent for Use with Thylakoids. Biochim Biophys Acta 548:608–615

    Google Scholar 

  3. Berthold DA, Babcock GT and Yocum CF (1981) A Highly Resolved, Oxygen-Evolving Photosystem II Preparation from Spinach Thylakoid Membranes. EPR and Electron Transport Properties. FEBS Letters 134:231–234

    Google Scholar 

  4. Dunahay TG, Staehelin LA, Seibert M, Ogilvie PD and Berg SP (1984) Structural, Biochemical and Biophysical Characterization of Four Oxygen-Evolving Photosystem II Preparations from Spinach. Biochim Biophys Acta 764:179–193

    Google Scholar 

  5. Folch J, Lees M and Sloane-Stanly GH (1975) A Simple Method for the Isolation and Purification of Total Lipids from Animal Tissues. J Biol Chem 226:492–509

    Google Scholar 

  6. Ford RC, Chapman DJ, Barber J, Pedersen JZ and Cox RP (1982) Fluorescence Polarization and Spin-Label Studies of the Fluidity of Stromal and Granal Chloroplast Membranes. Biochim Biophys Acta 681:145–151

    Google Scholar 

  7. Gaffney BJ (1976) Practical Considerations for the Calculation of Order Parameters for Fatty Acid or Phospholipid Spin Labels in Membranes, in: Spin Labeling Theory and Applications, (ed. LJ Berliner) Academic Press, New York, pp 567–571

    Google Scholar 

  8. Hiller RG and Raison JK (1980) The Fluidity of Chloroplast Thylakoid Membranes and Their Constituent Lipids. A comparitative Study by ESR, Biochim Biophys Acta 599:63–72

    Google Scholar 

  9. Hubbell WL and McConnell HM (1969) Orientation and Motion of Amphiphilic Spin Labels in Membranes. Proc Natl Acad Sci (USA) 64:20–27

    Google Scholar 

  10. Hubbell WL and McConnell HM (1971) Molecular Motion in Spin-Labeled Phospholipids and Membranes. J Am Chem Soc 93:314–326

    Google Scholar 

  11. Jost P, Libertini LJ, Herbert VC, and Griffith OH (1971) Lipid Spin Labels in Lecithin Multilayers. A Study of Motion Along Fatty Acid Chains. J Mol Biol 59: 77–98

    Google Scholar 

  12. Kivelson D (1960) Theory of ESR Linewidths of Free Radicals, J Chem Phys 33: 1094–1106

    Google Scholar 

  13. Klopfenstein C, Jost OH and Griffith OH (1972) The Dedicated Computer in Electron Spin Resonance Spectroscopy. in: Computers in Chemical and Biochemical Research (eds: Klopfenstein CE and Wilkins CL) Academic Press, New York, Volume 1:175–221

    Google Scholar 

  14. Kuwabara T, Murata N (1982) Inactivation of Photosynthetic Oxygen Evolution and Concomitant Release of Three Polypeptides in the Photosystem II Particles of Spinach Chloroplasts. Plant and Cell Physiol 23:533–539

    Google Scholar 

  15. Lavorel J, Seibert M, Maison-Peteri B, Briantais J-M (1984) Evaluation of the Plastoquinone Pool Size in Oxygen-Evolving Photosystem II (OES II) Preparations. In: the Proceedings of the 6th International Congress on Photosynthesis, August 1983, Brussels, Belgium, in the press

  16. Lowry OH, Rosebrough NJ, Farr Al, and Randall RJ (1951) Protein Measurements With the Folin Phenol Reagent. J Biol Chem 193:265–275

    Google Scholar 

  17. MorseII PD, Ruhlig M, Snipes W, and Keith AD (1975) A Spin-Label Study of the Viscosity Profile of Sarcoplasmic Reticular Vesicles. Arch Biochem Biophys 168: 40–56

    Google Scholar 

  18. Nichols BW (1963) Separation of the Lipids of Photosynthetic Tissues: Improvements in Analysis by Thin-Layer Chromatography. Biochim Biophys Acta 70: 417–422

    Google Scholar 

  19. Ogilvie PD, Reschl LB and Berg SP (1983) Electron Acceptance at Photosystem II in an Oxygen-Evolving Photosystem II Preparation: Clear Discrimination of Two Sites of Electron Acceptance for Quinones and Quinonediimines Associated with a Photosystem II Preparation. Arch Biochem Biophys 220:451–458

    Google Scholar 

  20. Smith ICP, (1972) The Spin Label Method. In Biological Application of Electron Spin Resonance (eds: HM Swartz, JR Bolton, DC Borg) Wiley-Interscience, New York, pp 483–539

    Google Scholar 

  21. Strzalka K and Subegynski WK, (1981) Formation of Thylakoid Membranes in Greening Leaves and Their Modification By Protein Synthesis Inhibitors. 2. A Spin Label Study of Membrane Lipid Mobility. Photobiochem Photobiophy 2:227–232

    Google Scholar 

  22. Murphy DJ and Woodrow IE, (1983) The Lateral Segregation Model. A New Paradigm for the Dynamic Role of Acyl Lipids in the Molecular Organization of Photosynthetic Membranes. In: Biosynthesis and Function of Plant Lipids (eds WWThomson, JBMudd and MGibbs), Proceedings of the Sixth Annual Symposium in Botany (January 13–15, 1983) Waverly Press, Baltimore, MD, USA, pp 104–125

    Google Scholar 

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Waggoner, C., Aronson, H., More, I. et al. Transverse heterogeneity in lipid fluidity in spinach thylakoids, photosystem II preparations, and thylakoid galactolipid vesicles. Photosynth Res 6, 57–72 (1985). https://doi.org/10.1007/BF00029046

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