Lateral heterogeneity of photosystems in thylakoid membranes studied by Brownian dynamics simulations

Biophysical Journal

Volumn 85, Issue 2, 2003, Pages 774-789

  Borodich, Andrei ^a   Rojdestvenski, Igor ^a   Cottam, Michael ^b  

^a UMEÅ UNIVERSITY   (Sweden)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CELL STIMULATION; CHEMICAL COMPOSITION; CHLOROPLAST; GENETIC HETEROGENEITY; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOLECULAR RECOGNITION; NONHUMAN; PHOTOSYNTHESIS; PROTEIN LIPID INTERACTION; SIMULATION; STROMA CELL; THERMODYNAMICS; THYLAKOID MEMBRANE;

EMBRYOPHYTA;

EID: 0042344866     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(03)74519-6     Document Type: Article

References (73)

1. Albertsson, P.-A. 2001. A quantitative model of the domain structure of the photosynthetic membrane. Trends Plant Sci. 6:349-358.
2. Alexander, S., P. M. Chaikin, P. Grant, G. J. Morales, P. Pincus, and D. Hone. 1984. Charge renormalization, osmotic pressure, and bulk modulus of colloidal crystals: theory. J. Chem. Phys. 80:5776-5781.
3. Allen, J. F., and N. G. Holmes. 1986. A general model for regulation of photosynthetic unit function by protein phosphorylation. FEBS Lett. 202:175-181.
4. Allen, J. F. 1992. How does protein phosphorylation regulate photosynthesis? TIBS. 17:12-17.
5. Anderson, J. M., and E.-M. Aro. 1994. Grana stacking and protection of photosystem II in thylakoid membranes of higher plant leaves under sustained high irradiance: a hypothesis. Photosynth. Res. 41:315-326.
6. Andersson, B., and J. M. Anderson. 1980. Lateral heterogeneity in the distribution of chlorophyll-protein complexes of the thylakoid membranes of spinach chloroplasts. Biochim. Biophys. Acta. 593:427-440.
7. Aranda-Espinoza, H., A. Berman, N. Dan, P. Pincus, and S. Safran. 1996. Interaction between inclusions embedded in membranes. Biophys. J. 71:648-656.
8. Barber, J. 1980. Membrane surface charges and potentials in relation to photosynthesis. Biochim. Biophys. Acta. 594:253-308.
9. Barber, J. 1982. Influence of surface charges on thylakoid structure and function. Annu. Rev. Plant Physiol. 33:261-295.
10. Beresford-Smith, B., D. Chan, and D. J. Mitchell. 1985. The electrostatic interaction in colloidal systems. J. Colloid Interface Sci. 105:216-234.
11. Boekema, E. J., A. F. Boonstra, J. P. Dekker, and M. Rogner. 1994. Electron microscopic structural analysis of Photosystem I, Photosystem II, and the cytochrome b6/f complex from green plants and cyanobacteria. J. Bioenerg. Biomembr. 26:17-29.
12. Boekema, E. J., J. F. L. van Breemen, H. van Roon, and J. P. Dekker. 2000. Arrangement of Photosystem II supercomplexes in crystalline macrodomains within the thylakoid membrane of green plant chloroplasts. J. Mol. Biol. 301:1123-1133.
13. Bostrom, M., D. R. Williams, and B. W. Ninham. 2001. Specific ion effects: why DLVO theory fails for biology and colloid systems. Phys. Rev. Lett. 87:168103.
14. Briantais, J. M., C. Vernotte, J. Olive, and F.-A. Wollman. 1984. Kinetics of cation-induced changes of photosystem II fluorescence and of lateral distribution of the two photosystems in the thylakoid membranes of pea chloroplasts. Biochim. Biophys. Acta. 766:1-8.
15. Chou, T., K. S. Kim, and G. Oster. 2001. Statistical thermodynamics of membrane bending-mediated protein-protein attractions. Biophys. J. 80:1075-1087.
16. Chow, W. S. 1984. Electron transport, photophosphorylation and thylakoid stacking. In Advances in Photosynthesis Research, Vol. 3. Kluwer Academic Publishers, Dordrecht, the Netherlands. pp.83-86.
17. Chow, W. S. 1999. Grana formation: entropy-assisted local order in chloroplasts? Aust. J. Plant Physiol. 26:641-647.
18. Dickman, R., and A. Yethiraj. 1994. Polymer-induced forces between colloidal particles. A Monte-Carlo simulation. J. Chem. Phys. 100:4683-4690.
19. Drepper, F., I. Carlberg, B. Andersson, and W. Haehnel. 1993. Lateral diffusion of an integral membrane protein: Monte Carlo analysis of the migration of phosphorylated light-harvesting complex II in the thylakoid membrane. Biochemistry. 32:11915-11922.
20. Ermak, D. L. 1975. A computer simulation of charged particles in solution. I. Technique and equilibrium properties. J. Chem. Phys. 62:4189-4196.
21. de Gennes, P. G. 1992. Simple Views On Condensed Matter. World Scientific, Singapore.
22. Gennis, R. B. 1989. Biomembranes: Molecular Structure and Function. Springer-Verlag, New York.
23. Golestanian, R., M. Goulian, and M. Kadar. 1996. Fluctuation-induced interactions between rods on membranes and interfaces. Eur. Phys. Lett. 33:241-245.
24. Goulian, M., R. Bruinsma, and P. Pincus. 1993. Long range forces in heterogeneous fluid membranes. Eur. Phys. Lett. 22:145-150. Erratum. Eur. Phys. Lett. 23:155.
25. Halperin, B. I., and P. C. Hohenberg. 1969. Scaling laws for dynamic critical phenomena. Phys. Rev. 177:952-971.
26. Haltia, T., and E. Freire. 1995. Forces and factors that contribute to the structural stability of membrane proteins. Biochim. Biophys. Acta. 1241:295-322.
27. Heimburg, T., and R. L. Biltonen. 1996. A Monte Carlo simulation study of protein-induced heat capacity changes and lipid-induced protein clustering. Biophys. J. 70:84-96.
28. Helfrish, P., and E. Jakobsson. 1990. Calculation of deformation energies and conformations in lipid membranes containing gramicidin channels. Biophys. J. 57:1075-1084.
29. Huang, H. W. 1986. Deformation free energy of bilayer membrane and its effects on gramicidin channel lifetime. Biophys. J. 50:1061-1070.
30. Israelachvili, J. N. 1992. Intermolecular and Surface Forces. Academic Press, London.
31. Itoh, S. 1978. Membrane surface potential and the reactivity of the system II primary electron accepter to charged electron carriers in the medium. Biochim. Biophys. Acta. 504:324-340.
32. Itoh, S. 1979. Surface potential and reaction of the membrane-bound electron transfer components: reaction of P-700 in sonicated chloroplasts with redox reagents. Biochim. Biophys. Acta. 548:579-595.
33. Kadanoff, L. P. 1966. The introduction of the idea that exponents could be derived from real-space scaling arguments. Physics. 2:263-273.
34. Kim, K. S., J. Neu, and G. Oster. 1998. Curvature-mediated interactions between membrane proteins. Biophys. J. 75:2274-2291.
35. Kirchhoff, H., S. Horstmann, and E. Weis. 2000. Control of the photosynthetic electron transport by PQ diffusion microdomains in thylakoids of higher plants. Biochim. Biophys. Acta. 1459:148-168.
36. Kleinschmidt, J. H., and D. Marsh. 1997. Spin-label electron spin resonance studies on the interactions of lysine peptides with phospholipid membranes. Biophys. J. 73:2546-2555.
37. Kuhlbrandt, W., D. N. Wang, and Y. Fujiyoshi. 1994. Atomic model of plant light-harvesting complex by electron crystallography. Nature. 367:614-621.
38. Lague, P., M. J. Zuckermann, and B. Roux. 2000. Lipid-mediated interactions between intrinsic membrane proteins: A theoretical study based on integral equations. Biophys. J. 79:2867-2879.
39. Levin, Y. 1999. When do like charges attract? Physica A. 265:432-439.
40. Marcelja, S. 1976. Lipid-mediated protein interaction in membranes. Biochim. Biophys. Acta. 455:1-7.
41. Mao, Y., M. E. Cates, and H. N. W. Lekkerkerker. 1995. Depletion force in colloidal systems. Physica A. 222:10-24.
42. Mouritsen, O., and M. Bloom. 1984. Mattress model of lipid-protein interactions in membranes. Biophys. J. 46:141-153.
43. Mullet, J. E., and C. J. Arntzen. 1980. Simulation of grana stacking in a model membrane system: mediation by a purified light-harvesting pigment-protein complex from chloroplasts. Biochim. Biophys. Acta. 589:100-117.
44. Murata, N., S.-I. Higashi, and Y. Fujimura. 1990. Glycerolipids in various preparations of Photosystem II from Spinach chloroplasts. Biochim. Biophys. Acta. 1019:261-268.
45. Nenonene, E. K., and M. Fragata. 1998. Interaction of Photosystem II proteins with nonaggregated membranes constituted of phosphatidylglycerol and the electrically neutral phosphatidylcholine enhances the oxygen-evolving activity. Chem. Phys. Lipids. 91:97-107.
46. Netz, R. R., and P. Pincus. 1995. Inhomogeneous fluid membranes: Segregation, ordering and effective rigidity. Phys. Rev. E. 52:4114-4128.
47. Netz, R. R. 1995. Complete unbinding of fluid membranes in the presence of short-range forces. Phys. Rev. E. 51:2286-2294.
48. Parsegian, V. A. 2000. Physical Forces Organizing Biomolecules. www.biophysics.org/biophys/society/btol/.
49. Pearson, L. T., J. Edelman, and S. I. Chan. 1984. Statistical mechanics of lipid membranes. Protein correlation function and lipid ordering. Biophys. J. 45:863-871.
50. Pink, D. A., and D. Chapman. 1979. Protein-lipid Interactions in bilayer lipids: a lattice model. Proc. Natl. Acad. Sci. USA. 76:1542-1546.
51. Poon, W. C. K., and M. D. Haw. 1997. Mesoscopic structure formation in colloidal aggregation and gelation. Adv. Colloid Interface Sci. 73:711-26.
52. Rojdestvenski, I., A. G. Ivanov, M. G. Cottam, and G. Öquist. 2000. A two-dimensional many body system with competing interactions as a model for segregation of photosystems in thylakoids of green plants. Eur. Biophys. J. 29:214-220.
53. Rojdestvenski, I., A. G. Ivanov, M. G. Cottam, A. Borodich, N. P. A. Huner, and G. Öquist. 2002. Segregation of photosystems in thylakoid membranes as a critical phenomenon. Biophys. J. 82:1719-1730.
54. Rubin, B., W. Chow, and J. Barber. 1981. Experimental and theoretical consideration of mechanisms controlling cation effects on thylakoid membrane stacking and chlorophyll fluorescence. Biochim. Biophys. Acta. 634:174-190.
55. Sanghiran, V., and K. S. Schmitz. 2000. Structure of the ion cloud and the effective charge of spherical colloidal particles: Brownian Dynamics simulations. Langmuir. 16:7566-7574.
56. Sanyal, S., and A. K. Sood. 1995. Brownian dynamics simulation of dense binary colloidal mixtures. I. Structural evolution and dynamics. Phys. Rev. E. 52:4154-4167.
57. Sanyal, S., and A. K. Sood. 1998. Relaxation dynamics in dense binary colloidal mixtures: Brownian dynamics simulations. Phys. Rev. E. 57:908-923.
58. Schroder, H. 1977. Aggregation of proteins in membranes. An example of fluctuation-induced interactions in liquid crystals. J. Chem. Phys. 67:1617-1619.
59. Sens, P., and S. A. Safran. 2000. Inclusions induced phase separation in mixed lipid film. Eur. Phys. J. 1:237-248.
60. Sintes, T., and A. Baumgartner. 1997. Protein attraction in membranes induced by lipid fluctuations. Biophys. J. 73:2251-2259.
61. Soga, K. G., J. R. Melrose, and R. C. Ball. 1999. Metastable states and the kinetics of colloid phase separation. J. Chem. Phys. 110:2280-2288.
62. Sogami, I., and N. Ise. 1984. On the electrostatic interaction in macroscopic solutions. J. Chem. Phys. 81:6320-6332.
63. Sperotto, M., and O. Mouritsen. 1991. Mean-field and Monte-Carlo simulation studies of the lateral distribution of proteins in membranes. Eur. Biophys. J. 19:157-168.
64. Staehelin, L. A., and C. J. Arntzen. 1983. Regulation of chloroplast membrane function: protein phosphorylation changes the spatial organization of membrane components. J. Cell Biol. 97:1327-1337.
65. Staehelin, L. A., and G. W. M. van der Staay. 1996. Structure, composition, functional organization and dynamic properties of thylakoid membranes. In Oxygenic Photosynthesis: The Light Reactions. D. R. Ort, and C. F. Yocum, editors. C.F. Kluwer Academic Publishers, Dordrecht, the Netherlands. pp. 11-30.
66. Stys, D. 1995. Stacking and separation of photosystem I and photosystem II in plant thylakoid membranes: A physico-chemical view. Physiol. Plant. 95:651-657.
67. Thorne, S. W., and J. T. Duniec. 1983. The physical principles of energy transduction in chloroplast thylakoid membranes. Q. Rev. Biophys. 16:197-278.
68. Trissl, H. W., and C. Wilhelm. 1993. Why do thylakoid membranes from higher plants form grana stacks? TIBS. 18:415-419.
69. Van Roon, H., J. F. L. van Breemen, F. L. de Weerd, J. P. Dekker, and E. J. Boekema. 2000. Solubilization of green plant thylakoid membranes with n-dodecyl-α,d-maltoside. Implications for the structural organization of the Photosystem II, Photosystem I, ATP synthase and cytochrome b6f complexes. Photosynth. Res. 64:155-166.
70. Verma, R., J. C. Crocker, T. C. Lubensky, and A. G. Yodh. 2000. Attraction between hard colloidal spheres in semiflexible polymer solutions. Macromolecules. 33:177-186.
71. Whitmarsh, J. and Govindjee. 1999. The photosynthetic process. At www.life.uiuc.edu/govindjee/.
72. Wollman, F.-A., and B. Diner. 1980. Cation control of fluorescence emission, light scatter, and membrane stacking in pigment mutants of Chlamidomonas reinhardtii. Arch. Biochem. Biophys. 201:646-658.
73. Wu, J., D. Bratko, and J. M. Praunsnitz. 1998. Interaction between like-charged colloidal spheres in electrolyte solutions. Proc. Natl. Acad. Sci. USA. 95:15169-15172.