Granal stacking of thylakoid membranes in higher plant chloroplasts: The physicochemical forces at work and the functional consequences that ensue

Photochemical and Photobiological Sciences

Volumn 4, Issue 12, 2005, Pages 1081-1090

  Chow, Wah Soon ^a   Kim, Eun Ha ^a   Horton, Peter ^b   Anderson, Jan M ^a  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTENNA; ARTICLE; CELL MEMBRANE FLUIDITY; CELL ULTRASTRUCTURE; CHLOROPLAST; ELECTRIC ACTIVITY; ENERGY TRANSFER; HYDRATION; LIGHT HARVESTING SYSTEM; MOLECULAR INTERACTION; NONPHOTOCHEMICAL QUENCHING; PH MEASUREMENT; PHOTOCHEMICAL EFFICIENCY; PHOTOSYNTHETIC PHOSPHORYLATION; PHOTOSYSTEM I; PHOTOSYSTEM II; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN DEGRADATION; STEREOSPECIFICITY; STROMA; THYLAKOID MEMBRANE;

EMBRYOPHYTA;

EID: 29144458149     PISSN: 1474905X     EISSN: 14749092     Source Type: Journal    
DOI: 10.1039/b507310n     Document Type: Article

References (105)

1. L. Mustárdy G. Garab Granum revisited. A three-dimensional model-where things fall into place Trends Plant Sci. 2003 8 117-122.
2. J. Barber Membrane surface charges and potentials in relation to photosynthesis Biochim. Biophys. Acta 1980 594 253-308.
3. F. V. Mercer A. J. Hodge A. B. Hope J. D. McLean The structure and swelling properties of Nitella chloroplasts Aust. J. Biol. Sci. 1955 8 1-18.
4. J. Barber Influence of surface charges on thylakoid structure and function Ann. Rev. Plant Physiol. 1982 33 261-295.
5. W. S. Chow L. Qian D. J. Goodchild J. M. Anderson Photosynthetic acclimation of Alocasia macrorrhiza(L.) G. Don to growth irradiance: structure, function and composition of chloroplasts Aust. J. Plant Physiol. 1988 15 107-122.
6. W. S. Chow S. W. Thorne J. T. Duniec M. J. Sculley N. K. Boardman The stacking of chloroplast thylakoids. Effects of cation screening and binding, studied by the digitonin method Arch. Biochem. Biophys. 1980 201 347-355.
7. J. Barber W. S. Chow A mechanism for controlling the stacking and unstacking of chloroplast thylakoid membranes FEBS Lett. 1979 105 5-10.
8. S. Izawa N. E. Good Effect of salts and electron transport on the conformation of isolated chloroplasts. II. Electron microscopy Plant Physiol. 1966 41 544-552.
9. S. Murakami L. Packer Protonation and chloroplast membrane structure J. Cell Biol. 1970 47 332-351.
10. B. T. Rubin W. S. Chow J. Barber Experimental and theoretical considerations of mechanisms controlling cation effects on thylakoid membrane stacking and chlorophyll fluorescence Biochim. Biophys. Acta 1981 634 174-190.
11. E. L. Gross S. H. Prasher Correlation between monovalent cation induced decrease in chlorophyll a fluorescence and chloroplast structural changes Arch. Biochem. Biophys. 1974 164 460-468.
12. J. T. Duniec S. W. Thorne An analysis of the effect of mono- and di-valent cations on the forces between charged lipid membranes with special reference to the grana thylakoids of chloroplasts J. Theor. Biol. 1979 79 473-484.
13. J. Barber J. Mills A. Love Electrical diffuse layers and their influence on photosynthetic processes FEBS Lett. 1977 74 174-181.
14. B. T. Rubin J. Barber The role of membrane surface charge in the control of photosynthetic processes and the involvement of electrostatic screening Biochim. Biophys. Acta 1980 592 87-102.
15. W. S. Chow C. Miller J. M. Anderson Surface charges, the heterogeneous lateral distribution of the two photosystems, and thylakoid stacking Biochim. Biophys. Acta 1991 1057 69-77.
16. M. J. Sculley J. T. Duniec S. W. Thorne W. S. Chow N. K. Boardman Quantitative analysis of the balance of forces between thylakoid membranes of chloroplasts, and the role of divalent cations Arch. Biochem. Biophys. 1980 201 339-346.
17. I. M. Nir D. C. Pease Chloroplast organisation and the ultrastructural location of Photosystem I and II J. Ultrastruct. Res. 1973 42 534-550.
18. J. P. Dekker E. J. Boekema Supramolecular organization of the thylakoid membrane proteins in green plants Biochim. Biophys. Acta 2005 1706 12-39.
19. J. Marra J. Israelachvili Direct measurement of forces between phosphatidylcholine and phosphatidylethanolamine bilayers in aqueous electrolyte solutions Biochemistry 1985 24 4608-4618.
20. 3 solutions Nature 1976 262 774-776.
21. D. M. LeNeveu R. P. Rand V. A. Parsegian Measurement of forces between lecithin bilayers Nature 1976 259 601-603.
22. A. C. Cowley N. L. Fuller R. P. Rand V. A. Parsegian Measurement of repulsive forces between charged phospholipids bilayers Biochemistry 1978 17 3163-3168.
23. J. N. Israelachvili R. M. Pashley Molecular layering of water at surfaces and origin of repulsive hydration forces Nature 1983 306 249-250.
24. S. W. Thorne J. T. Duniec The physical principles of energy transduction in chloroplasts thylakoid membranes Quart. Rev. Biophys. 1983 16 197-278.
25. W. S. Chow Grana formation: entropy-assisted local order in chloroplasts? Aust. J. Plant Physiol. 1999 26 641-647.
26. L. Onsager The effect of shape on the interaction of colloid particles Ann. N. Y. Acad. Sci. 1949 51 627-659.
27. M. Adams Z. Dogic S. L. Keller S. Fraden Entropically driven microphase transitions in mixtures of colloid rods and spheres Nature 1998 393 349-351.
28. A. D. Dinsmore A. G. Yodh D. J. Pine Entropic control of particle motion using passive surface microstructures Nature 1996 383 239-242.
29. E.-H. Kim W. S. Chow P. Horton J. M. Anderson Entropy-assisted stacking of thylakoid membranes Biochim. Biophys. Acta 2005 1708 187-195.
30. B. Andersson J. M. Anderson Lateral heterogeneity in the distribution of chlorophyll-protein complexes of the thylakoid membranes of spinach chloroplasts Biochim. Biophys. Acta 1980 593 427-440.
31. L. A. Stahelin Reversible particle movement associated with unstacking and restacking of chloroplast membranes in vitro J. Cell Biol. 1976 71 136-158.
32. W. S. Chow S. W. Thorne J. T. Duniec M. J. Sculley N. K. Boardman The stacking of chloroplast thylakoids: evidence for segregation of charged groups into nonstacked regions Arch. Biochem. Biophys. 1982 216 247-254.
33. W. S. Chow J. Barber Further studies of the relationship between cation-induced chlorophyll fluorescence and thylakoid membrane stacking changes Biochim. Biophys. Acta 1980 593 149-157.
34. A. Telfer, The importance of membrane surface electrical charge on the regulation of photosynthetic electron transport by reversible protein phosphorylation in Progress in Photosynthesis Research, ed. J. Biggins, Martinus Nijhoff, Dordrecht, 1987, vol. II, pp. 689–696.
35. Ben-Shem F. Frolow N. Nelson Crystal structure of plant Photosystem I Nature 2003 426 630-635.
36. N. Nelson A. Ben-Shem The complex architecture of oxygenic photosynthesis Nat. Rev. 2004 5 1-12.
37. J. E. Mullet C. J. Arntzen Simulation of grana stacking in a model membrane system. Mediation by a purified light-harvesting pigment-protein complex from chloroplasts Biochim. Biophys. Acta 1980 589 100-117.
38. J. F. Allen Protein phosphorylation in regulation of photosynthesis Biochim. Biophys. Acta 1992 1098 275-335.
39. H. Kirchhoff M. Borinski S. Lenhert L. Chi C. Büchel Transversal and lateral exciton energy transfer in grana thylakoids of spinach Biochemistry 2004 43 14508-14516.
40. J. Standfuss A. C. T. van Scheltinga M. Lamborghini W. Kühlbrandt Mechanisms of photoprotection and nonphotochemical quenching in pea light-harvesting complex at 2.5 Å resolution EMBO J. 2005 24 919-928.
41. D. Stys Stacking and separation of photosystem I and photosystem II in plant thylakoid membranes: A physico-chemical view Physiol. Plant. 1995 95 651-657.
42. B. R. Green, J. M. Anderson and W. W. Parson, Photosynthetic membranes and their light-harvesting antennas In Light-harvesting Antennas in Photosynthesis, ed. B. R. Green and W. W. Parsons, Kluwer Academic Publishers, Dordrecht/London/Boston, 2003, pp. 1–28.
43. B. E. S. Gunning O. M. Schwartz Confocal microscopy of thylakoid autofluorescence in relation to origin of grana and phylogeny in green algae Aust. J. Plant Physiol. 1999 26 695-708.
44. J. D. Pickett-Heaps Ultrastructure and differentiation in Chara sp. I. Vegetative cells Aust. J. Biol. Sci. 1967 20 539-551.
45. N. K. Boardman J. M. Anderson D. J. Goodchild Chlorophyll-protein complexes and structure of mature and developing chloroplasts Curr. Top. Bioenerg. 1978 8 36-109.
46. P. Homann Cation effects on the fluorescence of isolated chloroplasts Plant Physiol. 1969 44 932-936.
47. N. Murata Control of excitation transfer in photosynthesis I. Light-induced change of chlorophyll a fluorescence in Porphyridum cruentum Biochim. Biophys. Acta 1969 172 242-251.
48. N. Murata Control of excitation transfer in photosynthesis II. Magnesium ion dependent distribution of excitation energy between two pigment systems in spinach chloroplasts Biochim. Biophys. Acta 1969 189 171-181.
49. N. Murata Effects of monovalent cations on light energy distribution between two pigment systems of photosynthesis in isolated spinach chloroplasts Biochim. Biophys. Acta 1971 226 422-432.
50. U. W. Goodenough L. A. Stahelin Structural differentiation of stacked and unstacked chloroplast membranes J. Cell Biol. 1971 48 594-619.
51. C. J. Arntzen Dynamic structural features of chloroplasts lamellae Curr. Top. Bioenerg. 1978 8 111-160.
52. J. Barber, Energy transfer and its dependence on membrane properties in Chlorophyll Organisation and Energy Transfer in Photosynthesis, Ciba Foundation Symposium 61 (new series), Excerpta Medica, Amsterdam, 1979, pp. 283–304.
53. J. Barber An explanation for the relationship between salt-induced thylakoid stacking and the chlorophyll fluorescence changes associated with changes in spillover of energy from Photosystem II to Phototem I FEBS Lett. 1980 118 1-10.
54. 2+-induced rise of chlorophyll fluorescence from pea thylakoid membranes Biochim. Biophys. Acta 1981 638 69-74.
55. F.-A. Wollmann B. Diner Cation control of fluorescence emission, light scatter, and membrane stacking in pigment mutants of Chlamydomonas reinhardtii Arch. Biochem. Biophys. 1980 201 646-658.
56. G. Garab L. Mustárdy Role of LHCII-containing macrodomains in the structure, function and dynamics of grana Aust. J. Plant Physiol. 1999 26 649-658.
57. Rojdestvenski A. G. Ivanov M. G. Cottam A. Borodich N. P. A. Huner G. Öquist Segregation of photosystems in thylakoid membranes as a critical phenomenon Biophys. J. 2002 82 1719-1730.
58. A. Borodich I. Rojdestvenski M. G. Cottam J. M. Anderson G. Öquist Segregation of the photosystems in higher plant thylakoids and short- and long-term regulation by a mesoscopic approach J. Theor. Biol. 2003 225 431-441.
59. W. L. Butler Energy distribution in the photochemical apparatus of photosynthesis Annu. Rev. Plant Physiol. 1978 29 345-378.
60. J. M. Anderson Consequences of spatial separation of Photosystem 1 and 2 in thylakoid membranes of higher plant chloroplasts FEBS Lett. 1981 124 1-10.
61. J. M. Anderson The significance of grana stacking in chlorophyll b-containing chloroplasts Photobiochem. Photobiophys. 1982 3 225-241.
62. H.-W. Trissl C. Wilhelm Why do thylakoid membranes from higher plants form grana stacks? Trends Biochem. Sci. 1993 18 415-419.
63. G. Garab Z. Cseh L. Kovács S. Rajagopal Z. Várkonyi M. Wentworth L. Mustárdy A. Dér A. V. Ruban E. Papp A. Holzenburg P. Horton Light-induced trimer to monomer transition in the main light-harvesting antenna complex of plants, Thermo-optic mechanism Biochemistry 2002 41 15121-15129.
64. J. Andersson A. V. Ruban R. G. Walters C. Howard M. Wentworth P. Horton S. Jansson Absence of Lhcb1 and Lhcb2 proteins of the light-harvesting complex of photosystem II-effects on photosynthesis, grana stacking and fitness Plant J. 2003 35 350-361.
65. A. V. Ruban M. Wentworth A. E. Yakushevska J. Andersson P. J. Lee W. Keegstra J. P. Dekker E. J. Boekema S. Jansson P. Horton Plants lacking the main light-harvesting complex retain photosystem II macro-organization Nature 2003 421 648-652.
66. Bonaventura J. Myers Fluorescence and oxygen evolution from Chlorella pyrenoidosa Biochim. Biophys. Acta 1969 189 366-383.
67. P. Horton M. T. Black Activation of adenosine 5′-triphosphate-induced quenching of chlorophyll fluorescence by reduced plastoquinone FEBS Lett. 1980 119 141-144.
68. P. Horton M. T. Black Light-dependent quenching of chlorophyll fluorescence in pea chloroplasts induced by adenosine 5′-triphosphate Biochim. Biophys. Acta 1981 635 53-62.
69. M. T. Black P. Horton An investigation into the mechanistic aspects of excitation redistribution following thylakoid membrane protein phosphorylation Biochim. Biophys. Acta 1984 767 568-573.
70. M. T. Black P. Lee P. Horton Changes in the topography and function of thylakoid membranes following protein phosphorylation Planta 1986 168 330-336.
71. Lunde P. E. Jensen A. Haldrup J. Knoetzel, J. H. V. Scheller PSI-H subunit of photosystem I is essential for state transitions in plant photosynthesis Nature 2000 408 613-615.
72. J. F. Allen J. Forsberg Molecular recognition in thylakoid structure and function Trends Plant Sci. 2001 6 317-326.
73. A. A. Pascal Z. Liu K. Broess B. van Oort H. van Amerongen C. Wang P. Horton B. Robert W. Chang A. Ruban Molecular basis of photoprotection and control of photosynthetic light-harvesting Nature 2005 436 134-137.
74. P. Horton A. V. Ruban R. G. Walters Regulation of light harvesting in green plants Annu. Rev. Plant Physiol. Plant Mol. Biol. 1996 47 655-684.
75. P. Horton A. V. Ruban M. Wentworth Allosteric regulation of the light harvesting system of photosystem II Philos. Trans. R. Soc. London, Ser. B 2000 355 1361-1370.
76. R. Bassi S. Caffarri Lhc proteins and the regulation of photosynthetic light harvesting function by xanthophylls Photosynth. Res. 2000 64 243-256.
77. P. Horton M. Wentworth A. V. Ruban Control of the light harvesting function of chloroplast membranes: the LHCII-aggregation model for non-photochemical quenching FEBS Lett. 2005 579 4201-4206.
78. P. Horton Are grana necessary for regulation of light harvesting? Aust. J. Plant Physiol. 1999 26 659-669.
79. P. Horton A. V. Ruban Molecular design of the photosystem II light harvesting antenna: photosynthesis and photoprotection J. Exp. Bot. 2005 22 1-9.
80. D. M. Kramer T. J. Avenson G. E. Edwards Dynamic flexibility in the light reactions of photosynthesis governed by both electron and proton transfer reactions Trends Plant Sci. 2004 9 349-357.
81. J. M. Anderson E.-M. Aro Grana stacking and the protection of photosystem II membranes of higher plant leaves under sustained high irradiance: an hypothesis Photosynth. Res. 1994 41 315-326.
82. H.-Y. Lee Y.-N. Hong W. S. Chow Photoinactivation of Photosystem II complexes and photoprotection by non-functional neighbours in Capsicum annuum L. leaves Planta 2001 212 332-342.
83. W. S. Chow and E.-M. Aro, Photoinactivation and mechanisms of recovery in Photosystem II: The Water/Plastoquinone Oxido-Reductase in Photosynthesis, ed. T. Wydrzynski and K. Satoh, 2005, Springer, The Netherlands, in press.
84. E.-M. Aro I. Virgin B. Andersson Photoinhibition of Photosystem II. Inactivation, protein damage and turnover Biochim. Biophys. Acta 1993 1143 113-134.
85. E.-M. Aro M. Suorsa A. Rokka Y. Allahverdiyeva V. Paakkarinen A. Saleem N. Battchikova E. Rintamäki Dynamics of Photosystem II–a proteomic approach to thylakoid protein complexes J. Exp. Bot. 2005 56 347-356.
86. Baena-Gonzalez R. Barbato E.-M. Aro Role of PSII phosphorylation in the PSII repair cycle and oligomeric structure Planta 1999 208 196-204.
87. Rintamäki R. Kettunen E.-M. Aro Differential D1 dephosphorylation in functional and photodamaged Photosystem II centers. Dephosphorylation is a prerequisite for degradation of the damaged D1* J. Biol. Chem. 1996 271 14870-14875.
88. W. S. Chow The extent to which the spatial separation between photosystems I and II associated with granal formation limits noncyclic electron flow in isolated lettuce chloroplasts Arch. Biochem. Biophys. 1984 232 162-171.
89. W. S. Chow, Electron transport, photophosphorylation and thylakoid stacking In Advances in Photosynthesis Research, ed. C. Sybesma, Dr. W. Junk Publishers, The Hague, 1984, vol III, pp. 83–86.
90. E. C. Davies W. S. Chow B. R. Jordan A study of factors which regulate the membrane appression of lettuce thylakoids in relation to irradiance Photosynth. Res. 1986 9 359-370.
91. P. Scherrer U. Alexiev T. Marti H. G. Khorana M. P. Heyn Covalently bound pH-indicator dyes at selected extracellular or cytoplasmic sites in bacteriorhodopsin micelles and its delayed transfer from surface to bulk Biochemistry 1994 33 13684-13692.
92. J. M. Anderson The grana margins of plant thylakoid membranes Physiol. Plant. 1989 76 243-248.
93. P. Joliot A. Joliot Cyclic electron transfer in plant leaf Proc. Natl. Acad. Sci USA 2002 99 10209-10214.
94. P. Joliot A. Joliot Quantification of cyclic and linear flows in plants Proc. Natl. Acad. Sci USA 2005 102 4913-4918.
95. Öquist N. P. A. Huner Photosynthesis of overwintering evergreen plants Annu. Rev. Plant Biol. 2003 54 329-355.
96. A. P. Minton The influence of macromolecular crowding and macromolecular confinement on biochemical reactions in physiological media J. Biol. Chem. 2001 276 10577-10580.
97. C. P. Osborne D. J. Beerling B. H. Lomax W. G. Chaloner Biophysical constraints on the origin of leaves inferred from the fossil record Proc. Natl. Acad. Sci USA 2004 101 10306-10362.
98. K. R. Miller M. K. Lyon Do we really know why chloroplast membranes stack? Trends Biochem. Sci. 1985 10 219-222.
99. K. R. Miller A chloroplast membrane lacking photosystem I. Changes in unstacked membrane regions Biochim. Biophys. Acta 1980 592 143-152.
100. K. R. Miller The photosynthetic membrane Sci. Am. 1979 241 100-111.
101. 34, a photosystem I mutant Carlsberg Res. Commun. 1982 47 215-225.
102. A. Haldrup D. J. Simpson H. V. Scheller Down-regulation of the PSI-F subunit of Photosystem I (PSI) in Arabidopsis thaliana. The PSI-F subunit is essential for photoautotrophic growth and contributes to antenna function J. Biol. Chem. 2002 275 31211-31218.
103. P.-O. Arvidsson C. Sundby A model for the topology of the chloroplast thylakoid membranes Aust. J. Plant Physiol. 1999 26 687-694.
104. J. T. O. Kirk, The nature of plastids in The Plastids, J. T. O. Kirk and R. A. E. Tilney-Bassett, W. H. Freeman and Company, London, 1967, pp. 1–91.
105. L. Stryer, Photosynthesis in Biochemistry, L. Stryer, W. H. Freeman and Company, New York, 3rd edn, 1988, p. 517.