Visualizing the mobility and distribution of chlorophyll proteins in higher plant thylakoid membranes: Effects of photoinhibition and protein phosphorylation

Plant Journal

Volumn 62, Issue 6, 2010, Pages 948-959

  Goral, Tomasz K ^a   Johnson, Matthew P ^a   Brain, Anthony P R ^b   Kirchhoff, Helmut ^c   Ruban, Alexander V ^a   Mullineaux, Conrad W ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Chloroplast; Fluorescence microscopy; Freeze fracture electron microscopy; Photoinhibition; Protein phosphorylation; Thylakoid membrane

Indexed keywords

ARABIDOPSIS; CHLOROPHYLL FLUORESCENCE; CORE PROTEINS; FLUID STATE; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; FREEZE FRACTURE ELECTRON MICROSCOPY; HIGHER PLANTS; LASER SCANNING; LIGHT CONDITIONS; LIGHT-HARVESTING; LIGHT-HARVESTING COMPLEX; MEMBRANE SYSTEM; PACKING DENSITY; PHOSPHORYLATION OF PHOTOSYSTEM II; PHOTOINHIBITION; PHOTOSYSTEM-II; PROTEIN DIFFUSION; PROTEIN KINASE; PROTEIN MOBILITY; PROTEIN PHOSPHORYLATION; REAL TIME; SPINACIA OLERACEA; THYLAKOID MEMBRANES; THYLAKOID PROTEIN COMPLEXES; THYLAKOID PROTEINS; TIME-SCALES; WILD TYPES;

CHLOROPHYLL; FLUORESCENCE; FLUORESCENCE MICROSCOPY; FRACTURE; HARVESTING; MEMBRANES; PHOSPHORYLATION; PHOTOBLEACHING; PORPHYRINS; REPAIR; SCANNING ELECTRON MICROSCOPY;

PROTEINS;

CHLOROPHYLL; VEGETABLE PROTEIN; LIGHT HARVESTING SYSTEM; PHOTOSYSTEM II;

ARABIDOPSIS; ARTICLE; CONFOCAL MICROSCOPY; ELECTRON MICROSCOPY; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; IMAGE PROCESSING; LIGHT HARVESTING SYSTEM; METABOLISM; PHOSPHORYLATION; PHOTOSYSTEM II; PROTEIN TRANSPORT; SPINACH; THYLAKOID; ULTRASTRUCTURE;

ARABIDOPSIS; CHLOROPHYLL; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; IMAGE PROCESSING, COMPUTER-ASSISTED; LIGHT-HARVESTING PROTEIN COMPLEXES; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON; PHOSPHORYLATION; PHOTOSYSTEM II PROTEIN COMPLEX; PLANT PROTEINS; PROTEIN TRANSPORT; SPINACIA OLERACEA; THYLAKOIDS;

ARABIDOPSIS; EMBRYOPHYTA; SPINACIA OLERACEA;

EID: 77953523697     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2010.04207.x     Document Type: Article

References (38)

1. Albertsson, P.-Å. (2001) A quantitative model of the domain structure of the photosynthetic membrane. Trends Plant Sci. 6, 349 354.
2. Allen, J.F. Forsberg, J. (2001) Molecular recognition in thylakoid structure and function. Trends Plant Sci. 6, 317 326.
3. Anderson, J.M. Andersson, B. (1982) The architecture of photosynthetic membranes - lateral and transverse organization. Trends Biochem. Sci. 7, 288 292.
4. Aro, E.-M., Virgin, I. Andersson, B. (1993) Photoinhibition of Photosystem II. Inactivation, protein damage and turnover. Biochim. Biophys. Acta, 1143, 113 134.
5. Baena-Gonzalez, E. Aro, E.-M. (2002) Biogenesis, assembly and turnover of photosystem II units. Philos. Trans. R. Soc. Lond. B Biol. Sci. 357, 1451 1459.
6. Bonardi, V., Pesaresi, P., Becker, T., Schleiff, E., Wagner, R., Pfannschmidt, T., Jahns, P. Leister, D. (2005) Photosystem II core phosphorylation and photosynthetic acclimation require two different protein kinases. Nature, 437, 1179 1182.
7. Branton, D., Bullivant, S., Gilula, N.B. et al. (1975) Freeze-etching nomenclature. Science, 190, 54 56.
8. Chuartzmann, S.G., Nevo, R., Shimoni, E., Charuvi, D., Kiss, V., Ohad, I., Brumfeld, V. Reich, Z. (2008) Thylakoid membrane remodeling during state transitions in Arabidopsis. Plant Cell, 20, 1029 1039.
9. Consoli, E., Croce, R., Dunlap, D.D. Finzi, L. (2005) Diffusion of light harvesting complex II in the thylakoid membranes. EMBO Rep. 6, 782 786.
10. Crouchman, S., Ruban, A. Horton, P. (2006) PsbS enhances non-photochemical fluorescence quenching in the absence of zeaxanthin. FEBS Lett. 580, 2053 2058.
11. Dekker, J.P. Boekema, E.J. (2005) Supramolecular organization of thylakoid membrane proteins in green plants. Biochim. Biophys. Acta, 1706, 12 39.
12. Drepper, F., Carlberg, I., Andersson, B. Haehnel, W. (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.
13. Fristedt, R., Willig, A., Granath, P., Crèvecoeur, M., Rochaix, J.-D. Vener, A.V. (2009) Phosphorylation of Photosystem II controls functional macroscopic folding of photosynthetic membranes in Arabidopsis. Plant Cell, 21, 3950 3964.
14. Garab, G. Manella, C.A. (2008) Reply: on three-dimensional models of higher-plant thylakoid networks: elements of consensus, controversies and future experiments. Plant Cell, 20, 2549 2551.
15. Habeeb, A.F.S.A. Hiramoto, R. (1968) Reaction of proteins with glutaraldehyde. Arch. Biochem. Biophys. 126, 16 26.
16. Horton, P., Ruban, A.V. Walters, R.G. (1996) Regulation of light-harvesting in green plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 655 684.
17. Kirchhoff, H., Mukherjee, U. Galla, H.J. (2002) Molecular architecture of the thylakoid membrane: lipid diffusion space for plastoquinone. Biochemistry, 41, 4872 4882.
18. Kirchhoff, H., Tremmel, I., Haase, W. Kubitscheck, U. (2004) Supramolecular photosystem II organization in grana thylakoid membranes: evidence for a structured arrangement. Biochemistry, 43, 9204 9213.
19. Kirchhoff, H., Haferkamp, S., Allen, J.F., Epstein, D.B.A. Mullineaux, C.W. (2008a) Protein diffusion and macromolecular crowding in thylakoid membranes. Plant Physiol. 146, 1571 1578.
20. Kirchhoff, H., Lenhert, S., Büchel, C., Chi, L. Nield, J. (2008b) Probing the organization of Photosystem II in photosynthetic membranes by atomic force microscopy. Biochemistry, 47, 431 440.
21. Lenn, T., Leake, M.C. Mullineaux, C.W. (2008) Clustering and dynamics of cytochrome bd-I complexes in the Escherichia coli plasma membrane in vivo. Mol. Microbiol. 70, 1397 1407.
22. Long, S.P., Humphries, S. Falkowski, P.G. (1994) Photoinhibition of photosynthesis in nature. Annu. Rev. Plant Physiol. Plant Mol. Biol. 45, 633 662.
23. Maxwell, K. Johnson, G.N. (2000) Chlorophyll fluorescence - a practical guide. J. Exp. Bot. 51, 659 668.
24. Mullineaux, C.W. Sarcina, M. (2002) Probing the dynamics of photosynthetic membranes with Fluorescence Recovery after Photobleaching. Trends Plant Sci. 7, 237 240.
25. Mullineaux, C.W., Tobin, M.J. Jones, G.R. (1997) Mobility of photosynthetic complexes in thylakoid membranes. Nature, 390, 421 424.
26. Mustárdy, L., Buttle, K., Steinbach, G. Garab, G. (2008) The three-dimensional network of the thylakoid membranes in plants: quasihelical model of the granum-stroma assembly. Plant Cell, 20, 2552 2557.
27. Napier, J.A. Barnes, S.A. (1995) The isolation of intact chloroplasts. Methods Mol. Biol. 49, 355 360.
28. Porra, R.J., Thompson, W.A. Kriedemann, P.E. (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophyll a and chlorophyll b extracted with 4 different solvents - verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim. Biophys. Acta, 975, 384 394.
29. Reits, E.A.J. Neefjes, J.J. (2001) From fixed to FRAP: measuring protein mobility and activity in living cells. Nat. Cell Biol. 3, 145 147.
30. Rintamäki, E., Kettunen, R. Aro, E.-M. (1996) Differential D1 dephosphorylation in functional and photodamaged photosystem II centers. Dephosphorylation is a prerequisite for degradation of damaged D1. J. Biol. Chem. 271, 14870 14875.
31. Ruban, A.V., Berera, R., Ilioaia, C., van Stokkum, I.H.M., Kennis, J.T.M., Pascal, A.A., van Amerongen, H., Robert, B., Horton, P. van Grondelle, R. (2007) Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature, 450, 575 578.
32. Sarcina, M., Murata, N., Tobin, M.J. Mullineaux, C.W. (2003) Lipid diffusion in the thylakoid membranes of the cyanobacterium Synechococcus sp.: effect of fatty acid desaturation. FEBS Lett. 553, 295 298.
33. Sarcina, M., Bouzovitis, N. Mullineaux, C.W. (2006) Mobilization of Photosystem II induced by intense red light in the cyanobacterium Synechococcus sp. PCC7942. Plant Cell, 18, 457 464.
34. Shimoni, E., Rav-Hon, O., Ohad, I., Brumfeld, V. Reich, Z. (2005) Three-dimensional organization of higher-plant chloroplast thylakoid membranes revealed by electron tomography. Plant Cell, 17, 2580 2586.
35. Staehelin, L.A. (2003) Chloroplast structure: from chlorophyll granules to supra-molecular architecture of thylakoid membranes. Photosynth. Res. 76, 185 196.
36. Staehelin, L.A. Arntzen, C.J. (1983) Regulation of chloroplast membrane function: protein phosphorylation changes the spatial organization of membrane components. J. Cell Biol. 97, 1327 1337.
37. Stocking, C.R. Franceschi, V.R. (1982) Some properties of the chloroplast envelope as revealed by electrophoretic mobility studies of intact chloroplasts. Plant Physiol. 70, 1255 1259.
38. Tikkanen, M., Nurmi, M., Kangasjärvi, S. Aro, E.-M. (2008) Core protein phosphorylation facilitates the repair of photodamaged photosystem II at high light. Biochim. Biophys. Acta, 1777, 1432 1437.