Kirchhoff, Helmut, Haferkamp, Silvia, Allen, John F., Epstein, D. B. A. and Mullineaux, Conrad W.. (2008) Protein diffusion and macromolecular crowding in thylakoid membranes. Plant Physiology, Volume 146 (Number 4). pp. 1571-1578. ISSN 0032-0889

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Abstract

The photosynthetic light reactions of green plants are mediated by chlorophyll-binding protein complexes located in the thylakoid membranes within the chloroplasts. Thylakoid membranes have a complex structure, with lateral segregation of protein complexes into distinct membrane regions known as the grana and the stroma lamellae. It has long been clear that some protein complexes can diffuse between the grana and the stroma lamellae, and that this movement is important for processes including membrane biogenesis, regulation of light harvesting, and turnover and repair of the photosynthetic complexes. In the grana membranes, diffusion may be problematic because the protein complexes are very densely packed (approximately 75% area occupation) and semicrystalline protein arrays are often observed. To date, direct measurements of protein diffusion in green plant thylakoids have been lacking. We have developed a form of fluorescence recovery after photobleaching that allows direct measurement of the diffusion of chlorophyll-protein complexes in isolated grana membranes from Spinacia oleracea. We show that about 75% of fluorophores are immobile within our measuring period of a few minutes. We suggest that this immobility is due to a protein network covering a whole grana disc. However, the remaining fraction is surprisingly mobile (diffusion coefficient 4.6 +/- 0.4 x 10(-11) cm(2) s(-1)), which suggests that it is associated with mobile proteins that exchange between the grana and stroma lamellae within a few seconds. Manipulation of the protein-lipid ratio and the ionic strength of the buffer reveals the roles of macromolecular crowding and protein-protein interactions in restricting the mobility of grana proteins.

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Item Type:	Journal Article
Subjects:	Q Science > QK Botany Q Science > QP Physiology
Divisions:	Faculty of Science > Mathematics
Library of Congress Subject Headings (LCSH):	Thylakoids, Proteins, Diffusion, Macromolecules
Journal or Publication Title:	Plant Physiology
Publisher:	American Society of Plant Biologists
ISSN:	0032-0889
Date:	April 2008
Volume:	Volume 146
Number:	Number 4
Number of Pages:	8
Page Range:	pp. 1571-1578
Identification Number:	10.1104/pp.107.115170
Status:	Peer Reviewed
Publication Status:	Published
Access rights to Published version:	Restricted or Subscription Access
Funder:	Deutsche Forschungsgemeinschaft (DFG), Royal Society (Great Britain), Biotechnology and Biological Sciences Research Council (Great Britain), Wellcome Trust (London, England), Leverhulme Trust (LT)
References:	Albertsson PA (2001) A quantitative model of the domain structure of the photosynthetic membrane. Trends Plant Sci 6: 349–354 Allen JF, Forsberg J (2001) Molecular recognition in thylakoid structure and function. Trends Plant Sci 6: 317–326 Baena-Gonzalez E, Aro EM (2002) Biogenesis, assembly and turnover of photosystem II units. Philos Trans R Soc Lond B Biol Sci 357: 1451–1459 Barber J (1982) Influence of surface charges on thylakoid structure and function. Annu Rev Plant Physiol 33: 261–295 Barber J, Andersson B (1992) Too much of a good thing: light can be bad for photosynthesis. Trends Biochem Sci 17: 61–66 Consoli E, Croce R, Dunlap DD, Finzi L (2005) Diffusion of light-harvesting complex II in the thylakoid membranes. EMBO Rep 6: 782–786 Dekker JP, Boekema EJ (2005) Supramolecular organization of thylakoid membrane proteins in green plants. Biochim Biophys Acta 1706: 12–39 Drepper F, Carlberg I, Andersson B, HaehnelW(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 Ducheˆne S, Siegenthaler PA (2000) Do glycerolipids display lateral heterogeneity in the thylakoid membrane? Lipids 35: 739–744 Dunahay TG, Staehelin LA, Seibert M, Ogilvie PD, Berg SP (1984) Structural, biochemical and biophysical characterization of four oxygenevolving photosystem II preparations from spinach. Biochim Biophys Acta 764: 179–193 Engelman DM (2005) Membranes are more mosaic than fluid. Nature 438: 578–580 Gambin Y, Lopez-Esparza R, Reffay M, Sierecki E, Gov NS, Genest M, Hodges RS, Urbach W (2006) Lateral mobility of proteins in liquid membranes revisited. Proc Natl Acad Sci USA 103: 2098–2102 Haferkamp S, Kirchhoff H (2008) Significance of molecular crowding in grana membranes of higher plants for light harvesting by photosystem II. Photosynth Res 95: 129–134 HarrisonMA, Allen JF (1992) Protein phosphorylation and Mg21 influence light harvesting and electron transport in chloroplast thylakoid membrane material containing only the chlorophyll-a/b-binding light-harvesting complex of photosystem II and photosystem I. Eur J Biochem 204: 1107–1114 Haugland RP (2005) The Handbook: A Guide to Fluorescent Probes and Labeling Technologies. Invitrogen Corporation, Carlsbad, CA Jennings RC, Bassi R, Garlaschi FM, Dainese P, Zucchelli G (1993) Distribution of the chlorophyll spectral forms in the chlorophyll-protein complexes of photosystem II antenna. Biochemistry 32: 3203–3210 Jin S, Verkman AS (2007) Single particle tracking of complex diffusion in membranes: simulation and detection of barrier, raft, and interaction phenomena. J Phys Chem B 111: 3625–3632 Kirchhoff H, Borinski M, Lenhert S, Chi L, Bu¨ chel C (2004a) Transversal and lateral exciton energy transfer in grana thylakoids of spinach. Biochemistry 43: 14508–14516 Kirchhoff H, Mukherjee U, Galla HJ (2002) Molecular architecture of the thylakoid membrane: lipid diffusion space for plastoquinone. Biochemistry 41: 4872–4882 Kirchhoff H, Tremmel I, HaaseW, Kubitscheck U (2004b) Supramolecular photosystem II organization in grana thylakoid membranes: evidence for a structured arrangement. Biochemistry 43: 9204–9213 Mullineaux CW, Tobin MJ, Jones GR (1997) Mobility of photosynthetic complexes in thylakoid membranes. Nature 390: 421–424 Nelson N, Ben-Shem A (2004) The complex architecture of oxygenic photosynthesis. Nat Rev Mol Cell Biol 5: 971–982 Sarcina M, Bouzovitis N, Mullineaux CW (2006) Mobilization of photosystem ii induced by intense red light in the Cyanobacterium Synechococcus sp PCC7942. Plant Cell 18: 457–464 SarcinaM,Mullineaux CW(2004)Mobility of the IsiA chlorophyll-binding protein in cyanobacterial thylakoid membranes. J Biol Chem 279: 36514– 36518 Saxton MJ (1989) Lateral diffusion in an archipelago. Distance dependence of the diffusion coefficient. Biophys J 56: 615–622 Schiller H, Dau H (2000) Preparation protocols for high-activity photosystem II membrane particles of green algae and higher plants, pH dependence of oxygen evolution and comparison of S2-state multiline signal by X-band EPR spectroscopy. J Photochem Photobiol B 55: 138–144 Standfuss J, Terwisscha van Scheltinga AC, Lamborghini M, Ku¨ hlbrandt W (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea light-harvesting complex at 2.5 A resolution. EMBO J 24: 919–928 Tremmel IG, Kirchhoff H, Weis E, Farquhar GM (2003) Dependence of plastoquinol diffusion on the shape, size, and density of integral thylakoid proteins. Biochim Biophys Acta 1607: 97–109 Webb MS, Green BR (1989) Permeability properties of large unilamellar vescicles of thylakoid lipids. Biochim Biophys Acta 984: 41–49
URI:	http://wrap.warwick.ac.uk/id/eprint/29887

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