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Electron microscopy in structural studies of Photosystem II

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Abstract

Various techniques of electron microscopy (EM) such as ultrathin sectioning, freeze-fracturing, freeze-etching, negative staining and (cryo-)electron crystallography of two-dimensional crystals have been employed, since now, to obtain much of the structural information of the Photosystem II (PS II) pigment–protein complex at both low and high resolution. This review summarizes information about the structure of this membrane complex as well as its arrangement and interactions with the antenna proteins in thylakoid membranes of higher plants and cyanobacteria obtained by means of EM. Results on subunit organization, with the emphasis on the proteins of the oxygen-evolving complex (OEC), are compared with the data obtained by X-ray crystallography of cyanobacterial PS II.

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References

  • Andersson B and Akerlund HE (1978) Inside-out membrane vesicles isolated from spinach thylakoid. Biochim Biophys Acta 503: 462–472

    PubMed  CAS  Google Scholar 

  • Andersson B and Anderson JM (1980) Lateral heterogeneity in the distribution of chlorophyll–protein complexes of the thylakoid membranes of spinach chloroplasts. Biochim Biophys Acta 593: 427–440

    PubMed  CAS  Google Scholar 

  • Andersson B, Larsson C, Jansson C, Ljungberg U and Akerlund HE (1984) Immunological studies on the organization of proteins in photosynthetic oxygen evolution. Biochim Biophys Acta 766: 21–28

    CAS  Google Scholar 

  • Armond PA, Staehelin LA and Arntzen CJ (1977) Spatial relationship of Photosystem I, Photosystem II, and the light-harvesting complex in chloroplast membranes. J Cell Biol 73: 400–418

    PubMed  CAS  Google Scholar 

  • Aro EM, Virgin I and Andersson B (1993) Photoinhibition of Photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143: 113–134

    PubMed  CAS  Google Scholar 

  • Arvidsson PO and Sundby C (1999) A model for the topology of the chloroplast thylakoid membrane. Aust J Plant Physiol 26: 687– 694

    CAS  Google Scholar 

  • Baena-Gonzales E and Aro EM (2002) Biogenesis, assembly and turnover of Photosystem II units. Philos Trans R Soc London B Biol Sci 357: 1451–1459

    Google Scholar 

  • Bald D, Kruip J and Rogner M (1996) Supramolecular architecture of cyanobacterial thylakoid membranes: how is the phycobilisomes connected with the photosystems? Photosynth Res 49: 103–118

    CAS  Google Scholar 

  • Barber J (1998) Photosystem two. Biochim Biophys Acta 1365: 269–277

    PubMed  CAS  Google Scholar 

  • Barber J and Andersson B (1992) Too much of a good thing – light can be bad for photosynthesis. Trends Biochem Sci 17: 61–66

    PubMed  CAS  Google Scholar 

  • Barber J, Morris E and Büchel C (2000) Revealing the structure of the Photosystem II chlorophyll binding proteins, CP43 and CP47. Biochim Biophys Acta 1459: 239–247

    PubMed  CAS  Google Scholar 

  • Barber J, Nield J, Morris EP, Zheleva D and Hankamer B (1997) The structure, function and dynamics of Photosystem II. Physiol Plant 100: 817–827

    CAS  Google Scholar 

  • Bassi R, Magaldi AG, Tognon G, Giacometti GM and Miller KR (1989) Two-dimensional crystals of the Photosystem II reaction center complex from higher plants. Eur J Cell Biol 50: 84–93

    PubMed  CAS  Google Scholar 

  • Bassi R, Marquardt J and Lavergne J (1995) Biochemical and functional properties of Photosystem II in agranal membranes from maize mesophyll and bundle-sheath chloroplasts. Eur J Biochem 233: 709–719

    PubMed  CAS  Google Scholar 

  • Berthold DA, Babcock GT and Yocum CF (1981) A highly resolved, oxygen-evolving PS II preparation from spinach thylakoid membranes – electron-paramagnetic resonance and electron transport properties. FEBS Lett 134: 231–234

    CAS  Google Scholar 

  • Betts SD, Hachigian TM, Pichersky E and Yocum CF (1994) Reconstitution of the spinach oxygen-evolving complex with recombinant Arabidopsis manganese-stabilizing protein. PlantMol Biol 26: 117–130

    CAS  Google Scholar 

  • Boekema EJ, Boonstra AF, Dekker JP and Rogner M (1994) Electron microscopical structural analysis of Photosystem I, Photosystem II and the cytochrome-b6 /f complex from green plants and cyanobacteria. J Bioenerg Biomembr 26: 17–29

    PubMed  CAS  Google Scholar 

  • Boekema EJ, Hankamer B, Bald D, Kruip J, Nield J, Boonstra AF, Barber J and Rogner M (1995) Supramolecular structure of the Photosystem II complex from green plants and cyanobacteria. Proc Natl Acad Sci USA 92: 175–179

    PubMed  CAS  Google Scholar 

  • Boekema EJ, Nield J, Hankamer B and Barber J (1998a) Localization of the 23-kDa subunit of the oxygen evolving complex of Photosystem II by electron-microscopy. Eur J Biochem 252: 268–276

    PubMed  CAS  Google Scholar 

  • Boekema EJ, van Roon H and Dekker JP (1998b) Specific association of Photosystem II and light-harvesting complex II in partially solubilized Photosystem II membranes. FEBS Lett 424: 95–99

    PubMed  CAS  Google Scholar 

  • Boekema EJ, van Roon H, Calkoen F, Bassi R and Dekker JP (1999a) Multiple types of association of Photosystem II and its light-harvesting antenna in partially solubilized Photosystem II membranes. Biochemistry 38: 2233–2239

    PubMed  CAS  Google Scholar 

  • Boekema EJ, van Roon H, van Breemen JFL and Dekker JP (1999b) Supramolecular organization of Photosystem II and its light-harvesting antenna in partially solubilized Photosystem II membranes. Eur J Biochem 266: 444–452

    PubMed  CAS  Google Scholar 

  • Boekema EJ, van Breemen JFL, van Roon H and Dekker JP (2000a) Arrangement of Photosystem II supercomplexes in crystalline macrodomains within the thylakoid membrane of green plant chloroplasts. J Mol Biol 301: 1123–1133

    PubMed  CAS  Google Scholar 

  • Boekema EJ, van Breemen JFL, van Roon H and Dekker JP (2000b) Conformational changes in Photosystem II supercomplexes upon removal of extrinsic subunits. Biochemistry 39: 12907–12915

    PubMed  CAS  Google Scholar 

  • Branton DS, Bullivant NB, Gilula MJ, Karnovsky H, Moor K, Mühlthaler DH, Northcote L, Packer B, Satir P, Satir V, Speth LA, Staehelin LA, Steere RL and Weinstein RS (1975) Freezeetching nomenclature. Science 190: 54–56

    PubMed  CAS  Google Scholar 

  • Bricker TM (1990) The structure and function of CPA-1 and CPA-2 in Photosystem II. Photosynth Res24: 1–13

    CAS  Google Scholar 

  • Bricker TMand Frankel LK (1998) The structure and function of the 33 kDa extrinsic protein of Photosystem II: a critical assessment. Photosynth Res 56: 157–173

    CAS  Google Scholar 

  • Bricker TM and Frankel LK (2002) The structure and function of CP47 and CP43 in Photosystem II. Photosynth Res 72: 131–146

    PubMed  CAS  Google Scholar 

  • Büchel C, Morris E, Orlova E and Barber J (2001) Localization of the PsbH subunit in Photosystem II: a new approach using labeling of His-tags with a Ni2+-NTA gold cluster and single particle analysis. J Mol Biol 312: 371–379

    PubMed  Google Scholar 

  • Dainese P and Bassi R (1991) Subunit stoichiometry of the chloroplast Photosystem II antenna system and aggregation state of the component chlorophyll a/b binding proteins. J Biol Chem 266: 8136–8142

    PubMed  CAS  Google Scholar 

  • Debus RJ (1992) Themanganese and calcium ions of photosynthetic oxygen evolution. Biochim Biophys Acta 1102: 269–352

    PubMed  CAS  Google Scholar 

  • Deisenhofer J, Epp O, Miki K, Huber R and Michel H (1985) Structure of the protein subunits in the photosynthetic reaction centre of Rhodopseudomonas viridis at 3°A resolution. Nature 318: 618–624

    Google Scholar 

  • Dekker JP, Boekema EJ, Witt HT and Rogner M (1988) Refined purification and further characterization of oxygen-evolving and Tris-treated Photosystem II particles from the thermophilic cyanobacterium Synechococcus sp. Biochim Biophys Acta 936: 307–318

    CAS  Google Scholar 

  • Dekker JP, Betts SD, Yocum CF and Boekema EJ (1990) Characterization by electron microscopy of isolated particles and two-dimensional crystals of the CP47-D1-D2-cytochrome b559complex of Photosystem II. Biochemistry 29: 3220–3225

    PubMed  CAS  Google Scholar 

  • Dekker JP, Germano M, van Roon H and Boekema EJ (2002) Photosystem II solubilizes as a monomer by mild detergent treatment of unstacked thylakoid membranes. Photosynth Res 72: 203–210

    PubMed  CAS  Google Scholar 

  • Dunahay TG, Staehelin LA, Seibert M, Ogilvie PD and Berg S (1984) Structural, biochemical and biophysical characterization of four oxygen-evolving Photosystem II preparation from spinach. Biochim Biophys Acta 764: 179–193

    CAS  Google Scholar 

  • Eijckelhoff C, Dekker JP and Boekema EJ (1997) Characterization by electron microscopy of dimeric Photosystem II core com-plexes from spinach with and without CP43. Biochim Biophys Acta 1321: 10–20

    CAS  Google Scholar 

  • Enami I, Murayama H, Ohta H, Kamo M, Nakazato K and Shen JR (1995) Isolation and characterization of a Photosystem II complex from the red alga Cyanidium caldarium: association of cytochrome c550 and a 12 kDa protein with the complex. Biochim Biophys Acta 1232: 208–216

    PubMed  Google Scholar 

  • Enami I, Kikuchi S, Fukuda T, Ohta H and Shen JR (1998) Binding and functional properties of four extrinsic proteins of Photosystem II from a red alga, Cyanidium caldarium, as studied by release – reconstitution experiments. Biochemistry 37: 2787–2793

    PubMed  CAS  Google Scholar 

  • Enami I, Yoshihara S, Tohri A, Okumura A, Ohta H and Shen JR (2000) Cross-reconstitution of various extrinsic proteins and Photosystem II complexes from cyanobacteria, red algae and higher plants. Plant Cell Physiol 41: 1354–1364

    PubMed  CAS  Google Scholar 

  • Ford RC, Rosenberg MF, Shepherd FH, McPhie P and Holzenburg A (1995) Photosystem II 3-D structure and the role of the extrinsic subunits in photosynthetic oxygen evolution. Micron 26: 133–140

    CAS  Google Scholar 

  • Ford RC, Stoylova SS and Holzenburg A (2002) An alternative model for Photosystem II/light-harvesting complex II in grana membranes based on cryo-electron microscopy studies. Eur J Biochem 269: 326–336

    PubMed  CAS  Google Scholar 

  • Fromme P, Jordan P and Krauss N (2001) Structure of Photosystem I. Biochim Biophys Acta 1507: 5–31

    PubMed  CAS  Google Scholar 

  • Fujita Y, Murakami A, Aizawa K and Ohki K(1995) Short-term and long-term adaptation of the photosynthetic apparatus: homeostatic properties of thylakoids. In

  • Bryant DA (ed) The Molecular Biology of Cyanobacteria, pp 677–692. Kluwer Academic Publishers, Dordrecht, The Netherlands

  • Gantt E (1994) Supramolecular membrane organization. In

  • Bryant DA (ed) The Molecular Biology of Cyanobacteria, pp 139–216. Kluwer Academic Publishers, Dordrecht, The Netherlands

  • Ghanotakis DF and Yocum CF (1985) Polypeptides of Photosystem II and their role in oxygen evolution. Photosynth Res 7: 97–114

    CAS  Google Scholar 

  • Ghanotakis DF and Yocum CF (1990) Photosystem II and the oxygen-evolving complex. Ann Rev Plant Physiol Plant Mol Biol 41: 255–276

    CAS  Google Scholar 

  • Giddings TH and Staehelin LA (1979) Changes in thylakoid structure associated with the differentiation of heterocycsts in the cyanobacterium Anabaena cylindrica. Biochim Biophys Acta 546: 373–382

    PubMed  CAS  Google Scholar 

  • Giddings TH, Wasmann C and Staehelin LA (1983) Structure of the thylakoids and envelope membranes of the cyanelles of Cyanophora paradoxa. Plant Physiol 71: 409–419

    PubMed  CAS  Google Scholar 

  • Glazer AN (1982) Phycobilisomes: structure and dynamics. Ann Rev Microbiol 36: 173–198

    CAS  Google Scholar 

  • Gray MW (1992) The endosymbiont hypothesis revisited. Int Rev Cytol 141: 233–357

    Article  PubMed  CAS  Google Scholar 

  • Green BR and Durnford DG (1996) The chlorophyll-carotenoid proteins of oxygenic photosynthesis. Ann Rev Plant Physiol Plant Mol Biol 47: 685–714

    CAS  Google Scholar 

  • Green BR, Pichersky E and Kloppstech K (1991) Chlorophyll a/bbinding proteins: an extended family. Trends Biochem Sci 16: 181–186

    PubMed  CAS  Google Scholar 

  • Haag E, Irrgang KD, Boekema EJ and Renger G (1990) Functional and structural analysis of Photosystem II core complexes from spinach with high oxygen evolution capacity. Eur J Biochem 189: 47–53

    PubMed  CAS  Google Scholar 

  • Hainfeld JF, Liu WQ, Halsey cmR, Freimuth P and Powell RD (1999) Ni-NTA-gold clusters target his-tagged proteins. J Struct Biol 127: 185–198

    PubMed  CAS  Google Scholar 

  • Hankamer B, Boekema EJ and Barber J (1997a) Structure and membrane organization of Photosystem II in green plants. Ann Rev Plant Physiol Plant Mol Biol 48: 641–671

    CAS  Google Scholar 

  • Hankamer B, Nield J, Zheleva D, Boekema E, Jansson S and Barber J (1997b) Isolation and biochemical characterization of monomeric and dimeric Photosystem II complexes from spinach and their relevance to the organization of Photosystem II in vivo. Eur J Biochem 243: 422–429

    PubMed  CAS  Google Scholar 

  • Hankamer B, Morris EP and Barber J (1999) Revealing the structure of the oxygen-evolving core dimer of Photosystem II by cryoelectron crystallography. Nat Struct Biol 6: 560–564

    PubMed  CAS  Google Scholar 

  • Hankamer B, Morris EP, Nield J, Carne A and Barber J (2001a) Subunit positioning and transmembrane helix organisation in the core dimer of Photosystem II. FEBS Lett 504: 142–51

    PubMed  CAS  Google Scholar 

  • Hankamer B, Morris EP, Nield J, Gerle C and Barber J (2001b) Three-dimensional structure of the Photosystem II core dimer of higher plants determined by electron microscopy. J Struct Biol 135:262–269

    PubMed  CAS  Google Scholar 

  • Hansson O and Wydrzynski T (1990) Current perceptions of Photosystem II. Photosynth Res 23: 131–162

    CAS  Google Scholar 

  • Harrer R, Bassi R, Testi MG and Schafer C (1998) Nearestneighbor analysis of a Photosystem II complex from Marchantia polymorpha L. (liverwort), which contains reaction center and antenna proteins. Eur J Biochem 255: 196–205

    PubMed  CAS  Google Scholar 

  • Hasler L, Ghanotakis D, Fedtke B, Spyridaki A, Miller M, Muller SA, Engel A and Tsiotis G (1997) Structural analysis of Photosystem II: comparative study of cyanobacterial and higher plant Photosystem II complexes. J Struct Biol 119: 273–283

    PubMed  CAS  Google Scholar 

  • Heathcote P, Fyfe PK and Jones MR (2002) Reaction centres: the structure and evolution of biological solar power. Trends Biochem Sci 27: 79–87

    PubMed  CAS  Google Scholar 

  • Holzenburg A, Bewly MC, Wilson FH, Nicholson WV and Ford RC (1993) Three-dimensional structure of Photosystem II. Nature 363: 470–472

    CAS  Google Scholar 

  • Ikeuchi M (1992) Subunit proteins of Photosystem II. Bot Mag Tokyo 105: 327–373

    CAS  Google Scholar 

  • Irrgang KD, Boekema EJ, Vater J and Renger G (1988) Structural determination of the Photosystem II core complex from spinach. Eur J Biochem 178: 209–217

    PubMed  CAS  Google Scholar 

  • Jansson S (1994) The light-harvesting a/b-binding proteins. Biochim Biophys Acta 1184: 1–19

    PubMed  CAS  Google Scholar 

  • Jansson S, Stefansson H, Nystrom U, Gustafsson P and Albertsson PA (1997) Antenna protein composition of PS I and PS II in thylakoid sub-domains. Biochim Biophys Acta 1320: 297–309

    CAS  Google Scholar 

  • Kamiya N and Shen JR (2003) Crystal structure of oxygen-evolving Photosystem II from Thermosynechococcus vulcanus at 3.7 °A resolution. Proc Natl Acad Sci USA 100: 98–103

    PubMed  CAS  Google Scholar 

  • Kitmitto A, Mustafa AO, Ford JW, Holzenburg A and Ford RC (1999) Does photoinhibition and/or phosphorylation of Photosystem II influence its in vivo oligomeric state? Biochim Biophys Acta 1413: 21–30

    CAS  Google Scholar 

  • Koike H and Inoue Y (1985) Properties of a peripheral 34 kDa protein in Synechococcus vulcanus Photosystem II particles – its exchanbility with spinach 33 kDa protein in reconstitution of O2evolution. Biochim Biophys Acta 807: 64–73

    CAS  Google Scholar 

  • Komenda J, Lupinkova L and Kopecky J (2002) Absence of the psbH gene product destabilizes Photosystem II complex and bicarbonate binding on its acceptor side in Synechocystis PCC 6803. Eur J Biochem 269: 610–619

    PubMed  CAS  Google Scholar 

  • Krauss N, Schubert WD, Klukas O, Fromme P, Witt HT and Saenger W (1996) Photosystem I at 4 °A resolution represents the first structural model of a joint photosynthetic reaction centre and core antenna system. Nat Struct Biol 3: 965–973

    PubMed  CAS  Google Scholar 

  • Kruse O (2001) Light-induced short-term adaptation mechanisms under redox control in the PS II–LHC II supercomplex: LHC II state transitions and PS II repair cycle. Naturwissenschaften 88: 284–292

    PubMed  CAS  Google Scholar 

  • Kühl H, Rogner M, van Breemen JFL and Boekema EJ (1999) Localization of cyanobacterial Photosystem II donor-side subunits by electron microscopy and the supramolecular organization of Photosystem II in the thylakoid membrane. Eur J Biochem 266: 453–459

    PubMed  Google Scholar 

  • Kühlbrandt W, Wang DN and Fujiyoshi Y (1994) Atomic model of plant light-harvesting complex by electron crystallography. Nature 367: 614–21

    PubMed  Google Scholar 

  • Kuwabara T and Murata N (1982) Inactivation of photosynthetic oxygen evolution and concomitant release of three polypeptides in the Photosystem II particles of spinach chloroplasts. Plant Cell Physiol 23: 533–539

    CAS  Google Scholar 

  • Lacambra M, Larsen U, Olive J, Bennoun P and Wollman FA (1984) Characterization of the thylakoid membranes of wild-type and mutants of Chlorella sorokiniana. Photobiochem Photobiophys 8: 191–205

    CAS  Google Scholar 

  • Lupinkova L, Metz JG, Diner BA, Vass I and Komenda J (2002) Histidine residue 252 of the Photosystem II D1 polypeptide is involved in a light-induced cross-linking of the polypeptide with the alpha subunit of cytochrome b559: study of a site-directed mutant of Synechocystis PCC 6803. Biochim Biophys Acta 1554: 192–201

    PubMed  CAS  Google Scholar 

  • Lyon MK (1998) Multiple crystal types reveal Photosystem II to be a dimer. Biochim Biophys Acta 1364: 403–419 Lyon MK, Marr KM and Furcinitti PS (1993) Formation and characterization of two-dimensional crystals of Photosystem II. J Struct Biol 110: 133–140

    Google Scholar 

  • MacColl R (1998) Cyanobacterial phycobilisomes. J Struct Biol 124: 311–334

    PubMed  CAS  Google Scholar 

  • Mamedov F, Stefansson H, Albertsson PA and Styring S (2000) Photosystem II in different parts of the thylakoid membrane: a functional comparison between different domains. Biochemistry 39: 10478–10486

    PubMed  CAS  Google Scholar 

  • Marquardt J, Mörschel E, Rhiel E and Westermann M (2000) Ultrastructure of Acaryochloris marina, an oxyphotobacterium containing mainly chlorophyll d. Arch Microbiol 174: 181–188

    PubMed  CAS  Google Scholar 

  • Marr KM, Mastronarde DN and Lyon MK (1996a) Twodimensional crystals of Photosystem II: biochemical characterization, cryoelectron microscopy and localization of the D1 and cytochrome b559 polypeptides. J Cell Biol 132: 823–833

    PubMed  CAS  Google Scholar 

  • Marr KM, McFeeters RL and Lyon MK (1996b) Isolation and structural analysis of two-dimensional crystals of Photosystem II from Hordeum vulgare viridis zb63. J Struct Biol 117: 86–98

    PubMed  CAS  Google Scholar 

  • Mayanagi K, Ishikawa T, Toyoshima C, Inoue Y and Nakazato K (1998) Three-dimensional electron microscopy of the Photosystem II core complex. J Struct Biol 123: 211–224

    PubMed  CAS  Google Scholar 

  • Mayes SR, Cook KM, Self SJ, Zhang ZH and Barber J (1991) Deletion of the gene encoding the Photosystem II 33-kDa protein from Synechocystis sp. PCC 6803 does not inactivate water splitting but increases vulnerability to photoinhibition. Biochim Biophys Acta 1060: 1–12

    CAS  Google Scholar 

  • Mayfield SP, Bennoun P and Rochaix JD (1987) Expression of the nuclear encoded OEE1 protein is required for oxygen evolution and stability of Photosystem II particles in Chlamydomonas reinhardtii. EMBO J 6: 313–318

    PubMed  CAS  Google Scholar 

  • McFadden GI (1999) Endosymbiosis and evolution of the plant cell. Curr Opin Plant Biol 2: 513–519

    PubMed  CAS  Google Scholar 

  • Melis A (1991) Dynamics of photosynthetic membrane composition and function. Biochim Biophys Acta 1058:87–106

    CAS  Google Scholar 

  • Michel H and Deisenhofer J (1988) Relevance of the photosynthetic reaction center from purple bacteria to the structure of Photosystem II. Biochemistry 27: 1–7

    CAS  Google Scholar 

  • Miller KR and Cushman RA (1979) A chloroplast membrane lacking Photosystem II: Thylakoid stacking in the absence of the Photosystem II particle. Biochim Biophys Acta 546: 481–497

    PubMed  CAS  Google Scholar 

  • Miller KR, Miller GJ and McIntyre KR (1976) The light-harvesting chlorophyll–protein complex of Photosystem II: Its location in the photosynthetic membrane. J Cell Biol 71:624–638

    PubMed  CAS  Google Scholar 

  • Morris EP, Hankamer B, Zheleva D, Friso G and Barber J (1997) The three-dimensional structure of a Photosystem II core complex determined by electron crystallography. Structure 5: 837–849

    PubMed  CAS  Google Scholar 

  • Mörschel E (1991) The light-harvesting antennae of cyanobacteria and red algae. Photosynthetica 25: 137–144

    Google Scholar 

  • Mörschel E and Mühlethaler K (1983)On the linkage of exoplasmatic freeze-fracture particles to phycobilisomes. Planta 158: 451–457

    Google Scholar 

  • Mörschel E and Schatz GH (1987) Correlation of Photosystem II complexes with exoplasmatic freeze-fracture particles of thylakoids of the cyanobacterium Synechococcus sp. Planta 172: 145–154

    Google Scholar 

  • Mullineaux CW(1999) The thylakoid membranes of cyanobacteria: structure, dynamics and function. Aust J Plant Physiol 26: 671– 677

    Article  CAS  Google Scholar 

  • Murata N and Miyao M (1985) Extrinsic membrane proteins in the photosynthetic oxygen-evolving complex. Trends Biochem Sci 10: 122–124

    CAS  Google Scholar 

  • Mustardy L (1996) Development of thylakoid membrane stacking. In

  • Ort DR and Yocum CF (eds) Oxygenic Photosynthesis – The Light Reactions, pp 59–68. Kluwer Academic Publishers, Dordrecht, The Netherlands

  • Mustardy L, Cunningham FX and Gantt E (1992) Photosynthetic membrane topography: quantitative in situ localization of Photosystems I and II. Proc Natl Acad Sci USA 89: 10021–10025

    PubMed  CAS  Google Scholar 

  • Nakazato K, Toyoshima C, Enami I and Inoue Y (1996) Twodimensional crystallization and cryo-electron microscopy of Photosystem II. J Mol Biol 257: 225–232

    PubMed  CAS  Google Scholar 

  • Nanba O and Satoh K (1987) Isolation of a Photosystem II reaction center consisting of D1 and D2 polypeptides and cytochrome b559. Proc Natl Acad Sci USA 84: 109–112

    PubMed  CAS  Google Scholar 

  • Neushul M (1971) Uniformity of the thylakoid structure in a red, brown and two blue-green algae. J Ultrastruct Res 37: 532–543

    PubMed  CAS  Google Scholar 

  • Nicholson WV, Ford RC and Holzenburg A (1996) A current assessment of Photosystem II structure. Bioscience Rep 16: 159–187

    Google Scholar 

  • Nield J, Balsera M, De Las Rivas J and Barber J (2002) Threedimensional electron cryo-microscopy study of the extrinsic domains of the oxygen-evolving complex of spinach. J Biol Chem 277: 15006–15012

    PubMed  CAS  Google Scholar 

  • Nield J, Kruse O, Ruprecht J, da Fonseca P, Büchel C and Barber J (2000a) Three-dimensional structure of Chlamydomonas reinhardtii and Synechococcus elongatus Photosystem II complexes allows for comparison of their oxygen-evolving complex organization. J Biol Chem 275: 27940–27946

    PubMed  CAS  Google Scholar 

  • Nield J, Orlova EV, Morris EP, Gowen B, vanHeel M and Barber J (2000b) 3D map of the plant Photosystem II supercomplex obtained by cryoelectron microscopy and single particle analysis. Nat Struct Biol 7: 44–47

    PubMed  CAS  Google Scholar 

  • Nilsson F, Simpson DJ, Jansson C and Andersson B (1992) Ultrastructural and biochemical characterization of a Synechocystis 6803 mutant with inactivated psbA genes. Arch Biochem Biophys 295: 340–347

    PubMed  CAS  Google Scholar 

  • Olive J and Valon O (1991) Structural organisation of the thylakoid membrane: freeze-fracture and immunocytochemical analysis. J Electr Micr Tech 18: 360–374

    CAS  Google Scholar 

  • Olive J and Wollman FA (1998) Supramolecular organization of the chloroplast and of the thylakoid membranes. In

  • Rochaix JD, Goldschmidt-Clermont M and Merchan S (eds) The Molecular Biology of Chloroplast and Mitochondria in Chlamydomonas, pp 233–254. Kluwer Academic Publishers, Dordtrecht, The Netherlands

  • Olive J, Wollman FA, Bennoun P and Recouvreur M (1981) Ultrastructure of thylakoid membranes in C. reinhardtii: evidence for variations in the partition coefficient of the light-harvesting complex containing particles upon membrane fracture. Arch Biochem Biophys 208: 456–467

    PubMed  CAS  Google Scholar 

  • Olive J, Recouvreur M, Girardbascou J and Wollman FA (1992) Further identification of the exoplasmic face particles on the freeze-fractured thylakoid membranes – a study using double and triple mutants from Chlamydomonas reinhardtii lacking various Photosystem II subunits and the cytochrome b6/f complex. Eur J Cell Biol 59: 176–186

    PubMed  CAS  Google Scholar 

  • Olive J, Ajlani G, Astier C, Recouvreur M and Vernotte C (1997) Ultrastructure and light adaptation of phycobilisome mutants of Synechocystis PCC 6803. Biochim Biophys Acta 1319: 275–282

    CAS  Google Scholar 

  • Paulsen H (1995) Chlorophyll a/b-binding proteins. Photochem Photobiol 62: 367–382

    CAS  Google Scholar 

  • Peter GF and Thornber JP (1991) Biochemical evidence that the higher plant Photosystem II core complex is organized as a dimer. Plant Cell Physiol 32: 1237–1250

    CAS  Google Scholar 

  • Philbrick JB, Diner BA and Zilinskas BA (1991) Construction and characterization of cyanobacterial mutants lacking the manganese-stabilizing polypeptide of Photosystem II. J Biol Chem 266: 13370–13376

    PubMed  CAS  Google Scholar 

  • Rhee KH (2001) Photosystem II: the solid structural era. Annu Rev Biophys Biomol 30: 307–328

    CAS  Google Scholar 

  • Rhee KH, Morris EP, Zheleva D, Hankamer B, Kuhlbrandt W and Barber J (1997) Two-dimensional structure of plant Photosystem II at 8°A resolution. Nature 389: 522–526

    CAS  Google Scholar 

  • Rhee KH, Morriss EP, Barber J and Kuhlbrandt W (1998) Threedimensional structure of the plant Photosystem II reaction centre at 8°A resolution. Nature 396: 283–286

    PubMed  CAS  Google Scholar 

  • Rögner M, Boekema EJ and Barber J (1996) How does Photosystem 2 split water? The structural basis of efficient energy conversion. Trends Biochem Sci 21: 44–49

    PubMed  Google Scholar 

  • Rögner M, Dekker JP, Boekema EJ and Witt HT (1987) Size, shape and mass of the oxygen-evolving Photosystem II complex from the thermophilic cyanobacterium Synechococcus sp. FEBS Lett 219: 207–211

    Google Scholar 

  • Rosenberg MF, Holzenburg A, Shepherd FH, Nicholson WV, Flint TD and Ford RC (1997) Rebinding of the extrinsic proteins of Photosystem II studied by electron microscopy and single particle alignment: an assessment with small two-dimensional ordered arrays of Photosystem II. Biochim Biophys Acta 1319: 119–132

    CAS  Google Scholar 

  • Ruprecht J and Nield J (2001) Determining the structure of biological macromolecules by transmission electron microscopy, single particle analysis and 3-D reconstruction. Prog Biophys Mol Biol 75: 121–164

    PubMed  CAS  Google Scholar 

  • Sandonà D, Croce R, Pagano A, Crimi M and Bassi R (1998) Higher plants light-harvesting proteins. Structure and function as revealed by mutation analysis of either protein or chromophore moieties. Biochim Biophys Acta 1365: 207–214

    PubMed  Google Scholar 

  • Santini C, Tidu V, Tognon G, Magaldi AG and Bassi R (1994) Three-dimensional structure of the higher plant Photosystem II reaction center and evidence for its dimeric organization in vivo. Eur J Biochem 221: 307–315

    PubMed  CAS  Google Scholar 

  • Schubert WD, Klukas O, Saenger W, Witt HT, Fromme P and Krauss N (1998) A common ancestor for oxygenic and anoxygenic photosynthetic systems: a comparison based on the structural model of Photosystem I. J Mol Biol 280: 297–314

    PubMed  CAS  Google Scholar 

  • Seibert M, deWitt M and Staehelin A (1987) Structural localization of the O2-evolving apparatus to multimeric (tetrameric) particles on the lumenal surfaces of freeze-etched photosynthetic membranes. J Cell Biol 105: 2257–2265

    PubMed  CAS  Google Scholar 

  • Seidler A (1996) The extrinsic polypeptides of Photosystem II. Biochim Biophys Acta 1277: 35–60

    PubMed  Google Scholar 

  • Shen JR and Inoue Y (1993) Binding and functional properties of two new extrinsic components, cytochrome c550 and 12-kDa protein, in cyanobacterial Photosystem II. Biochemistry 32: 1825–1832

    PubMed  CAS  Google Scholar 

  • Shen JR, Ikeuchi M and Inoue Y (1992) Stoichiometric association of extrinsic cytochrome c550 and 12-kDa protein with a highly purified oxygen-evolving Photosystem II core complexes from Synechococcus vulcanus. FEBS Lett 301: 145–149

    PubMed  CAS  Google Scholar 

  • Shen JR, Burnap RL and Inoue Y (1995) An independent role of cytochrome c550 in cyanobacterial Photosytem II as revealed by double deletion mutagenesis of the psbO and psbV genes in Synechocystis sp. PCC 6803. Biochemistry 34: 12661–12668

    PubMed  CAS  Google Scholar 

  • Shen JR, Ikeuchi M and Inoue Y (1997) Analysis of the psbU gene encoding the 12 kDa extrinsic protein of Photosystem II and studies on its role by deletion mutagenesis in Synechocystis sp. PCC 6803. J Biol Chem 272: 17821–17826

    PubMed  CAS  Google Scholar 

  • Sherman DM, Troyan TA and Sherman LA (1994) Localization of membrane proteins in the cyanobacterium Synechococcus sp. PCC 7942 – radial asymmetry in the photosynthetic complexes. Plant Physiol 106: 251–262

    PubMed  CAS  Google Scholar 

  • Shi LX, Lorkovic ZJ, Oelmuller R and Schroder WP (2000) The low molecular mass PsbWprotein is involved in the stabilization of the dimeric Photosystem II complex in Arabidopsis thaliana. J Biol Chem 275: 37945–37950

    PubMed  CAS  Google Scholar 

  • Simpson DJ (1978) Freeze-fracture studies on barley plastid membranes. II. Wild-type chloroplast. Carlsberg Res Commun 43: 365–389

    Google Scholar 

  • Simpson DJ (1979) Freeze-fracture studies on barley plastid membranes. III. Location of the light-harvesting chlorophyll protein. Carlsberg Res Commun 44: 305–336

    CAS  Google Scholar 

  • Simpson DJ and Andersson B (1986) Extrinsic polypeptides of the chloroplast oxygen evolving complex constitute the tetrameric ESs particles of higher plant thylakoids. Carlsberg Res Commun 51: 467–474

    Article  CAS  Google Scholar 

  • Sprague SG, Camm EL, Green BR and Staehelin LA (1985) Reconstitution of light-harvesting complexes and Photosystem II cores into galactolipid and phopholipid liposomes. J Cell Biol 100: 552–557

    PubMed  CAS  Google Scholar 

  • Staehelin LA (1975) Chloroplast membrane structure: intramembranous particles of different sizes make contact in stacked membrane regions. Biochim Biophys Acta 408: 1–11

    PubMed  CAS  Google Scholar 

  • Staehelin LA (1976) Reversible particle movements associated with unstacking and restacking of chloroplast membranes in vitro. J Cell Biol 71: 136–158

    PubMed  CAS  Google Scholar 

  • Staehelin LA and Arntzen CJ (1983) Regulation of chloroplast membrane function: protein phosphorylation changes the spatial organization of membrane components. J Cell Biol 97: 1327–1337

    PubMed  CAS  Google Scholar 

  • Staehelin LA and deWitt M (1984) Correlation of structure and function of chloroplast membranes at the supramolecular level. J Cell Biochem 24: (3) 261–269

    PubMed  CAS  Google Scholar 

  • Staehelin LA and van der Staay GWM (1996) Structure, composition, functional organisation and dynamics properties of thylakoid membranes. In

  • Ort DR and Yocum CF (eds) Oxygenic Photosynthesis – the Light Reactions, pp 11–30. Kluwer Academic Publishers, Dordrecht, The Netherlands

  • Stoylova SS, Flint TD, Ford RC and Holzenburg A (1997) Projection structure of Photosystem II in vivo determined by cryoelectron crystallography. Micron 28: 439–446

    CAS  Google Scholar 

  • Stoylova SS, Flint TD, Ford RC and Holzenburg A (2000) Structural analysis of Photosystem II in far-red-light-adapted thylakoid membranes – new crystal forms provide evidence for a dynamic reorganization of light-harvesting antennae subunits. Eur J Biochem 267: 207–215

    PubMed  CAS  Google Scholar 

  • Swiatek M, Kuras R, Sokolenko A, Higgs D, Olive J, Cinque G, Muller B, Eichacker LA, Stern DB, Bassi R, Herrmann RG and Wollman FA (2001) The chloroplast gene ycf9 encodes a Photosystem II (PS II) core subunit, PsbZ, that participates in PS II supramolecular architecture. Plant Cell 13: 1347–1367

    PubMed  CAS  Google Scholar 

  • Trissl HW and Wilhelm C (1993) Why do thylakoid membranes from higher plants form grana stacks? Trends Biochem Sci 18: 415–419

    PubMed  CAS  Google Scholar 

  • Tsiotis G, McDermott G and Ghanotakis D (1996a) Progress towards structural elucidation of Photosystem II. Photosynth Res 50: 93–101

    CAS  Google Scholar 

  • Tsiotis G, Walz T, Spyridaki A, Lustig A, Engel A and Ghanotakis D (1996b) Tubular crystals of a Photosystem II core complex. J Mol Biol 259: 241–248

    PubMed  CAS  Google Scholar 

  • Tsiotis G, Psylinakis M, Woplensinger B, Lustig A, Engel A and Ghanotakis D (1999) Investigation of the structure of spinach Photosystem II reaction center complex. Eur J Biochem 259: 320–324

    Google Scholar 

  • Tsvetkova NM, Brain APR and Quinn PJ (1994) Structural characteristic of thylakoid membranes of Arabidopsis mutants deficient in lipid fatty-acid desaturation. Biochim Biophys Acta 1192: 263–271

    PubMed  CAS  Google Scholar 

  • Tsvetkova NM, Apostolova EL, Brain APR, Williams WP and Quinn PJ (1995) Factors influencing PS II particle array formation in Arabidopsis thaliana chloroplasts and the relationship of such arrays to the thermostability of PS II. Biochim Biophys Acta 1228: 201–210

    Google Scholar 

  • Vácha F, Vácha M, Bumba L, Hashizume K and Tani T (2000) Inner structure of intact chloroplasts observed by a low temperature laser scanning microscope. Photosynthetica 38: 493–496

    Google Scholar 

  • Vallon O, Wollman FA and Olive J (1985) Distribution of intrinsic and extrinsic subunits of PS II protein complex between appressed and non-appressed regions of the thylakoid membrane: an immunocytochemical study. FEBS Lett 183: 245–250

    Google Scholar 

  • Vallon O, Wollman FA and Olive J (1986) Lateral distribution of the main protein complexes of the photosynthetic apparatus in Chlamydomonas reinheirdtii and in spinach: an immunocytochemical study using intact thylakoid membanes and a PS II-enriched membrane preparation. Photobiochem Photobiophys 12: 203–220

    CAS  Google Scholar 

  • van der Staay GWM and Staehelin LA (1994) Biochemical characterization of protein composition and protein phophorylation patterns in stacked and unstacked thylakoid membranes of the prochlorophyte Prochlorothrix hollandica. J Biol Chem 269: 24834–24844

    PubMed  CAS  Google Scholar 

  • van Roon H, van Breemen JFL, de Weerd FL, Dekker JP and Boekema EJ (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 b6/f complexes. Photosynth Res 64: 155–166

    PubMed  CAS  Google Scholar 

  • Vermaas WFJ (1994) Molecular-genetic approaches to study photosynthetic and respiratory electron transport in thylakoids from cyanobacteria. Biochim Biophys Acta 1187: 181–186

    CAS  Google Scholar 

  • Whitmarsh J and Govindjee (1999) The photosynthetic process. In

  • Singhal GS, Renger G, Sopory SK, Irrgang KD and Govindjee (eds) Concepts in Photobiology: Photosynthesis and Photomorphogenesis, pp 11–51. Narosa Publishing House, New Delhi, India

  • Wollman FA, Olive J, Bennoun P and Recouvreur M (1980) Organization of the Photosystem II centers and their associatted antennae in the thylakoid membranes: a comparative ultrastructural, biochemical and biophysical study of Chlamydomonas wild type and mutants lacking in Photosystem II reaction centers. J Cell Biol 87: 728–735

    PubMed  CAS  Google Scholar 

  • Xu Q and Bricker TM (1992) Structural organization of proteins on the oxidizing side of Photosystem II – two molecules of the 33kDa manganese-stabilizing proteins per reaction center. J Biol Chem 267: 25816–25821

    PubMed  CAS  Google Scholar 

  • Yakushevska AE, Jensen PE, Keegstra W, van Roon H, Scheller HV, Boekema EJ and Dekker JP (2001) Supermolecular organization of Photosystem II and its associated light-harvesting antenna in Arabidopsis thaliana. Eur J Biochem 268: 6020–6028

    PubMed  CAS  Google Scholar 

  • Yamamoto Y, Ueda T, Shinkai H and Nishimura M (1982) Preparation of O2-evolving Photosystem II subchloroplasts from spinach. Biochim Biophys Acta 679: 347–350

    CAS  Google Scholar 

  • Zouni A, Witt HT, Kern J, Fromme P, Krauss N, Saenger Wand Orth P (2001) Crystal structure of Photosystem II from Synechococcus elongatus at 3.8°A resolution. Nature 409: 739–743

    PubMed  CAS  Google Scholar 

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Bumba, L., Vácha, F.e. Electron microscopy in structural studies of Photosystem II. Photosynthesis Research 77, 1–19 (2003). https://doi.org/10.1023/A:1024927631196

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