Electron Crystallography in Photosynthesis Research

  • Paula C. A. da Fonseca
  • Edward P. Morris
  • Claudia Büchel
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 26)

Electron crystallography covers the analysis of crystals by electron microscopy based methods in order to infer into the structure of the crystallized molecules. Electron crystallography of two-dimensional crystals has become a powerful alternative to X-ray crystallography and NMR spectroscopy for the determination of the structure of proteins or protein complexes. The electron crystallography approach is particularly suitable for the study of membrane proteins, which due to their amphiphilic properties are stable in lipid bilayers, their natural environment, where they can form crystalline arrays. This method of structural analysis has also proved suitable for the study of soluble proteins, which can be induced to form two-dimensional lattices, as well as the study of very thin three-dimensional crystals. The preparation of two-dimensional crystals normally requires less protein and at a lower concentration than required for three-dimensional crystallization. Overall, the structural analysis based on electron microscopy is more amenable to the study of conformational variations associated with different functional states of membrane proteins than other techniques used in structural biology. Furthermore, the analysis of two-dimensional crystals enables the calculation of preliminary structural maps at relatively low resolutions, which at early stages in the optimization crystallization and image analysis may render valuable information on the overall protein architecture. Here we present a summary of the methods involved in protein electron crystallography, regarding both the crystallization process itself and the fundaments of electron microscopy and image analysis required. We also show how electron crystallography has greatly contributed for the development of the present knowledge on the structural organization of photosynthetic protein complexes, focusing on the studies involving transmembrane pigmented proteins and protein complexes.

Keywords

Diffraction Spot Purple Membrane Synechococcus Elongatus Electron Crystallography High Resolution Analysis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Adrian M, Dubochet J, Lepault J and McDowall AW (1984) Cryoelectron microscopy of viruses. Nature 308: 32-36PubMedGoogle Scholar
  2. Aebi U and Pollard TD (1987) A glow discharge unit to render electron microscope grids and other surfaces hydrophilic. J Electron Microsc Tech 7: 29-33PubMedGoogle Scholar
  3. Amelincks S, van Dyck D, van Landuyt J and van Tendeloo G (1997) Electron Microscopy. VCH Wiley, WeinheimGoogle Scholar
  4. Auer M (2000) Three-dimensional electron cryo-microscopy as a powerful structural tool in molecular medicine. J Mol Med 78: 191-202PubMedGoogle Scholar
  5. Auer M, Scarborough GA and Kühlbrandt W (1999) Surface crystallization of the plasma membrane H+-ATPase on a carbon support film for electron crystallography. J Mol Biol 287: 961-968PubMedGoogle Scholar
  6. Baldwin J and Henderson R (1984) Measurement and evaluation of electron diffraction patterns from two-dimensional crystals. Ultramicroscopy 14: 319-336Google Scholar
  7. Baldwin JM, Henderson R, Beckmann E and Zemlin F (1988) Images of purple membrane at 2.8Å resolution obtained by cryo-electron microscopy. J Mol Biol 202: 585-591PubMedGoogle Scholar
  8. 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: 84-93PubMedGoogle Scholar
  9. Ben-Shem A, Frolow F and Nelson N (2003) Crystal structure of plant Photosystem I. Nature 426: 630-635PubMedGoogle Scholar
  10. Berriman J and Leonard KR (1986) Methods for specimen thickness determination in electron microscopy. II. Changes in thickness with dose. Ultramicroscopy 19: 349-366PubMedGoogle Scholar
  11. Biesiadka J, Loll B, Kern J, Irrgang KD and Zouni A (2004) Crystal structure of cyanobacterial Photosystem II at 3.2Å resolution: A closer look at the Mn cluster. Phys Chem Chem Phys 6: 4733-4736Google Scholar
  12. Booy FP and Pawley JB (1993) Cryo-crinkling: What happens to carbon films on copper grids at low temperature. Ultramicroscopy 56: 241-252Google Scholar
  13. Böttcher B, Gräber P and Boekema EJ (1992) The structure of Photosystem I from the thermophilic cyanobacterium Synechococcus sp. determined by electron microscopy of two-dimensional crystals. Biochim Biophys Acta 1100: 125-136PubMedGoogle Scholar
  14. Büchel C and Kühlbrandt W (2005) Structural differences in the inner part of Photosystem II between higher plants and cyanobacteria. Photosynth Res 85: 3-13PubMedGoogle Scholar
  15. Büchel C, Morris E and Barber J (2000) Crystallization of CP43, a chlorophyll binding protein of Photosystem II: An electron microscopy analysis of molecular packing. J Struct Biol 131: 181-186PubMedGoogle Scholar
  16. Büchel C, Morris E, Orlova E and Barber J (2001) Localization of the psbH-subunit in Photosystem II — a new approach using labelling of His-tags with a Ni2+-NTA-goldcluster and single particle analysis. J Mol Biol 312: 371-379PubMedGoogle Scholar
  17. Bullough PA and Tulloch PA (1991) Spot-scan imaging of microcrystals of an influenza neuraminidase-antibody fragment complex. Ultramicroscopy 35: 131-143PubMedGoogle Scholar
  18. Bumba L and Vácha F (2003) Electron microscopy in structural studies of Photosystem II. Photosynth Res 77: 1-19PubMedGoogle Scholar
  19. Buseck P, Cowley J and Eyring L (1988) High-Resolution Transmission Electron Microscopy and Associated Techniques. Oxford University Press, OxfordGoogle Scholar
  20. Caldes MT, Deniard P, Zou XD, Marchand R, Diot N and Brec R (2001) Solving modulated structures by X-ray and electron crystallography. Micron 32: 497-507PubMedGoogle Scholar
  21. Ceska TA and Henderson R (1990) Analysis of high-resolution patterns from purple membrane labelled with heavy atoms. J Mol Biol 213: 539-560PubMedGoogle Scholar
  22. Cheng A and Yeager M (2004) A graphical representation of image quality for three-dimensional structure analysis of twodimensional crystals. Acta Cryst A 60: 351-354Google Scholar
  23. Crowther RA, Henderson R and Smith JM (1996) MRC image processing programs. J Struct Biol 116: 9-16PubMedGoogle Scholar
  24. Cyrklaaf M, Auer M, Kühlbrandt W and Scarborough GA (1995) 2D structure of the Neurospora crassa plasma membrane ATPase as determined by electron cryomicroscopy. EMBO J 14: 1854-1857Google Scholar
  25. Da Fonseca P, Morris EP, Hankamer B and Barber J (2002) Electron crystallographic study of Photosystem II of the cyanobacterium Synechococcus elongatus. Biochemistry 41: 5163-5167PubMedGoogle Scholar
  26. Deisenhofer J, Epp O, Miki K, Huber R and Michel H (1985) Structure of the protein subunits in the photosynthetic reaction center of Rhodopseudomonas viridis at 3 Å resolution. Nature 318: 618-624Google Scholar
  27. Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid membrane proteins in green plants. Biochim Biophys Acta 1706: 12-39PubMedGoogle Scholar
  28. Dekker JP, Betts SD, Yocum CF and Boekema EJ (1990) Characterization by electron microscopy of isolated particles and twodimensional crystals of the CP47-D1-D2-cytochrome b-559 complex of Photosystem II. Biochemistry 29: 3220-3225PubMedGoogle Scholar
  29. De Rosier D and Klug A (1968) Reconstruction of 3-dimensional structures from electron micrographs. Nature 217: 130-134Google Scholar
  30. Dorset DL (1996) Electron crystallography. Acta Cryst B 52: 753-769Google Scholar
  31. Dubochet J, Adrian M, Chang JJ, Homo JC, Lepault J, McDowall AW and Schultz P (1988) Cryo-electron microscopy of vitrified specimens. Q Rev Biophys 21: 129-228PubMedGoogle Scholar
  32. Ellis MJ and Hebert H (2001) Structure analysis of soluble proteins using electron crystallography. Micron 32: 541-550PubMedGoogle Scholar
  33. Ferreira KN, Iverson TM, Maghlaoui K, Barber J and Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303: 1831-1838PubMedGoogle Scholar
  34. Flachmann R and Kühlbrandt W (1995) Accumulation of plant antenna complexes is regulated by post-transcriptional mechanisms in tobacco. Plant Cell 7: 149-160PubMedGoogle Scholar
  35. Frank J (2002) Single-particle imaging of macromolecules by cryo-electron microscopy. Annu Rev Biophys Biomol Struc 31: 303-319Google Scholar
  36. Frank J (2005) Three-Dimensional Electron Microscopy of Macromolecular Assemblies. Oxford University Press, OxfordGoogle Scholar
  37. Fritzsch G, Koepke J, Diem R, Kuglstatter A and Baciou L (2002) Charge separation induces conformational changes in the photosynthetic reaction center of purple bacteria. Acta Crystallogr D 58: 1660-1663PubMedGoogle Scholar
  38. Fujiyoshi Y, Mizusaki T, Morikawa K, Yamagishi H, Aoki Y, Kihara H and Harada Y (1991) Development of a superfluid helium stage for high-resolution cryo electron microscopy. Ultramicroscopy 38: 241-251Google Scholar
  39. Fujiyoshi Y (1998) The structural study of membrane proteins by electron crystallography. Advan Biophys 35: 25-80Google Scholar
  40. Garab G, Löhner K, Laggner P and Farkas T (2000) Self-regulation of the lipid content of membranes by non-bilayer lipids: A hypothesis. Trends Plant Sci 5: 489-494PubMedGoogle Scholar
  41. Glaeser RM (1971) Limitations to significant information in biological electron microscopy as a result of radiation damage. J Ultrastruct Res 36: 466-482PubMedGoogle Scholar
  42. Glaeser RM (1999) Electron crystallography: Present excitement, a nod to the past, anticipating the future. J Struct Biol 128: 3-14PubMedGoogle Scholar
  43. Glaeser RM, Tong L and Kim SH (1989) 3-dimensional reconstructions from incomplete data — interpretability of density maps at atomic resolution. Ultramicroscopy 27: 307-318PubMedGoogle Scholar
  44. Glaeser RM, Zilker A, Radermacher M, Gaub HE, Hartmann T and Baumeister W (1991) Interfacial energies and surfacetension forces involved in the preparation of thin, flat crystals of biological macromolecules for high-resolution electron microscopy. J Microsc 161: 21-45PubMedGoogle Scholar
  45. Gonen T, Sliz P, Kistler J, Cheng Y and Walz T (2004) Aquaporin-0 membrane junctions reveal the structure of a closed water pore. Nature 429: 193-197PubMedGoogle Scholar
  46. Gonen T, Cheng Y, Sliz P, Hiroaki Y, Fujiyoshi Y, Harrison SC and Walz T (2005) Lipid-protein interactions in double-layered two-dimensional AQP0 crystals. Nature 438: 633-638PubMedGoogle Scholar
  47. Grigorieff N, Beckmann E and Zemlin F (1995) Lipid location in deoxycholate-treated purple membrane at 2.6 Ångström. J Mol Biol 254: 404-415PubMedGoogle Scholar
  48. Gyobu N, Tani K, Hiroaki Y, Kamegawa A, Mitsuoka K and Fujiyoshi Y (2004) Improved specimen preparation for cryo-electron microscopy using a symmetric carbon sandwich technique. J Struct Biol 146: 325-333PubMedGoogle Scholar
  49. Hankamer B, Boekema E and Barber J (1997) Structure and membrane organization of Photosystem II of green plants. Annu Rev Plant Physiol Mol Biol 48: 641-671Google Scholar
  50. Hankamer B, Morris EP and Barber J (1999) Revealing the structure of the oxygen-evolving core dimer of Photosystem II by cryoelectron crystallography. Nature Struct Biol 6: 561-564Google Scholar
  51. Hankamer B, Morris E, Nield J, Gerle C and Barber J (2001) Three-dimensional structure of the Photosystem II core dimer of higher plants determined by electron microscopy. J Struct Biol 135: 262-269PubMedGoogle Scholar
  52. Hasler L, Heymann JB, Engel A and Walz T (1998) 2D crystallization of membrane proteins: Rationales and examples. J Struct Biol 121: 162-171PubMedGoogle Scholar
  53. Henderson R (1995) The potential and limitations of neutrons, electrons and X-rays for atomic resolution microscopy of unstained biological molecules. Q Rev Biophys 28: 171-193PubMedGoogle Scholar
  54. Henderson R and Glaeser RM (1985) Quantitative analysis of image contrast in electron-micrographs of beam-sensitive crystals. Ultramicroscopy 16: 139-150Google Scholar
  55. Henderson R, Baldwin JM, Downing KH, Lepault J and Zemlin F (1986) Structure of the purple membrane from Halobacterium halobium: Recording, measurement and evaluation of electron-micrographs at 3.5Å resolution. Ultramicroscopy 19: 147-178Google Scholar
  56. Hobe S, Prytulla S, Kühlbrandt W and Paulsen H (1994) Trimerization and crystallization of reconstituted light-harvesting chlorophyll a/b complex. EMBO J 13: 3423-3429PubMedGoogle Scholar
  57. Holzenburg A, Bowley MC, Wilson FH, Nicholson WV and Ford RC (1993) Three-dimensional structure of Photosystem II. Nature 363: 470-472Google Scholar
  58. Hosokawa F, Danev R, Arai Y and Nagayama K (2005) Transfer doublet and an elaborated phase plate holder for 120 kV electron-phase microscope. J Electron Microsc 54: 317-324Google Scholar
  59. Ikeda-Yamasaki I, Odahara T, Mitsuoka K, Fujiyoshi Y and Murata K (1998) Projection map of the reaction center light-harvesting 1 complex from Rhodopseudomonas viridis at 10Å resolution. FEBS Lett 425: 505-508PubMedGoogle Scholar
  60. Jamieson SJ, Wang P, Quian P, Kirkland JY, Conroy MJ, Hunter CN and Bullough PA (2002) Projection structure of the photosynthetic reaction center-antenna complex of Rhodospirillum rubrum at 8.5Å resolution. EMBO J 21: 3927-3935PubMedGoogle Scholar
  61. Jiang W and Ludtke SJ (2005) Electron cryomicroscopy of single particles at subnanometer resolution. Curr Opin Struct Biol 15: 571-577PubMedGoogle Scholar
  62. Jordan P, Fromme P, Witt HT, Klukas O, Saenger W and Krauss N (2001) Three-dimensional structure of cyanobacterial Photosystem I at 2.5 Ångstrom resolution. Nature 411: 909-917PubMedGoogle Scholar
  63. Jungas C, Ranck JL, Rigaud JL, Joliot P and Vermeglio A (1999) Supramolecular organization of the photosynthetic apparatus of Rhodobacter sphaeroides. EMBO J 18: 534-542PubMedGoogle Scholar
  64. Kamiya N and Shen JR (2003) Crystal structure of oxygen-evolving Photosystem II from Thermosynechococcus vulcanus at 3.7 Å resolution. Proc Natl Acad Sci USA 100: 98-103PubMedGoogle Scholar
  65. Karrasch S, Bullough PA and Ghosh R (1995) A 8.5 Å projection map of the light-harvesting complex I from Rhodospirillum rubrum reveals a ring composed of 16 subunits. EMBO J 14: 631-638PubMedGoogle Scholar
  66. Karrasch S, Typke D, Walz T, Miller M, Tsiotis G and Engel A (1996) Highly ordered two-dimensional crystals of Photosystem I reaction center from Synechococcus sp.: Functional and structural analyzes. J Mol Biol 262: 336-348PubMedGoogle Scholar
  67. Kern J, Loll B, Zouni A, Saenger W, Irrgang KD and Biesiadka J (2005) Cyanobacterial Photosystem II at 3.2Å resolution — the plastoquinone binding pockets. Photosynth Res 84: 153-159PubMedGoogle Scholar
  68. Kimura Y, Vassylyev DG, Miyazawa A, Kidera A, Matsushima M, Mitsuoka K, Murata K, Hirai T and Fujiyoshi Y (1997) Surface structure of bacteriorhodopsin revealed by high resolution electron crystallography. Nature 389: 206-211PubMedGoogle Scholar
  69. Kitmitto A, Mustafa AO, Holzenburg A and Ford RC (1998) Three-dimensional structure of higher plant Photosystem I determined by electron crystallography. J Biol Chem 273: 29592-29599PubMedGoogle Scholar
  70. Koepke J, Hu X, Muenke C, Schulten K and Michel H (1996) The crystal structure of the light-harvesting complex II (B800-B850) from Rhodospirillum molischianum. Structure 4: 581-597PubMedGoogle Scholar
  71. Kraulis PJ (1991) Molscript — A program to produce both detailed and schematic plots of protein structures. J Appl Crystallogr 24: 946-950Google Scholar
  72. Krauss N, Hinrichs W, Witt I, Fromme P, Pritzkow W, Dauter Z, Betzel C, Wilson KS, Witt HT and Saenger W (1993) Threedimensional structure of system I of photosynthesis at 6 Å resolution. Nature 361: 326-331Google Scholar
  73. Kunji ERS, von Gronau S, Oesterhelt D and Henderson R (2000) The three-dimensional structure of halorhodopsin to 5 Ångstrom by electron crystallography: A new unbending procedure for two-dimensional crystals by using a global reference structure. Proc Natl Acad Sci USA 97: 4637-4642PubMedGoogle Scholar
  74. Kühlbrandt W (1992) Two-dimensional crystallization of membrane proteins. Q Rev Biophys 25: 1-49PubMedGoogle Scholar
  75. Kühlbrandt W and Williams KA (1999) Analysis of macromolecular structure and dynamics by electron cryo-microscopy. Curr Opin Chem Biol 3: 537-543PubMedGoogle Scholar
  76. Kühlbrandt W, Wang DN and Fujiyoshi Y (1994) Atomic model of plant light-harvesting complex by electron crystallography. Nature 367: 614-621PubMedGoogle Scholar
  77. Lange C, Nett JH, Trumpower BL and Hunte C (2001) Specific roles of protein-phospholipid interactions in the yeast cytochrome bc 1 complex structure. EMBO J 20: 6591-6600PubMedGoogle Scholar
  78. Lentzen M (2004) The tuning of a Zernike phase plate with defocus and variable spherical aberration and its use in HRTEM imaging. Ultramicroscopy 99: 211-220PubMedGoogle Scholar
  79. le Maire M, Champeil P and Møller JV (2001) Interaction of membrane proteins and lipids with solubilizing detergents. Biochim Biophys Acta 1508: 86-111Google Scholar
  80. Leslie C, Landree E, Collazo-Davila C, Bengu E, Grozea D and Marks LD (1999) Electron crystallography in surface structure analysis. Microsc Res Tech 46: 160-177PubMedGoogle Scholar
  81. Lévy D, Mosser G, Lambert O, Moeck GS, Bald D and Rigaud JL (1999) Two-dimensional crystallization on lipid layer: A successful approach for membrane proteins. J Struct Biol 127: 44-52PubMedGoogle Scholar
  82. Liu Z, Yan H, Wang K, Kuang T, Zhang J, Gui L, An X and Chang W (2004) Crystal structure of spinach major light-harvesting complex at 2.72Å resolution. Nature 428: 287-292PubMedGoogle Scholar
  83. Loll B, Kern J, Zouni A, Saenger W, Biesiadka J and Irrgang KD (2005) The antenna system of Photosystem II from Thermosynechococcus elongatus at 3.2Å resolution. Photosynth Res 86: 175-184PubMedGoogle Scholar
  84. Lyon MK, Marr KM and Furcinitti PS (1993) Formation and characterization of two-dimensional crystals of Photosystem II. J Struct Biol 110: 133-140PubMedGoogle Scholar
  85. Marr KM, Mastronarde D and Lyon MK (1996a) Two-dimensional crystals of Photosystem II: Biochemical characterization, cryoelectron microscopy and localization of the D1 and cytochrome b559 polypeptides. J Cell Biol 132: 823-833Google Scholar
  86. 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 17: 86-98Google Scholar
  87. McDermott G, Prince SM, Freer AA, Hawthornthwaite-Lawless AM, Papiz MZ, Cogdell RJ and Isaacs NW (1995) Crystal structure of an integral membrane light-harvesting complex from photosynthetic bacteria. Nature 374: 517-521Google Scholar
  88. Miller KR (1982) Three-dimensional structure of a photosynthetic membrane. Nature 300: 53-55Google Scholar
  89. Montoya G, Cyrklaff M and Sinning I (1995) Two-dimensional crystallization and preliminary structure analysis of light harvesting II (B800-B850) complex from the purple bacterium Rhodovulum sulfidophilum. J Mol Biol 250: 1-10PubMedGoogle Scholar
  90. 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: 837-849PubMedGoogle Scholar
  91. Mosser G (2001) Two-dimensional crystallogenesis of transmembrane proteins. Micron 32: 517-540PubMedGoogle Scholar
  92. Nakazato K, Toyoshima C, Enai I and Inoue Y (1996) Twodimensional crystallization and cryoelectron microscopy of Photosystem II. J Mol Biol 257: 225-232PubMedGoogle Scholar
  93. Oling F, Boekema EJ, de Zarate IO, Visschers R, van Grondelle R, Keegstra W, Brisson A and Picorel A (1996) Two-dimensional crystals of LH2 light-harvesting complexes from Ectothiorhodospira sp. and Rhodobacter capsulatus investigated by electron microscopy. Biochim Biophys Acta 1273: 44-50Google Scholar
  94. Orlova EV and Saibil HR (2004) Structure determination of macromolecular assemblies by single-particle analysis of cryoelectron micrographs. Curr Opin Struct Biol 14: 584-590PubMedGoogle Scholar
  95. Paulsen H, Finkenzeller B and Kühlen N (1993) Pigments induced folding of light-harvesting chlorophyll a/b-binding protein. Eur J Biochem 215: 809-816PubMedGoogle Scholar
  96. Potter CS, Pulokas J, Smith P, Suloway C and Carragher B (2004) Robotic grid loading system for a transmission electron microscope. J Struct Biol 146: 431-40PubMedGoogle Scholar
  97. Qian P, Hunter CN and Bullough PA (2005) The 8.5 Å projection structure of the core RC-LH1-PufX dimer of Rhodobacter sphaeroides. J Mol Biol 349: 948-960PubMedGoogle Scholar
  98. Ranck JL, Ruiz T, Pehau-Arnaudet G, Arboux B and Reiss-Husson F (2001) Two-dimensional structure of the native lightharvesting complex LH2 from Rubrivivax gelatinosus and of a truncated form. Biochim Biophys Acta 1506: 67-78PubMedGoogle Scholar
  99. Reimer R (1997) Transmission Electron Microscopy. Springer Publisher, Wien  , New YorkGoogle Scholar
  100. Rhee KH, Morris EP, Zheleva D, Hankamer B, Kühlbrandt W and Barber J (1997) Two-dimensional structure of plant Photosystem II at 8-Å resolution. Nature 389: 522-526Google Scholar
  101. Rhee KH, Morris E, Barber J and Kühlbrandt W (1998) Threedimensional structure of the Photosystem II reaction center at 8 Å resolution. Nature 396: 283-286PubMedGoogle Scholar
  102. Rigaud JL, Mosser G, Lacapere JJ, Olofsson A, Levy D and Ranck JL (1997) Bio-beads: An efficient strategy for twodimensional crystallization of membrane proteins. J Struct Biol 118: 226-235PubMedGoogle Scholar
  103. Rigaud JL, Chami M, Lambert O, Levy D and Ranck JL (2000) Use of detergents in two-dimensional crystallization of membrane proteins. Biochim Biophys Acta 1508: 112-128PubMedGoogle Scholar
  104. Rosenbusch JP, Lustig A, Grabo M, Zulauf M and Regenass M (2001) Approaches to determining membrane protein structures to high resolution: Do selections of subpopulations occur? Micron 32: 75-90PubMedGoogle Scholar
  105. Roszak AW, Howard TD, Southall J, Gardiner AT, Law CL, Isaacs NW and Cogdell RJ (2003) Crystal structure of the RC-LH1 core complex from Rhodopseudomonas palustris. Science 30: 1969-1972Google Scholar
  106. Sandona 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: 207-214PubMedGoogle Scholar
  107. Santini C, Tidu V, Tognon G, Magladi A and Bassi R (1994) Three-dimensional structure of the higher plant Photosystem II reaction center and evidence for its dimeric organization in vivo. J Biochem 221: 307-315Google Scholar
  108. Savage H, Cyrklaff M, Montoya G, Kühlbrandt W and Sinning I (1996) Two-dimensional structure of light harvesting complex II (LHII) from the purple bacterium Rhodovulum sulfidophilum and comparison with LHII from Rhodopseudomonas acidophila. Structure 4: 243-252PubMedGoogle Scholar
  109. Shaw PJ and Hills GJ (1981) Tilted specimen in the electron microscope: A simple specimen holder and the calculation of tilt angles for crystalline specimens. Micron 12: 279-282Google Scholar
  110. Siebert CA, Qian P, Fotiadis D, Engel A, Hunter CN and Bullough PA (2004) Molecular architecture of photosynthetic membranes in Rhodobacter sphaeroides: The role of PufX. EMBO J 23: 690-700PubMedGoogle Scholar
  111. Stahlberg H, Dubochet J, Vogel H and Gosh R (1998) Are lightharvesting I complexes from Rhodospirillum rubrum arranged around the reaction center in a square geometry? J Mol Biol 282: 819-831PubMedGoogle Scholar
  112. Stahlberg H, Fotiadis D, Scheuring S, Rémigy H, Braun T, Mitsuoka K, Fujiyoshi Y and Engel A (2001) Two-dimensional crystals: A powerful approach to assess structure, function and dynamics of membrane proteins. FEBS Lett 504: 166-172PubMedGoogle Scholar
  113. Standfuss J, van Scheltinga ACT, Lamborghini M and Kühlbrandt W (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea light-harvesting complex at 2.5 Å resolution. EMBO J 24: 919-928PubMedGoogle Scholar
  114. Stark W, Kühlbrandt W, Wildhaber H, Wehrli E and Mühlethaler K (1984) The structure of the photoreceptor unit of Rhodopseudomonas viridis. EMBO J 3: 777-783PubMedGoogle Scholar
  115. Toyoshima C and Unwin N (1990) Three-dimensional structure of the acetylcholine receptor by cryoelectron microscopy and helical image reconstruction. J Cell Biol 111: 2623-2635PubMedGoogle Scholar
  116. Tsiotis G, McDermott G and Ghanotakis D (1996) Progress towards structural elucidation of Photosystem II. Photosynth Res 50: 93-101Google Scholar
  117. Unger V (2000) Assessment of electron crystallographic data obtained from two-dimensional crystals of biological specimen. Acta Cryst D 56: 1259-1269Google Scholar
  118. Unger VM (2001) Electron cryomicroscopy methods. Curr Opin Struct Biol 11: 548-554PubMedGoogle Scholar
  119. Unwin N (2005) Refined structure of the nicotinic acetylcholine receptor at 4 Ångström resolution. J Mol Biol 346: 967-989PubMedGoogle Scholar
  120. Unwin PNT and Henderson R (1975) Molecular structure determination by electron microscopy of unstained crystalline specimens. J Mol Biol 94: 425-440PubMedGoogle Scholar
  121. Van Heel M, Gowen B, Matadeen R, Orlova EV, Finn R, Pape T, Cohen D, Stark H, Schmidt R, Schatz M and Patwardhan A (2000) Single-particle electron cryo-microscopy: Towards atomic resolution. Quart Rev Biophys 33: 307-369Google Scholar
  122. Walz T and Gosh R (1997) Two-dimensional crystallization of the light-harvesting I-reaction center photounit from Rhodospirillum rubrum. J Mol Biol 265: 107-111PubMedGoogle Scholar
  123. Walz T and Gregorieff N (1998) Electron crystallography of two-dimensional crystals of membrane proteins. J Struct Biol 121: 142-161PubMedGoogle Scholar
  124. Walz T, Jamieson SJ, Bowers CM, Bullough PA and Hunter CN (1998) Projection structures of three photosynthetic complexes from Rhodobacter sphaeroides: LH2 at 6 Å, LH1 and RC-LH1 at 25 Å. J Mol Biol 282: 833-845PubMedGoogle Scholar
  125. Wang DN and Kühlbrandt W (1991) High-resolution electron crystallography of light-harvesting chlorophyll a/b-protein complex in three different media. J Mol Biol 217: 691-699PubMedGoogle Scholar
  126. Werten PJL, Rémigy HW, de Groot BL, Fotiadis D, Philippsen A, Stahlberg H, Grubmüller H and Engel A (2002) Progress in the analysis of membrane protein structure and function. FEBS Lett 529: 65-72PubMedGoogle Scholar
  127. Williams RC and Fisher HW (1970) Electron microscopy of tobacco mosaic virus under conditions of minimal beam exposure. J Mol Biol 52: 121-123PubMedGoogle Scholar
  128. Yeager M, Unger VM and Mitra AK (1999) Three-dimensional structure of membrane proteins determined by two-dimensional crystallization. Electron cryomicroscopy and image analysis. Meth Enzymolog 294: 135-179Google Scholar
  129. Zemlin F (1998) Image formation in high-resolution electron microscopy. Cryst Res Technol 33: 1097-1111Google Scholar
  130. Zouni A, Witt HT, Kern J, Fromme P, Krauß N, Saenger W and Orth P (2001) Crystal structure of Photosystem II from Synechococcus elongatus at 3.8 Å resolution. Nature 409: 739-744PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V 2008

Authors and Affiliations

  • Paula C. A. da Fonseca
    • 1
  • Edward P. Morris
    • 1
  • Claudia Büchel
    • 2
  1. 1.Section of Structural BiologyChester Beatty LaboratoriesUK
  2. 2.Institute of Molecular BiosciencesUniversity of FrankfurtFrankfurt

Personalised recommendations