Architecture of Thylakoid Membrane Networks

  • Reinat NevoEmail author
  • Silvia G. Chuartzman
  • Onie Tsabari
  • Ziv Reich
  • Dana CharuviEmail author
  • Eyal Shimoni
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 30)


The primary events of oxygenic photosynthesis are carried out within intricate membrane lamellar systems called thylakoid networks. These networks, which are present in cyanobacteria, algae, and higher plants, accommodate all of the molecular complexes necessary for the light-driven reactions of photosynthesis and provide a medium for energy transduction. Here, we describe the ultrastructure of thylakoid membranes and their three-dimensional organization in various organisms along the evolutionary tree. Along the way we discuss issues pertaining to the formation and maintenance of these membranes, the means by which they enable molecular traffic within and across them, and the manner by which they respond to short- and long-term variations in light conditions.


Thylakoid Membrane Brown Alga Stroma Lamella Granal Stack Microcoleus Chthonoplastes 
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.



Chemical fixation




Cryo-electron microscopy of vitreous sections


Electron microscope tomography


Electron microscopy


Freeze substitution


High pressure freezing


Light-harvesting protein complexes


Photosystem I


Photosystem II






Ultraviolet radiation B (280–315 nm)


Ultraviolet radiation C (100–280 nm)



We thank Sharon G. Wolf for her helpful comments about electron microscopy techniques. This work was supported by a grant from the Israeli Science Foundation (Ziv Reich).


  1. Adir N (2005) Elucidation of the molecular structures of components of the phycobilisome: reconstructing a giant. Photosynth Res 85: 15–32PubMedGoogle Scholar
  2. Al-Amoudi A, Dubochet J, Gnaegi H, Lüthi W and Studer D (2003) An oscillating cryo-knife reduces cutting-induced deformation of vitreous ultrathin sections. J Microsc-Oxford 212: 26–33Google Scholar
  3. Al-Amoudi A, Chang JJ, Leforestier A, McDowall A, Sala-min LM, Norlen LPO, Richter K, Blanc NS, Studer D and Dubochet J (2004) Cryo-electron microscopy of vitreous sections. EMBO J 23: 3583–3588PubMedGoogle Scholar
  4. Al-Amoudi A, Studer D and Dubochet J (2005) Cutting artefacts and cutting process in vitreous sections for cryo-electron microscopy. J Struct Biol 150: 109–121PubMedGoogle Scholar
  5. Albertsson P (2001) A quantitative model of the domain structure of the photosynthetic membrane. Trends Plant Sci 6: 349–358PubMedGoogle Scholar
  6. Algera L, Belier JJ, Van Iterson W, Karstens WKH and Thung TH (1947) Some data on the structure of the chlo-roplast, obtained by electron microscopy. Biochim Bio-phys Acta 1: 517–526Google Scholar
  7. Allen JF (1990) How does protein phosphorylation control protein—protein interactions in the photosynthetic membrane? In: Baltscheffsky M (ed) Current Research in Photosynthesis 2. Kluwer, Dordrecht, pp. 915–918Google Scholar
  8. Allen JF (1992a) How does protein phosphorylation regulate photosynthesis? Trends Biochem Sci 17: 12–17Google Scholar
  9. Allen JF (1992b) Protein-phosphorylation in regulation of photosynthesis. Biochim Biophys Acta 1098: 275–335Google Scholar
  10. Allen JF and Forsberg J (2001) Molecular recognition in thylakoid structure and function. Trends Plant Sci 6: 317–326PubMedGoogle Scholar
  11. Allen JF, Bennett J, Steinback KE and Arntzen CJ (1981) Chloroplast protein-phosphorylation couples plasto-quinone redox state to distribution of excitation-energy between photosystems. Nature 291: 25–29Google Scholar
  12. Allen MM (1968) Photosynthetic membrane system in Ana-cystis nidulans. J Bacteriol 96: 836–841PubMedGoogle Scholar
  13. Anderson JM (1981) Consequences of spatial separation of photosystem-1 and photosystem-2 in thylakoid membranes of higher-plant chloroplasts. FEBS Lett 124: 1–10Google Scholar
  14. Anderson JM (1989) The grana margins of plant thylakoid membranes. Physiol Plant 76: 243–248Google Scholar
  15. Anderson JM (1999) Insights into the consequences of grana stacking of thylakoid membranes in vascular plants: a personal perspective. Aust J Plant Physiol 26: 625–639Google Scholar
  16. Anderson JM and Aro EM (1994) Grana stacking and protection of photosystem-II in thylakoid membranes of higher-plant leaves under sustained high irradiance — a hypothesis. Photosynth Res 41: 315–326Google Scholar
  17. Anderson JM and Vernon LP (1967) Digitonin incubation of spinach chloroplasts in tris(hydroxymethyl)methylgly-cine solutions of varying ionic strengths. Biochim Bio-phys Acta 143: 363–376Google Scholar
  18. Anderson JM, Chow WS and Goodchild DJ (1988) Thy-lakoid membrane organization in sunshade acclimation. Aust J Plant Physiol 15: 11–26Google Scholar
  19. 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: 427–440PubMedGoogle Scholar
  20. Aro EM and Ohad I (2003) Redox regulation of thylakoid protein phosphorylation. Antioxid Redox Sign 5: 55–67Google Scholar
  21. Arvidsson PO and Sundby C (1999) A model for the topology of the chloroplast thylakoid membrane. Aust J Plant Physiol 26: 687–694Google Scholar
  22. Atilgan E and Sun SX (2007) Shape transitions in lipid membranes and protein mediated vesicle fusion and fission. J Chem Phys 126: 095102–10PubMedGoogle Scholar
  23. Austin JR, Frost E, Vidi PA, Kessler F and Staehelin LA (2006) Plastoglobules are lipoprotein subcompartments of the chloroplast that are permanently coupled to thylakoid membranes and contain biosynthetic enzymes. Plant Cell 18: 1693–1703PubMedGoogle Scholar
  24. Bahatyrova S, Frese RN, Siebert CA, Olsen JD, van der Werf KO, van Grondelle R, Niederman RA, Bullough PA, Otto C and Hunter CN (2004) The native architecture of a photosynthetic membrane. Nature 430: 1058–1062PubMedGoogle Scholar
  25. Barber J (1980) 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 photosystem-I. FEBS Lett 118: 1–10Google Scholar
  26. Barber J (1982) Influence of surface-charges on thylakoid structure and function. Annu Rev Plant Physiol 33: 261–295Google Scholar
  27. Baumeister W (2002) Electron tomography: towards visualizing the molecular organization of the cytoplasm. Curr Opin Struc Biol 12: 679–684Google Scholar
  28. Beck M, Lučić V, Förster F, Baumeister W and Medalia O (2007) Snapshots of nuclear pore complexes in action cap tured by cryo-electron tomography. Nature 449: 611–615PubMedGoogle Scholar
  29. Bellafiore S, Bameche F, Peltier G and Rochaix JD (2005) State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 433: 892–895PubMedGoogle Scholar
  30. Bennett J (1977) Phosphorylation of chloroplast membrane polypeptides. Nature 269: 344–346Google Scholar
  31. Bennett J (1979a) Chloroplast phosphoproteins — phosphor-ylation of polypeptides of the light-harvesting chlorophyll protein complex. Eur J Biochem 99: 133–137Google Scholar
  32. Bennett J (1979b) Chloroplast phosphoproteins. The protein kinase of thylakoid membranes is light-dependent. FEBS Lett 103: 342–344Google Scholar
  33. Bennett J (1980) Chloroplast phosphoproteins — evidence for a thylakoid-bound phosphoprotein phosphatase. Eur J Biochem 104: 85–89PubMedGoogle Scholar
  34. Bennett J (1991) Protein-phosphorylation in green plant chloroplasts. Annu Rev Plant Physiol 42: 281–311Google Scholar
  35. Berkaloff C, Duval JC, Hauswirth N and Rousseau B (1983) Freeze-fracture study of thylakoids of Fucus serratus. J Phycol 19: 96–100Google Scholar
  36. Bjorkman O, Boardman NK, Anderson JM, Thorne SW, Goodchild DJ and Pyliotis NA (1972) Effect of light intensity during growth of Atriplex patula on the photo-synthetic capacity of photosynthetic reactions, chloroplast components and structure. Carnegie Institution of Washington Year Book, Vol 71. Carnegie Institution of Washington, Washington, pp. 115–135Google Scholar
  37. Blumwald E and Tel-Or E (1982) Structural aspects of the adaptation of Nostoc muscorum to salt. Arch Microbiol 132: 163–167Google Scholar
  38. Böhm J, Frangakis AS, Hegerl R, Nickell S, Typke D and Baumeister W (2000) Toward detecting and identifying macromolecules in a cellular context: template matching applied to electron tomograms. Proc Natl Acad Sci USA 97: 14245–14250PubMedGoogle Scholar
  39. Bonaventura C and Myers J (1969) Fluorescence and oxygen evolution from Chlorella pyrenoidosa. Biochim Bio-phys Acta 189: 366–383Google Scholar
  40. Bouchet-Marquis C, Starkuviene V and Grabenbauer M (2008) Golgi apparatus studied in vitreous sections. J Microsc-Oxford 230: 308–316Google Scholar
  41. Bouck GB (1965) Fine structure and organelle associations in brown algae. J Cell Biol 26: 523–537PubMedGoogle Scholar
  42. Brangeon J (1974) Structural modifications in lamellar system of isolated Zea mays chloroplasts under different ionic conditions. J Microsc-Oxford 21: 75–84Google Scholar
  43. Brangeon J and Mustárdy L (1979) Ontogenetic assembly of intra-chloroplastic lamellae viewed in 3-dimension. Biol Cell 36: 71–80Google Scholar
  44. Briantais JM, Vernotte C, Olive J and Wollman FA (1984) Kinetics of cation-induced changes of photosystem-II fluorescence and of lateral distribution of the 2 photosystems in the thylakoid membranes of pea chloroplasts. Biochim Biophys Acta 766: 1–8Google Scholar
  45. Brody M and Vatter AE (1959) Observations on cellular structures of Porphyridium cruentum. J Biophys Biochem Cytol 5: 289–294PubMedGoogle Scholar
  46. Carde JP, Joyard J and Douce R (1982) Electron-microscopic studies of envelope membranes from spinach plastids. Biol Cell 44: 315–324Google Scholar
  47. Cavalier-Smith T (2000) Membrane heredity and early chlo-roplast evolution. Trends Plant Sci 5: 174–182PubMedGoogle Scholar
  48. Chisholm SW, Olson RJ, Zettler ER, Goericke R, Water-bury JB and Welschmeyer NA (1988) A novel free-living prochlorophyte abundant in the oceanic euphotic zone. Nature 334: 340–343Google Scholar
  49. Chow WS (1984) Electron transport, photophosphorylation and thylakoid stacking. In: Sybesma C (ed) Advances in Photosynthesis Research, Vol III. Dr. W. Junk Publishers, The Hague, pp. 83–86Google Scholar
  50. Chow WS (1999) Grana formation: entropy-assisted local order in chloroplasts? Aust J Plant Physiol 26: 641–647Google Scholar
  51. Chow WS, Miller C and Anderson JM (1991) Surface-charges, the heterogeneous lateral distribution of the 2 photosystems, and thylakoid stacking. Biochim Biophys Acta 1057: 69–77Google Scholar
  52. Chow WS, Kim EH, Horton P and Anderson JM (2005) Granal stacking of thylakoid membranes in higher plant chloroplasts: the physicochemical forces at work and the functional consequences that ensue. Photochem Photobiol Sci 4: 1081–1090PubMedGoogle Scholar
  53. Chuartzman SG, Nevo R, Shimoni E, Charuvi D, Kiss V, Ohad I, Brumfeld V and Reich Z (2008) Thylakoid membrane remodeling during state transitions in Arabidopsis. Plant Cell 20: 1029–1039PubMedGoogle Scholar
  54. Collins VP, Arborgh B and Brunk U (1977) Comparison of effects of 3 widely used glutaraldehyde fixatives on cellular volume and structure — TEM, SEM, volumetric and cytochemical study. Acta Path Micro Im A 85: 157–168Google Scholar
  55. Consoli E, Croce R, Dunlap DD and Finzi L (2005) Diffusion of light-harvesting complex II in the thylakoid membranes. EMBO Rep 6: 782–786PubMedGoogle Scholar
  56. Crawley JC (1964) Cytoplasmic fine structure in Acetabu-laria. Exp Cell Res 35: 507–514PubMedGoogle Scholar
  57. Cyrklaff M, Linaroudis A, Boicu M, Chlanda P, Baumeister W, Griffiths G and Krijnse-Locker J (2007) Whole cell cryo-electron tomography reveals distinct disassembly intermediates of vaccinia virus. PLoS ONE 2: e420PubMedGoogle Scholar
  58. Dai W, Jia QM, Bortz E, Shah S, Liu J, Atanasov I, Li XD, Taylor KA, Sun R and Zhou ZH (2008) Unique structures in a tumor herpesvirus revealed by cryo-electron tomography and microscopy. J Struct Biol 161: 428–438PubMedGoogle Scholar
  59. Das G (1975) Changes in chloroplast structure during autospore formation in Scenedesmus obtusiusculus. Protoplasma 84: 175–180Google Scholar
  60. Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid membrane proteins in green plants. Biochim Biophys Acta 1706: 12–39PubMedGoogle Scholar
  61. Des Marais DJ (2000) Evolution — When did photosynthesis emerge on earth? Science 289: 1703–1705Google Scholar
  62. Doutreligne SJ (1935) Note sur la structure des chloroplastes. Proc Kon Acad Wetensch (Amsterdam) 38: 886–896Google Scholar
  63. Drepper F, Carlberg I, Andersson B and 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: 11915–11922PubMedGoogle Scholar
  64. Dubochet J and Blanc NS (2001) The cell in absence of aggregation artifacts. Micron 32: 91–99PubMedGoogle Scholar
  65. Dubochet J and McDowall AW (1981) Vitrification of pure water for electron microscopy. J Microsc-Oxford 124: Rp3–Rp4Google Scholar
  66. Dubochet J, Zuber B, Eltsov M, Bouchet-Marquis C, Al-Amoudi A and Livolant F (2007) How to “read” a vitreous section. Methods Cell Biol 79: 385–406PubMedGoogle Scholar
  67. Durnford DG, Deane JA, Tan S, McFadden GI, Gantt E and Green BR (1999) A phylogenetic assessment of the eukaryotic light-harvesting antenna proteins, with implications for plastid evolution. J Mol Evol 48: 59–68PubMedGoogle Scholar
  68. Edwards MR and Gantt E (1971) Phycobilisomes of the thermophilic blue-green alga Synechococcus lividus. J Cell Biol 50: 896–900PubMedGoogle Scholar
  69. Edwards MR, Berns DS, Ghiorse WC and Holt SC (1968) Ultrastructure of thermophilic blue-green alga Synechoc-occus lividus Copeland. J Phycol 4: 283–298Google Scholar
  70. Evans LV (1966) Distribution of pyrenoids among some brown algae. J Cell Sci 1: 449–454PubMedGoogle Scholar
  71. Falk RH and Sitte P (1963) Zellfeinbau bei Plasmolyse. I. Der Feinbau der Elodea-Blattzellen. Protoplasma 57: 290–303Google Scholar
  72. Falkowski PG (2006) Evolution — tracing oxygen's imprint on earth's metabolic evolution. Science 311: 1724–1725PubMedGoogle Scholar
  73. Falkowski PG, Katz ME, Knoll AH, Quigg A, Raven JA, Schofield O and Taylor FJ (2004) The evolution of modern eukaryotic phytoplankton. Science 305: 354–360PubMedGoogle Scholar
  74. Förster F, Medalia O, Zauberman N, Baumeister W and Fass D (2005) Retrovirus envelope protein complex structure in situ studied by cryo-electron tomography. Proc Natl Acad Sci USA 102: 4729–4734PubMedGoogle Scholar
  75. Frey TG and Mannella CA (2000) The internal structure of mitochondria. Trends Biochem Sci 25: 319–324PubMedGoogle Scholar
  76. Gantt E and Conti SF (1965) Ultrastructure of Porphyridium cruentum. J Cell Biol 26: 365–381PubMedGoogle Scholar
  77. Gantt E and Conti SF (1966) Granules associated with chlo-roplast lamellae of Porphyridium cruentum. J Cell Biol 29: 423–434PubMedGoogle Scholar
  78. Gantt E and Conti SF (1969) Ultrastructure of blue-green algae. J Bacteriol 97: 1486–1493PubMedGoogle Scholar
  79. Gao H, Sage TL and Osteryoung KW (2006) FZL, an FZO-like protein in plants, is a determinant of thylakoid and chloroplast morphology. Proc Natl Acad Sci USA 103: 6759–6764PubMedGoogle Scholar
  80. Garab G, Kieleczawa J, Sutherland JC, Bustamante C and Hind G (1991) Organization of pigment protein complexes into macrodomains in the thylakoid membranes of wild-type and chlorophyll b-less mutant of barley as revealed by circular dichroism. Photochem Photobiol 54: 273–281Google Scholar
  81. Gibbs SP (1970) Comparative ultrastructure of algal chloro-plast. Ann NY Acad Sci 175: 454–473Google Scholar
  82. Giddings TH, Withers NW and Staehelin LA (1980) Supramolecular structure of stacked and unstacked regions of the photosynthetic membranes of Prochloron sp., a Prokaryote. Proc Natl Acad Sci USA 77: 352–356PubMedGoogle Scholar
  83. Goodale GL (1889) Protoplasm and its history. Science 14: 352–355Google Scholar
  84. Goodchild DJ, Highkin HR and Boardman NK (1966) The fine structure of chloroplasts in a barley mutant lacking chlorophyll b. Exp Cell Res 43: 684–688PubMedGoogle Scholar
  85. Goodchild DJ, Björkman O and Pyliotis NA (1972) Chlo-roplast ultrastructure, leaf anatomy, and soluble protein in rainforest species. Carnegie Institution of Washington Year Book, Vol 71. Carnegie Institution of Washington, Washington, pp. 102–107Google Scholar
  86. Goodenough UW and Levine RP (1969) Chloroplast ultrastructure in mutant strains of Chlamydomonas rein-hardi lacking components of photosynthetic apparatus. Plant Physiol 44: 990–993PubMedGoogle Scholar
  87. Granick S and Porter KR (1947) The structure of the spinach chloroplast as interpreted with the electron microscope. Am J Bot 34: 545–550Google Scholar
  88. Gray MW (1992) The endosymbiont hypothesis revisited. Int Rev Cytol 141: 233–357PubMedGoogle Scholar
  89. Grebvy C, Axelsson L and Sundqvist C (1989) Light-independent plastid differentiation in the brown alga Laminaria saccharina (Phaeophyceae). Phycologia 28: 375–384Google Scholar
  90. Grossman AR, Schaefer MR, Chiang GG and Collier JL (1993) The phycobilisome, a light-harvesting complex responsive to environmental conditions. Microbiol Rev 57: 725–749PubMedGoogle Scholar
  91. Guglielmi G, Cohen-Bazire G and Bryant DA (1981) The structure of Gloeobacter violaceus and its phycobili-somes. Arch Microbiol 129: 181–189Google Scholar
  92. Haldrup A, Jensen PE, Lunde C and Scheller HV (2001) Balance of power: a view of the mechanism of photosyn-thetic state transitions. Trends Plant Sci 6: 301–305PubMedGoogle Scholar
  93. Hall DH (1995) Electron microscopy and three-dimensional image reconstruction. Methods Cell Biol 48: 395–436PubMedGoogle Scholar
  94. Han HM, Zuber B and Dubochet J (2008) Compression and crevasses in vitreous sections under different cutting conditions. J Microsc-Oxford 230: 167–171Google Scholar
  95. Heitz E (1936) Untersuchungen über den Bau der Plastiden I: die gerichteten Chlorophyllscheiben der Chloroplasten. Planta 26: 134–163Google Scholar
  96. Heslop-Harrison J (1963) Structure and morphogenesis of lamellar systems in grana-containing chloroplasts. Planta 60: 243–260Google Scholar
  97. Hess MW (2007) Cryopreparation methodology for plant cell biology. Method Cell Biol 79: 57–100Google Scholar
  98. Hodge AJ, McLean JD and Mercer FV (1955) Ultrastructure of the lamellae and grana in the chloroplasts of Zea mays. J Biophys Biochem Cytol 1: 605–614PubMedGoogle Scholar
  99. Hodges M and Barber J (1983) State 1-state 2 transitions in a unicellular green algae: analysis of in vivo chlorophyll fluorescence induction curves in the presence of 3-(3,4-dichlorophenyl)-1, 1-dimethylurea (DCMU). Plant Physiol 72: 1119–1122PubMedGoogle Scholar
  100. Hoober JK, Boyd CO and Paavola LG (1991) Origin of thy-lakoid membranes in Chlamydomonas reinhardtii y-1 at 38°C. Plant Physiol 96: 1321–1328PubMedGoogle Scholar
  101. Hoog JL and Antony C (2007) Whole-cell investigation of microtubule cytoskeleton architecture by electron tomography. Methods Cell Biol 79: 145–167PubMedGoogle Scholar
  102. Horton P (1999) Are grana necessary for regulation of light harvesting? Aust J Plant Physiol 26: 659–669Google Scholar
  103. Horton P and Black MT (1983) A comparison between cation and protein-phosphorylation effects on the fluorescence induction curve in chloroplasts treated with 3-(3,4-dichlorophenyl)-1,1-dimethylurea. Biochim Bio-phys Acta 722: 214–218Google Scholar
  104. Horton P and Ruban A (2005) Molecular design of the photosystem II light-harvesting antenna: photosynthesis and photoprotection. J Exp Bot 56: 365–373PubMedGoogle Scholar
  105. Horton P, Wentworth M and Ruban A (2005) Control of the light harvesting function of chloroplast membranes: the LHCII-aggregation model for non-photochemical quenching. FEBS Lett 579: 4201–4206PubMedGoogle Scholar
  106. Hsieh CE, Marko M, Frank J and Mannella CA (2002) Electron tomographic analysis of frozen-hydrated tissue sections. J Struct Biol 138: 63–73PubMedGoogle Scholar
  107. Hsieh CE, Leith A, Mannella CA, Frank J and Marko M (2006) Towards high-resolution three-dimensional imaging of native mammalian tissue: electron tomography of frozen-hydrated rat liver sections. J Struct Biol 153: 1–13PubMedGoogle Scholar
  108. Humbel B and Müller M (1986) Freeze-substitution and low temperature embedding. In: Müller M, Becker RP, Boyde A and Wolosewick JJ (eds) Science of Biological Specimen Preparation 1995. SEM, Inc. AFM O'Hara, Chicago, IL, pp. 175–183Google Scholar
  109. Izawa S and Good NE (1966) Effect of salts and electron transport on conformation of isolated chloroplasts. II. Electron microscopy. Plant Physiol 41: 544–552Google Scholar
  110. Jensen GJ and Briegel A (2007) How electron cryotomogra-phy is opening a new window onto prokaryotic ultrastructure. Curr Opin Struc Biol 17: 260–267Google Scholar
  111. Joliot P and Joliot A (2002) Cyclic electron transfer in plant leaf. Proc Natl Acad Sci USA 99: 10209–10214PubMedGoogle Scholar
  112. Joliot P and Joliot A (2005) Quantification of cyclic and linear flows in plants. Proc Natl Acad Sci USA 102: 4913–4918PubMedGoogle Scholar
  113. Jonas J (1982) Nuclear magnetic resonance at high pressure. Science 216: 1179–1184PubMedGoogle Scholar
  114. Kaftan D, Brumfeld V, Nevo R, Scherz A and Reich Z (2002) From chloroplasts to photosystems: in situ scanning force microscopy on intact thylakoid membranes. EMBO J 21: 6146–6153PubMedGoogle Scholar
  115. Kanervo E, Suorsa M and Aro EM (2005) Functional flexibility and acclimation of the thylakoid membrane. Photo-chem Photobiol Sci 4: 1072–1080Google Scholar
  116. Kausche GA and Ruska H (1940) Zur Frage der Chloroplas-tenstruktur. Naturwissenschaften 28: 303–304Google Scholar
  117. Kellenberger E, Johansen R, Maeder M, Bohrmann B, Stauffer E and Villiger W (1992) Artifacts and morphological changes during chemical fixation. J Microsc-Oxford 168: 181–201Google Scholar
  118. Kenrick P and Crane PR (1997) The origin and early evolution of plants on land. Nature 389: 33–39Google Scholar
  119. Kim EH, Chow WS, Horton P and Anderson JM (2005) Entropy-assisted stacking of thylakoid membranes. Bio-chim Biophys Acta 1708: 187–195Google Scholar
  120. Kirchhoff H, Haferkamp S, Allen JF, Epstein DB and Mul-lineaux CW (2008) Protein diffusion and macromolecu-lar crowding in thylakoid membranes. Plant Physiol 146: 1571–1578PubMedGoogle Scholar
  121. Knoll G, Verkleij AJ and Plattner H (1987) Cryofixation of dynamic processes in cells. In: Steinbrecht RA and Zierold K (eds) Cryotechniques in Biological Electron Microscopy. Springer-Verlag, Berlin, pp. 258–271Google Scholar
  122. Komárek J and Cepák V (1998) Cytomorphological characters supporting the taxonomic validity of Cyanothece (Cyanoprokaryota). Plant Syst Evol 210: 25–39Google Scholar
  123. Koning RI, Zovko S, Barcena M, Oostergetel GT, Koerten HK, Galjart N, Koster AJ and Mieke Mommaas A (2008) Cryo electron tomography of vitrified fibroblasts: micro-tubule plus ends in situ. J Struct Biol 161: 459–468PubMedGoogle Scholar
  124. Konorty M, Kahana N, Linaroudis A, Minsky A and Medalia O (2008) Structural analysis of photosynthetic membranes by cryo-electron tomography of intact Rhodopseu-domonas viridis cells. J Struct Biol 161: 393–400PubMedGoogle Scholar
  125. Kramer DM, Avenson TJ and Edwards GE (2004) Dynamic flexibility in the light reactions of photosynthesis governed by both electron and proton reactions. Trends Plant Sci 9: 349–357PubMedGoogle Scholar
  126. Kroll D, Meierhoff K, Bechtold N, Kinoshita M, Westphal S, Vothknecht UC, Soll J and Westhoff P (2001) VIPP1, a nuclear gene of Arabidopsis thaliana essential for thy-lakoid membrane formation. Proc Natl Acad Sci USA 98: 4238–4242PubMedGoogle Scholar
  127. Kunkel DD (1982) Thylakoid centers: structures associated with the cyanobacterial photosynthetic membrane system. Arch Microbiol 133: 97–99Google Scholar
  128. Kurner J, Medalia O, Linaroudis AA and Baumeister W (2004) New insights into the structural organization of eukaryotic and prokaryotic cytoskeletons using cryo-electron tomography. Exp Cell Res 301: 38–42PubMedGoogle Scholar
  129. Kutik J (1998) The development of chloroplast structure during leaf ontogeny. Photosynthetica 35: 481–505Google Scholar
  130. Kyle DJ, Staehelin LA and Arntzen CJ (1983) Lateral mobility of the light-harvesting complex in chloroplast membranes controls excitation energy distribution in higher plants. Arch Biochem Biophys 222: 527–541PubMedGoogle Scholar
  131. Lee RMKW, McKenzie R, Kobayashi K, Garfield RE, Forrest JB and Daniel EE (1982) Effects of glutaraldehyde fixative osmolarities on smooth-muscle cell-volume, and osmotic reactivity of the cells after fixation. J Microsc-Oxford 125: 77–88Google Scholar
  132. Lembi CA and Lang NJ (1965) Electron microscopy of cart-eria and Chlamydomonas. Am J Bot 52: 464–477Google Scholar
  133. Lewin RA (2002) Prochlorophyta — a matter of class distinctions. Photosynth Res 73: 59–61PubMedGoogle Scholar
  134. Li HM, Kaneko Y and Keegstra K (1994) Molecular cloning of a chloroplastic protein associated with both the envelope and thylakoid membranes. Plant Mol Biol 25: 619–632PubMedGoogle Scholar
  135. Liberton M and Pakrasi HB (2008) Membrane system in cyanobacteria. In: Herrero A and Flores E (eds) The Cyanobacteria: Molecular Biology, Genomics and Evolution. Caister Academic Press, Norfolk, VA, pp. 271–287Google Scholar
  136. Liberton M, Howard Berg R, Heuser J, Roth R and Pakrasi HB (2006) Ultrastructure of the membrane systems in the unicellular cyanobacterium Synechocystis sp. strain PCC 6803. Protoplasma 227: 129–138Google Scholar
  137. Lichtle C, Spilar A and Duval JC. (1992) Immunogold localization of light-harvesting and photosystem-I complexes in the thylakoids of Fucus serratus (Phaeophyceae). Protoplasma 166: 99–106Google Scholar
  138. Lopez-Juez E and Pyke KA (2005) Plastids unleashed: their development and their integration in plant development. Int J Dev Biol 49: 557–577PubMedGoogle Scholar
  139. Lučić V, Förster F and Baumeister W (2005) Structural studies by electron tomography: from cells to molecules. Annu Rev Biochem 74: 833–865PubMedGoogle Scholar
  140. Lüdemann HD (1996) Recent developments in high pressure high resolution NMR in liquids. Pol J Chem 70: 387–408Google Scholar
  141. Lunde C, Jensen PE, Haldrup A, Knoetzel J and Scheller HV (2000) The PSI-H subunit of photosystem I is essential for state transitions in plant photosynthesis. Nature 408: 613–615PubMedGoogle Scholar
  142. Macagno ER, Levinthal C and Sobel I (1979) 3-Dimensional computer reconstruction of neurons and neuronal assemblies. Annu Rev Biophys Bio 8: 323–351Google Scholar
  143. Maneta-Peyret L, Compere P, Moreau P, Goffinet G and Cassagne C (1999) Immunocytochemistry of lipids: chemical fixatives have dramatic effects on the preservation of tissue lipids. Histochem J 31: 541–547PubMedGoogle Scholar
  144. Mannella CA (2006) The relevance of mitochondrial membrane topology to mitochondrial function. Biochim Bio-phys Acta 1762: 140–147Google Scholar
  145. Mannella CA, Pfeiffer DR, Bradshaw PC, Moraru, II, Slep-chenko B, Loew LM, Hsieh CE, Buttle K and Marko M (2001) Topology of the mitochondrial inner membrane: dynamics and bioenergetic implications. IUBMB Life 52: 93–100PubMedGoogle Scholar
  146. Marko M, Hsieh C, Schalek R, Frank J and Mannella C (2007) Focused-ion-beam thinning of frozen-hydrated biological specimens for cryo-electron microscopy. Nat Methods 4: 215–217PubMedGoogle Scholar
  147. Marsh BJ, Mastronarde DN, Buttle KF, Howell KE and McIntosh JR (2001) Organellar relationships in the Golgi region of the pancreatic beta cell line, HIT-T15, visualized by high resolution electron tomography. Proc Natl Acad Sci U S A 98: 2399–2406PubMedGoogle Scholar
  148. Mastronarde DN, Ladinsky MS and McIntosh JR (1997) Super-thin serial sectioning for high-resolution 3-D reconstruction of cellular structures. Microsc Microanal 3: 221–222Google Scholar
  149. Matthijs HC, Van der Staay GWM and Mur LR (1994) Prochlorophytes: the other cyanobacteria? In: Bryant DA (ed) The Molecular Biology of Cyanobacteria. Kluwer, Dordrecht, pp. 49–64Google Scholar
  150. McCourt RM (1995) Green algal phylogeny. Trends Ecol Evol 10: 159–163PubMedGoogle Scholar
  151. McDonald K (2007) Cryopreparation methods for electron microscopy of selected model systems. Method Cell Biol 79: 23–56Google Scholar
  152. McDonnel A and Staehelin LA (1980) Adhesion between liposomes mediated by the chlorophyll a-b light-harvesting complex isolated from chloroplast membranes. J Cell Biol 84: 40–56PubMedGoogle Scholar
  153. McEwen BF and Marko M (1999) Three-dimensional transmission electron microscopy and its application to mitosis research. Methods Cell Biol 61: 81–111PubMedGoogle Scholar
  154. McEwen BF and Marko M (2001) The emergence of electron tomography as an important tool for investigating cellular ultrastructure. J Histochem Cytochem 49: 553–563PubMedGoogle Scholar
  155. Medalia O, Weber I, Frangakis AS, Nicastro D, Gerisch G and Baumeister W (2002) Macromolecular architecture in eukaryotic cells visualized by cryoelectron tomography. Science 298: 1209–1213PubMedGoogle Scholar
  156. Meisch HU, Becker LJM and Schwab D (1980) Ultrastructural changes in Chlorella fusca during iron-deficiency and vanadium treatment. Protoplasma 103: 273–280Google Scholar
  157. Melloy P, Shen S, White E, McIntosh JR and Rose MD (2007) Nuclear fusion during yeast mating occurs by a three-step pathway. J Cell Biol 179: 659–670PubMedGoogle Scholar
  158. Menke W (1940a) Die Lamellarstruktur der Chloroplasten im ultravioletten Licht. Naturwissenesch 28: 158–159Google Scholar
  159. Menke W (1940b) Untersuchungen über den Feinbau des Protoplasmas mit dem Universal-Elektronenmikroskop. Protoplasma 35: 115–130Google Scholar
  160. Menke W (1960) Das allgemeine Bauprinzip des Lamel-larsystems der Chloroplasten. Experientia 16: 537–538Google Scholar
  161. Menke W (1962) Über die Chloroplasten von Anthoceros punctatus. Zeit Naturforsch 16: 334–336Google Scholar
  162. Menke W (1966) The structure of the chloroplasts. In Goodwin TE (ed) Biochemistry of Chloroplasts, Vol 1. Academic Press, New York, pp. 3–18Google Scholar
  163. Merchant S and Sawaya MR (2005) The light reactions: A guide to recent acquisitions for the picture gallery. Plant Cell 17: 648–663PubMedGoogle Scholar
  164. Meyer A (1883) Das Chlorophyllkorn in chemischer, morphologischer und biologischer Beziehung, Arthur Felix LeipzigGoogle Scholar
  165. Michel M, Hillmann T and Müller M (1991) Cryosection-ing of plant-material frozen at high-pressure. J Microsc-Oxford 163: 3–18Google Scholar
  166. Miller KR, Jacob JS, Burger-Wiersma T and Matthijs HC (1988) Supramolecular structure of the thylakoid membrane of Prochlorothrix hollandica: a chlorophyll b-containing prokaryote. J Cell Sci 91: 577–586PubMedGoogle Scholar
  167. Mironov AA, Beznoussenko GV, Nicoziani P, Martella O, Trucco A, Kweon HS, Di Giandomenico D, Polishchuk RS, Fusella A, Lupetti P, Berger EG, Geerts WJC, Koster AJ, Burger KNJ and Luini A (2001) Small cargo proteins and large aggregates can traverse the Golgi by a common mechanism without leaving the lumen of cisternae. J Cell Biol 155: 1225–1238PubMedGoogle Scholar
  168. Misteli T and Warren G (1995) Mitotic disassembly of the Golgi apparatus in vivo. J Cell Sci 108: 2715–2727PubMedGoogle Scholar
  169. Mogelsvang S, Gomez-Ospina N, Soderholm J, Glick BS and Staehelin LA (2003) Tomographic evidence for continuous turnover of Golgi cisternae in Pichia pastoris. Mol Biol Cell 14: 2277–2291PubMedGoogle Scholar
  170. Monaghan P, Perusinghe N and Müller M (1998) High-pressure freezing for immunocytochemistry. J Microsc-Oxford 192: 248–258Google Scholar
  171. Moor H (1987) Theory and practice of high-pressure freezing. In: Steinbrecht RA and Zierold K (eds) Cryo-Techniques in Biological Electron Microscopy. Springer Verlag, Berlin, pp. 175–191Google Scholar
  172. Moor H and Hoechli M (1970) The influence of high-pressure freezing on living cells. In: Favard P (ed) Societe Fran-caise de Microscopie Lectronique, Vol 1. Proceedings of the 7th International Congress of Electron Microscopy, Paris, pp. 449–450.Google Scholar
  173. Morré DJ, Séllden G, Sundqvist C and Sandelius AS (1991) Stromal low temperature compartment derived from the inner membrane of the chloroplast envelope. Plant Phys-iol 97: 1558–1564Google Scholar
  174. Mühlethaler K and Frey-Wyssling A (1959) Entwicklung und Struktur der Proplastiden. J Biophys Biochem Cytol 6: 507–512Google Scholar
  175. Mullet JE and Arntzen CJ (1980) Simulation of grana stacking in a model membrane system. Mediation by a purified light-harvesting pigment-protein complex from chloro-plasts. Biochim Biophys Acta 589: 100–117PubMedGoogle Scholar
  176. Mullineaux CW (1999) The thylakoid membranes of cyano-bacteria: structure, dynamics and function. Aust J Plant Phys 26: 671–677Google Scholar
  177. Mullineaux CW (2008) Biogenesis and dynamics of thy-lakoid membranes and the photosynthetic apparatus. In: Herrero A and Flores E (eds) The Cyanobacteria: Molecular Biology, Genomics and Evolution. Caister Academic Press, Norfolk, VA, pp. 289–309Google Scholar
  178. Mullineaux CW and Emlyn-Jones D (2005) State transitions: an example of acclimation to low-light stress. J Exp Bot 56: 389–393PubMedGoogle Scholar
  179. Murakami S and Packer L (1971) Role of cations in organization of chloroplast membranes. Arch Biochem Biophys 146: 337–347PubMedGoogle Scholar
  180. Murata N (1969) Control of excitation transfer in photosynthesis. I. Light-induced change of chlorophyll a fluorescence in Porphyridium cruentum. Biochim Biophys Acta 172: 242–251PubMedGoogle Scholar
  181. Murk JLAN, Posthuma G, Koster AJ, Geuze HJ, Verkleij AJ, Kleijmeer MJ and Humbel BM (2003) Influence of aldehyde fixation on the morphology of endosomes and lysosomes: quantitative analysis and electron tomography. J Microsc-Oxford 212: 81–90Google Scholar
  182. Murphy GE, Leadbetter JR and Jensen GJ (2006) In situ structure of the complete Treponema primitia flagellar motor. Nature 442: 1062–1064PubMedGoogle Scholar
  183. Mustárdy L (1996) Development of thylakoid membrane stacking. In: Ort DR and Yocum CF (eds) Oxygenic Photosynthesis: The Light Reactions. Kluwer, Dordrecht, pp. 59–68Google Scholar
  184. Mustárdy L and Garab G (2003) Granum revisited. A three-dimensional model — where things fall into place. Trends Plant Sci 8: 117–122PubMedGoogle Scholar
  185. Mustárdy LA and Jánossy AGS (1979) Evidence of helical thylakoid arrangement by scanning electron-microscopy. Plant Sci Lett 16: 281–284Google Scholar
  186. Nagayama K and Danev R (2008) Phase contrast electron microscopy: development of thin-film phase plates and biological applications. Philos Trans R Soc Lond B Biol Sci 363: 2153–2162PubMedGoogle Scholar
  187. Nakamura Y, Kaneko T, Sato S, Mimuro M, Miyashita H, Tsuchiya T, Sasamoto S, Watanabe A, Kawashima K, Kishida Y, Kiyokawa C, Kohara M, Matsumoto M, Mat-suno A, Nakazaki N, Shimpo S, Takeuchi C, Yamada M and Tabata S (2003) Complete genome structure of Gloeobacter violaceus PCC 7421, a cyanobacterium that lacks thylakoids. DNA Res 10: 137–145PubMedGoogle Scholar
  188. Nelson N and Ben-Shem A (2004) The complex architecture of oxygenic photosynthesis. Nat Rev Mol Cell Bio 5: 971–982Google Scholar
  189. Neushul M (1971) Uniformity of thylakoid structure in a red, a brown, and two blue-green algae. J Ultrastruct Res 37: 532–543PubMedGoogle Scholar
  190. Nevo R, Charuvi D, Shimoni E, Schwarz R, Kaplan A, Ohad I and Reich Z (2007) Thylakoid membrane perforations and connectivity enable intracellular traffic in cyanobac-teria. EMBO J 26: 1467–1473PubMedGoogle Scholar
  191. Nicastro D, Frangakis AS, Typke D and Baumeister W (2000) Cryo-electron tomography of neurospora mitochondria. J Struct Biol 129: 48–56PubMedGoogle Scholar
  192. Nicastro D, McIntosh JR and Baumeister W (2005) 3D structure of eukaryotic flagella in a quiescent state revealed by cryo-electron tomography. Proc Natl Acad Sci USA 102: 15889–15894PubMedGoogle Scholar
  193. Nierzwicki-Bauer SA, Balkwill DL and Stevens SE (1983) 3-Dimensional ultrastructure of a unicellular cyanobacte-rium. J Cell Biol 97: 713–722PubMedGoogle Scholar
  194. Noske AB, Costin AJ, Morgan GP and Marsh BJ (2008) Expedited approaches to whole cell electron tomography and organelle mark-up in situ in high-pressure frozen pancreatic islets. J Struct Biol 161: 298–313PubMedGoogle Scholar
  195. Ohad I, Siekevit P and Palade GE (1967a) Biogenesis of chloroplast membranes. I. Plastid dedifferentiation in a dark-grown algal mutant (Chlamydomonas reinhardi). J Cell Biol 35: 521–551Google Scholar
  196. Ohad I, Siekevit P and Palade GE (1967b) Biogenesis of chloroplast membranes.II. Plastid differentiation during greening of a dark-grown algal mutant (Chlamydomonas Reinhardi). J Cell Biol 35: 553–584Google Scholar
  197. O'Toole ET, Winey M and McIntosh JR (1999) High-voltage electron tomography of spindle pole bodies and early mitotic spindles in the yeast Saccharomyces cerevisiae. Mol Biol Cell 10: 2017–2031PubMedGoogle Scholar
  198. O'Toole ET, Giddings TH Jr and Dutcher SK (2007) Understanding microtubule organizing centers by comparing mutant and wild-type structures with electron tomography. Methods Cell Biol 79: 125–143PubMedGoogle Scholar
  199. Pali T, Garab G, Horvath LI and Kota Z (2003) Functional significance of the lipid-protein interface in photosyn-thetic membranes. Cell Mol Life Sci 60: 1591–1606PubMedGoogle Scholar
  200. Palmer JD (2000) Molecular evolution — A single birth of all plastids? Nature 405: 32–33PubMedGoogle Scholar
  201. Paolillo DJ Jr (1970) The three-dimensional arrangement of intergranal lamellae in chloroplasts. J Cell Sci 6: 243–255PubMedGoogle Scholar
  202. Paolillo DJ Jr and Falk RH (1966) The ultrastructure of grana in mesophyll plastids of Zea mays. Am J Bot 53: 173–180Google Scholar
  203. Paolillo DJ, Mackay NC and Graffius JR (1969) Structure of grana in flowering plants. Am J Bot 56: 344–347Google Scholar
  204. Penczek P, Marko M, Buttle K and Frank J (1995) Double-tilt electron tomography. Ultramicroscopy 60: 393–410PubMedGoogle Scholar
  205. Pendland JC and Aldrich HC (1973) Ultrastructural organization of chloroplast thylakoids of green-alga Oocystis marssonii. J Cell Biol 57: 306–314PubMedGoogle Scholar
  206. Penttila A, McDowell EM and Trump BF (1975) Effects of fixation and post-fixation treatments on volume of injured cells. J Histochem Cytochem 23: 251–270PubMedGoogle Scholar
  207. Perkins GA, Sosinsky GE, Ghassemzadeh S, Perez A, Jones Y and Ellisman MH (2008) Electron tomographic analysis of cytoskeletal cross-bridges in the paranodal region of the node of Ranvier in peripheral nerves. J Struct Biol 161: 469–480PubMedGoogle Scholar
  208. Pfeiffer S and Krupinska K (2005) Chloroplast ultrastructure in leaves of Urtica dioica L. analyzed after high-pressure freezing and freeze-substitution and compared with conventional fixation followed by room temperature dehydration. Microsc Res Tech 68: 368–376Google Scholar
  209. Pfeiffer S, Vielhaber G, Vietzke JP, Wittern KP, Hintze U and Wepf R (2000) High-pressure freezing provides new information on human epidermis: simultaneous protein antigen and lamellar lipid structure preservation. Study on human epidermis by cryoimmobilization. J Invest Der-matol 114: 1030–1038Google Scholar
  210. Plattner H (1989) Current trends in the electron microscopic analysis of dynamic processes in the field of cell and molecular biology. In: Plattner H (ed) Electron Microscopy of Subcellular Dynamics. CRC, Boca Raton, FL, pp. 1–12Google Scholar
  211. Porta D, Rippka R and Hernandez-Marine M (2000) Unusual ultrastructural features in three strains of Cyanothece (cyanobacteria). Arch Microbiol 173: 154–163PubMedGoogle Scholar
  212. Puhka M, Vihinen H, Joensuu M and Jokitalo E (2007) Endoplasmic reticulum remains continuous and undergoes sheet-to-tubule transformation during cell division in mammalian cells. J Cell Biol 179: 895–909PubMedGoogle Scholar
  213. Reddy KJ, Haskell JB, Sherman DM and Sherman LA (1993) Unicellular, aerobic nitrogen-fixing cyanobacteria of the genus Cyanothece. J Bacteriol 175: 1284–1292PubMedGoogle Scholar
  214. Rippka R, Waterbury J and Cohen-Bazire G (1974) Cyano-bacterium which lacks thylakoids. Arch Microbiol 100: 419–436Google Scholar
  215. Robertson D and Laetsch WM (1974) Structure and function of developing barley plastids. Plant Physiol 54: 148–159PubMedGoogle Scholar
  216. Robinson J, Tan AU, Wilensky RL, Matthai W, Munoz M and Rosas SE (2007) Electron-beam computerized tomography correlates with coronary angiogram in chronic kidney disease patients. Am J Nephrol 27: 247–252PubMedGoogle Scholar
  217. Rozema J, Björn LO, Bornman JF, Gaberscik A, Häder DP, Trost T, Germ M, Klisch M, Gröniger A, Sinha RP, Lebert M, He Y-Y, Buffoni-Hall R, de Bakker NVJ, van de Staaij J and Meijkamp BB (2002) The role of UV-B radiation in aquatic and terrestrial ecosystems—an experimental and functional analysis of the evolution of UV-absorbing compounds. J Photochem Photobiol B 66: 2–12PubMedGoogle Scholar
  218. Scheffel A, Gruska M, Faivre D, Linaroudis A, Plitzko JM and Schuler D (2006) An acidic protein aligns magneto-somes along a filamentous structure in magnetotactic bacteria. Nature 440: 110–114PubMedGoogle Scholar
  219. Scheuring S and Sturgis JN (2005) Chromatic adaptation of photosynthetic membranes. Science 309: 484–487PubMedGoogle Scholar
  220. Scheuring S, Seguin J, Marco S, Levy D, Robert B and Rigaud JL (2003) Nanodissection and high-resolution imaging of the Rhodopseudomonas viridis photosynthetic core complex in native membranes by AFM. Proc Natl Acad Sci USA 100: 1690–1693PubMedGoogle Scholar
  221. Scheuring S, Sturgis JN, Prima V, Bernadac A, Levy D and Rigaud JL (2004) Watching the photosynthetic apparatus in native membranes. Proc Natl Acad Sci USA 101: 11293–11297PubMedGoogle Scholar
  222. Schimper AFW (1883) Uber die Entwicklung der Chloro-phyllkorner und Farbkorper. Bot Zeitung 41: 105–114, 121–131, 137–146, 153–162Google Scholar
  223. Schimper AFW (1885) Untersuchungen über die Chloro-phyllkorner und die Ihnen Homologen Gebilde. Jahrbucher fur Wissenschaftliche Botanik 16: 1–247Google Scholar
  224. Schnepf E (1980) Types of plastids: their development and interconversions. In: Reinert J (ed) Chloroplasts. SpringerVerlag, Berlin, pp. 1–28Google Scholar
  225. Segui-Simarro JM, Austin JR, White EA and Staehelin LA (2004) Electron tomographic analysis of somatic cell plate formation in meristematic cells of Arabidopsis preserved by high-pressure freezing. Plant Cell 16: 836–856PubMedGoogle Scholar
  226. 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: 251–262PubMedGoogle Scholar
  227. Shimoni E, Rav-Hon O, Ohad I, Brumfeld V and Reich Z (2005) Three-dimensional organization of higher-plant chloroplast thylakoid membranes revealed by electron tomography. Plant Cell 17: 2580–2586PubMedGoogle Scholar
  228. Simidjiev I, Stoylova S, Amenitsch H, Javorfi T, Mustardy L, Laggner P, Holzenburg A and Garab G (2000) Self-assembly of large, ordered lamellae from non-bilayer lipids and integral membrane proteins in vitro. Proc Natl Acad Sci USA 97: 1473–1476PubMedGoogle Scholar
  229. Simpson CL and Stern DB (2002) The treasure trove of algal chloroplast genomes. Surprises in architecture and gene content, and their functional implications. Plant Physiol 129: 957–966Google Scholar
  230. Sjostran FS (1974) Search for circuitry of directional selectivity and neural adaptation through 3-dimensional analysis of outer plexiform layer of rabbit retina. J Ultrastruct Res 49: 60–156Google Scholar
  231. Snyders S and Kohorn BD (1999) TAKs, thylakoid membrane protein kinases associated with energy transduction. J Biol Chem 274: 9137–9140PubMedGoogle Scholar
  232. Snyders S and Kohorn BD (2001) Disruption of thylakoid-associated kinase 1 leads to alteration of light harvesting in Arabidopsis. J Biol Chem 276: 32169–32176PubMedGoogle Scholar
  233. Sprey B (1973) Licbtinduzierte Entwiclkung von Etioplas-ten zu Chloroplasten: Induktion und Regulation der Membranbildung. Berlin Kernforsch Fülich Nr. 1019 BOGoogle Scholar
  234. Staehelin LA (1976) Reversible particle movements associated with unstacking and restacking of chloroplast membranes in vitro. J Cell Biol 71: 136–158PubMedGoogle Scholar
  235. Staehelin LA (1986) Chloroplast structure and supramo-lecular organization of photosynthetic membranes. In Staehelin LA and Arntzen CJ (eds) Photosynthesis III. Springer-Verlag, Berlin, pp. 1–84Google Scholar
  236. Staehelin LA (2003) Chloroplast structure: from chlorophyll granules to supra-molecular architecture of thylakoid membranes. Photosynth Res 76: 185–196PubMedGoogle Scholar
  237. Stanier G (1988) Fine structure of cyanobacteria. Methods Enzymol 167: 157–172Google Scholar
  238. Stanier RY and Cohen-Bazire G (1977) Phototrophic prokaryotes: the cyanobacteria. Annu Rev Microbiol 31: 225–274PubMedGoogle Scholar
  239. Steinbrecht RA and Müller M (1987) Cryotechniques. In: Steinbrecht RA and Zierolds K (eds) Biological Electron Microscopy. Springer-Verlag, Berlin, pp. 149–172Google Scholar
  240. Steinmann E and Sjostrand FS (1955) The ultrastructure of chloroplasts. Exp Cell Res 8: 15–23PubMedGoogle Scholar
  241. Stillinger FH and Rahman A (1974) Molecular-dynamics study of liquid water under high compression. J Chem Phys 61: 4973–4980Google Scholar
  242. Stoffler D, Feja B, Fahrenkrog B, Walz J, Typke D and Aebi U (2003) Cryo-electron tomography provides novel insights into nuclear pore architecture: implications for nucleocytoplasmic transport. J Mol Biol 328: 119–130PubMedGoogle Scholar
  243. tolz JF (2007) Bacterial Intracellular Membranes. Wiley, New YorkGoogle Scholar
  244. Studer D, Hennecke H and Müller M. (1992) High-pressure freezing of soybean nodules leads to an improved preservation of ultrastructure. Planta 188: 155–163Google Scholar
  245. Stys D (1995) Stacking and separation of photosystem I and photosystem II in plant thylakoid membranes: a physico-chemical view. Physiol Plant 95: 651–657Google Scholar
  246. Subramaniam S, Bartesaghi A, Liu J, Bennett AE and Sougrat R (2007) Electron tomography of viruses. Curr Opin Struc Biol 17: 596–602Google Scholar
  247. Swingley WD, Blankenship RE and Raymond J (2008) Integrating markov clustering and molecular phylogenetics to reconstruct the cyanobacterial species tree from conserved protein families. Mol Biol Evol 25: 643–654PubMedGoogle Scholar
  248. Szczesny PJ, Walther P and Müller M (1996) Light damage in rod outer segments: the effects of fixation on ultrastructural alterations. Curr Eye Res 15: 807–814PubMedGoogle Scholar
  249. Telfer A, Hodges M and Barber J (1983) Analysis of chlorophyll fluorescence induction curves in the presence of 3-(3,4-dichlorophenyl)-1,1-dimethylurea as a function of magnesium concentration and NADPH-activated light-harvesting chlorophyll a/b-protein phosphorylation. Bio-chim Biophys Acta 724: 167–175Google Scholar
  250. Telfer A, Bottin H, Barber J and Mathis P (1984) The effect of magnesium and phosphorylation of light-harvesting chlorophyll a/b-protein on the yield of P700 photooxi-dation in pea chloroplasts. Biochim Biophys Acta 764: 324–330Google Scholar
  251. Ting CS, Hsieh C, Sundararaman S, Mannella C and Marko M (2007) Cryo-electron tomography reveals the comparative three-dimensional architecture of Prochlorococcus, a globally important marine cyanobacterium. J Bacteriol 189: 4485–4493PubMedGoogle Scholar
  252. Trissl HW and Wilhelm C (1993) Why do thylakoid membranes from higher plants form grana stacks. Trends Bio-chem Sci 18: 415–419Google Scholar
  253. Trissl HW, Breton J, Deprez J and Leibl W (1987) Primary electrogenic reactions of photosystem II as probed by the light-gradient method. Biochim Biophys Acta 893: 305–319Google Scholar
  254. van de Meene AML, Hohmann-Marriott MF, Vermaas WFJ and Roberson RW (2006) The three-dimensional structure of the cyanobacterium Synechocystis sp. PCC 6803. Arch Microbiol 184: 259–270PubMedGoogle Scholar
  255. van Donselaar E, Posthuma G, Zeuschner D, Humbel BM and Slot JW (2007) Immunogold labeling of cryosections from high-pressure frozen cells. Traffic 8: 471–485PubMedGoogle Scholar
  256. van Harreveld A and Crowell J (1964) Electron microscopy after rapid freezing on a metal surface and substitution fixation. Anat Rec 149: 381–386Google Scholar
  257. Voeltz GK and Prinz WA (2007) Sheets, ribbons and tubules — how organelles get their shape. Nat Rev Mol Cell Biol 8: 258–264PubMedGoogle Scholar
  258. von Mohl H (1837) Untersuchungen über anatomische Verhältnisse des Chlorophylls. University of Tübingen, GermanyGoogle Scholar
  259. von Wettstein D (1959) The effect of genetic factors on the submicroscopic structures of the chloroplast. J Ultrastruct Res 3: 234–240Google Scholar
  260. Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid membranes. Biochim Biophys Acta 1541: 91–101PubMedGoogle Scholar
  261. Wang Q, Sullivan RW, Kight A, Henry RL, Huang JR, Jones AM and Korth KL (2004) Deletion of the chloro-plast-localized Thylakoid Formation1 gene product in Arabidopsis leads to deficient thylakoid formation and variegated leaves. Plant Physiol 136: 3594–3604PubMedGoogle Scholar
  262. Webb DT (1982) Structure and ultrastructure of plastids in light-and dark-grown Zamia floridana DC. seedling roots in vitro. New Phytol 91: 721–725Google Scholar
  263. Wehrmeyer W (1964) Zur Klärung der strukturellen Variabilität der Chloroplastengrana des Spinats in Profil und Aufsicht. Planta 62: 272–293Google Scholar
  264. Weier TE, Stocking CR, Thomson WW and Drever HJ (1963) The grana as structural units in chloroplasts of mesophyll of Nicotiana rustica and Phaseolus vulgaris. J Ultrastruct Res 8: 122–143Google Scholar
  265. Westphal S, Soll J and Vothknecht UC (2001) A vesicle transport system inside chloroplasts. FEBS Lett 506: 257–261PubMedGoogle Scholar
  266. Westphal S, Soll J and Vothknecht UC (2003) Evolution of chloroplast vesicle transport. Plant Cell Physiol 44: 217–222PubMedGoogle Scholar
  267. Whitton BA, Carr NG and Craig IW (1971) A comparison of the fine structure and nucleic acid biochemistry of chloro-plasts and blue-green algae. Protoplasma 72: 325–357PubMedGoogle Scholar
  268. Wildon DC and Mercer FV (1963) The ultrastructure of the vegetative cell of the blue-green algae. Aust J Biol Sci 16: 585–596Google Scholar
  269. Wolfe GR, Cunningham FX, Durnford D, Green BR and Gantt E (1994) Evidence for a common origin of chlo-roplasts with light-harvesting complexes of different pigmentation. Nature 367: 566–568Google Scholar
  270. Wollman FA (2001) State transitions reveal the dynamics and flexibility of the photosynthetic apparatus. EMBO J 20: 3623–3630PubMedGoogle Scholar
  271. Xiong J, Fischer WM, Inoue K, Nakahara M and Bauer CE (2000) Molecular evidence for the early evolution of photosynthesis. Science 289: 1724–1730PubMedGoogle Scholar
  272. Zhao Q, Öfverstedt LG, Skoglund U and Isaksson LA (2004a) Morphological variation of individual Escherichia coli 30S ribosomal subunits in vitro and in situ, as revealed by cryo-electron tomography. Exp Cell Res 297: 495–507Google Scholar
  273. Zhao Q, Öfverstedt LG, Skoglund U and Isaksson LA (2004b) Morphological variation of individual Escherichia coli 50S ribosomal subunits in situ, as revealed by cryo-electron tomography. Exp Cell Res 300: 190–201Google Scholar
  274. Zito F, Finazzi G, Delosme R, Nitschke W, Picot D and Wollman FA (1999) The Qo site of cytochrome b 6 f complexes controls the activation of the LHCII kinase. EMBO J 18: 2961–2969PubMedGoogle Scholar

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© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  1. 1.Department of Biological ChemistryWeizmann Institute of ScienceRehovotIsrael
  2. 2.The Robert H. Smith Institute of Plant Sciences and Genetics in AgricultureThe Hebrew University of JerusalemRehovotIsrael
  3. 3.Electron Microscopy UnitWeizmann Institute of ScienceRehovotIsrael

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