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Architecture of Thylakoid Membrane Networks

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Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 30))

Summary

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.

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Abbreviations

CF:

Chemical fixation

Chl:

Chlorophyll

CEMOVIS:

Cryo-electron microscopy of vitreous sections

EMT:

Electron microscope tomography

EM:

Electron microscopy

FS:

Freeze substitution

HPF:

High pressure freezing

LHC:

Light-harvesting protein complexes

PS I:

Photosystem I

PS II:

Photosystem II

PBS:

Phycobilisomes

PQ:

Plastoquinone

UVB:

Ultraviolet radiation B (280–315 nm)

UVC:

Ultraviolet radiation C (100–280 nm)

References

  • Adir N (2005) Elucidation of the molecular structures of components of the phycobilisome: reconstructing a giant. Photosynth Res 85: 15–32

    PubMed  CAS  Google Scholar 

  • 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: 26–33

    CAS  Google Scholar 

  • 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: 3583–3588

    PubMed  CAS  Google Scholar 

  • 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: 109–121

    PubMed  CAS  Google Scholar 

  • Albertsson P (2001) A quantitative model of the domain structure of the photosynthetic membrane. Trends Plant Sci 6: 349–358

    PubMed  CAS  Google Scholar 

  • 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: 517–526

    Google Scholar 

  • 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. 915–918

    Google Scholar 

  • Allen JF (1992a) How does protein phosphorylation regulate photosynthesis? Trends Biochem Sci 17: 12–17

    CAS  Google Scholar 

  • Allen JF (1992b) Protein-phosphorylation in regulation of photosynthesis. Biochim Biophys Acta 1098: 275–335

    CAS  Google Scholar 

  • Allen JF and Forsberg J (2001) Molecular recognition in thylakoid structure and function. Trends Plant Sci 6: 317–326

    PubMed  CAS  Google Scholar 

  • 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: 25–29

    CAS  Google Scholar 

  • Allen MM (1968) Photosynthetic membrane system in Ana-cystis nidulans. J Bacteriol 96: 836–841

    PubMed  CAS  Google Scholar 

  • Anderson JM (1981) Consequences of spatial separation of photosystem-1 and photosystem-2 in thylakoid membranes of higher-plant chloroplasts. FEBS Lett 124: 1–10

    CAS  Google Scholar 

  • Anderson JM (1989) The grana margins of plant thylakoid membranes. Physiol Plant 76: 243–248

    CAS  Google Scholar 

  • Anderson JM (1999) Insights into the consequences of grana stacking of thylakoid membranes in vascular plants: a personal perspective. Aust J Plant Physiol 26: 625–639

    CAS  Google Scholar 

  • 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: 315–326

    CAS  Google Scholar 

  • 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: 363–376

    CAS  Google Scholar 

  • Anderson JM, Chow WS and Goodchild DJ (1988) Thy-lakoid membrane organization in sunshade acclimation. Aust J Plant Physiol 15: 11–26

    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 

  • Aro EM and Ohad I (2003) Redox regulation of thylakoid protein phosphorylation. Antioxid Redox Sign 5: 55–67

    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 

  • Atilgan E and Sun SX (2007) Shape transitions in lipid membranes and protein mediated vesicle fusion and fission. J Chem Phys 126: 095102–10

    PubMed  Google Scholar 

  • 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: 1693–1703

    PubMed  CAS  Google Scholar 

  • 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: 1058–1062

    PubMed  CAS  Google Scholar 

  • 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: 1–10

    CAS  Google Scholar 

  • Barber J (1982) Influence of surface-charges on thylakoid structure and function. Annu Rev Plant Physiol 33: 261–295

    CAS  Google Scholar 

  • Baumeister W (2002) Electron tomography: towards visualizing the molecular organization of the cytoplasm. Curr Opin Struc Biol 12: 679–684

    CAS  Google Scholar 

  • 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: 611–615

    PubMed  CAS  Google Scholar 

  • Bellafiore S, Bameche F, Peltier G and Rochaix JD (2005) State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 433: 892–895

    PubMed  CAS  Google Scholar 

  • Bennett J (1977) Phosphorylation of chloroplast membrane polypeptides. Nature 269: 344–346

    CAS  Google Scholar 

  • Bennett J (1979a) Chloroplast phosphoproteins — phosphor-ylation of polypeptides of the light-harvesting chlorophyll protein complex. Eur J Biochem 99: 133–137

    CAS  Google Scholar 

  • Bennett J (1979b) Chloroplast phosphoproteins. The protein kinase of thylakoid membranes is light-dependent. FEBS Lett 103: 342–344

    CAS  Google Scholar 

  • Bennett J (1980) Chloroplast phosphoproteins — evidence for a thylakoid-bound phosphoprotein phosphatase. Eur J Biochem 104: 85–89

    PubMed  CAS  Google Scholar 

  • Bennett J (1991) Protein-phosphorylation in green plant chloroplasts. Annu Rev Plant Physiol 42: 281–311

    CAS  Google Scholar 

  • Berkaloff C, Duval JC, Hauswirth N and Rousseau B (1983) Freeze-fracture study of thylakoids of Fucus serratus. J Phycol 19: 96–100

    Google Scholar 

  • 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. 115–135

    Google Scholar 

  • Blumwald E and Tel-Or E (1982) Structural aspects of the adaptation of Nostoc muscorum to salt. Arch Microbiol 132: 163–167

    CAS  Google Scholar 

  • 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: 14245–14250

    PubMed  Google Scholar 

  • Bonaventura C and Myers J (1969) Fluorescence and oxygen evolution from Chlorella pyrenoidosa. Biochim Bio-phys Acta 189: 366–383

    CAS  Google Scholar 

  • Bouchet-Marquis C, Starkuviene V and Grabenbauer M (2008) Golgi apparatus studied in vitreous sections. J Microsc-Oxford 230: 308–316

    CAS  Google Scholar 

  • Bouck GB (1965) Fine structure and organelle associations in brown algae. J Cell Biol 26: 523–537

    PubMed  CAS  Google Scholar 

  • Brangeon J (1974) Structural modifications in lamellar system of isolated Zea mays chloroplasts under different ionic conditions. J Microsc-Oxford 21: 75–84

    Google Scholar 

  • Brangeon J and Mustárdy L (1979) Ontogenetic assembly of intra-chloroplastic lamellae viewed in 3-dimension. Biol Cell 36: 71–80

    Google Scholar 

  • 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: 1–8

    CAS  Google Scholar 

  • Brody M and Vatter AE (1959) Observations on cellular structures of Porphyridium cruentum. J Biophys Biochem Cytol 5: 289–294

    PubMed  CAS  Google Scholar 

  • Carde JP, Joyard J and Douce R (1982) Electron-microscopic studies of envelope membranes from spinach plastids. Biol Cell 44: 315–324

    Google Scholar 

  • Cavalier-Smith T (2000) Membrane heredity and early chlo-roplast evolution. Trends Plant Sci 5: 174–182

    PubMed  CAS  Google Scholar 

  • 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: 340–343

    Google Scholar 

  • 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. 83–86

    Google Scholar 

  • Chow WS (1999) Grana formation: entropy-assisted local order in chloroplasts? Aust J Plant Physiol 26: 641–647

    CAS  Google Scholar 

  • 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: 69–77

    CAS  Google Scholar 

  • 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: 1081–1090

    PubMed  CAS  Google Scholar 

  • 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: 1029–1039

    PubMed  CAS  Google Scholar 

  • 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: 157–168

    Google Scholar 

  • Consoli E, Croce R, Dunlap DD and Finzi L (2005) Diffusion of light-harvesting complex II in the thylakoid membranes. EMBO Rep 6: 782–786

    PubMed  CAS  Google Scholar 

  • Crawley JC (1964) Cytoplasmic fine structure in Acetabu-laria. Exp Cell Res 35: 507–514

    PubMed  CAS  Google Scholar 

  • 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: e420

    PubMed  Google Scholar 

  • 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: 428–438

    PubMed  CAS  Google Scholar 

  • Das G (1975) Changes in chloroplast structure during autospore formation in Scenedesmus obtusiusculus. Protoplasma 84: 175–180

    Google Scholar 

  • Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid membrane proteins in green plants. Biochim Biophys Acta 1706: 12–39

    PubMed  CAS  Google Scholar 

  • Des Marais DJ (2000) Evolution — When did photosynthesis emerge on earth? Science 289: 1703–1705

    Google Scholar 

  • Doutreligne SJ (1935) Note sur la structure des chloroplastes. Proc Kon Acad Wetensch (Amsterdam) 38: 886–896

    Google Scholar 

  • 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: 11915–11922

    PubMed  CAS  Google Scholar 

  • Dubochet J and Blanc NS (2001) The cell in absence of aggregation artifacts. Micron 32: 91–99

    PubMed  CAS  Google Scholar 

  • Dubochet J and McDowall AW (1981) Vitrification of pure water for electron microscopy. J Microsc-Oxford 124: Rp3–Rp4

    Google Scholar 

  • 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: 385–406

    PubMed  CAS  Google Scholar 

  • 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: 59–68

    PubMed  CAS  Google Scholar 

  • Edwards MR and Gantt E (1971) Phycobilisomes of the thermophilic blue-green alga Synechococcus lividus. J Cell Biol 50: 896–900

    PubMed  CAS  Google Scholar 

  • Edwards MR, Berns DS, Ghiorse WC and Holt SC (1968) Ultrastructure of thermophilic blue-green alga Synechoc-occus lividus Copeland. J Phycol 4: 283–298

    Google Scholar 

  • Evans LV (1966) Distribution of pyrenoids among some brown algae. J Cell Sci 1: 449–454

    PubMed  CAS  Google Scholar 

  • Falk RH and Sitte P (1963) Zellfeinbau bei Plasmolyse. I. Der Feinbau der Elodea-Blattzellen. Protoplasma 57: 290–303

    CAS  Google Scholar 

  • Falkowski PG (2006) Evolution — tracing oxygen's imprint on earth's metabolic evolution. Science 311: 1724–1725

    PubMed  CAS  Google Scholar 

  • Falkowski PG, Katz ME, Knoll AH, Quigg A, Raven JA, Schofield O and Taylor FJ (2004) The evolution of modern eukaryotic phytoplankton. Science 305: 354–360

    PubMed  CAS  Google Scholar 

  • 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: 4729–4734

    PubMed  Google Scholar 

  • Frey TG and Mannella CA (2000) The internal structure of mitochondria. Trends Biochem Sci 25: 319–324

    PubMed  CAS  Google Scholar 

  • Gantt E and Conti SF (1965) Ultrastructure of Porphyridium cruentum. J Cell Biol 26: 365–381

    PubMed  CAS  Google Scholar 

  • Gantt E and Conti SF (1966) Granules associated with chlo-roplast lamellae of Porphyridium cruentum. J Cell Biol 29: 423–434

    PubMed  CAS  Google Scholar 

  • Gantt E and Conti SF (1969) Ultrastructure of blue-green algae. J Bacteriol 97: 1486–1493

    PubMed  CAS  Google Scholar 

  • 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: 6759–6764

    PubMed  CAS  Google Scholar 

  • 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: 273–281

    CAS  Google Scholar 

  • Gibbs SP (1970) Comparative ultrastructure of algal chloro-plast. Ann NY Acad Sci 175: 454–473

    Google Scholar 

  • 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: 352–356

    PubMed  CAS  Google Scholar 

  • Goodale GL (1889) Protoplasm and its history. Science 14: 352–355

    Google Scholar 

  • Goodchild DJ, Highkin HR and Boardman NK (1966) The fine structure of chloroplasts in a barley mutant lacking chlorophyll b. Exp Cell Res 43: 684–688

    PubMed  CAS  Google Scholar 

  • 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. 102–107

    Google Scholar 

  • Goodenough UW and Levine RP (1969) Chloroplast ultrastructure in mutant strains of Chlamydomonas rein-hardi lacking components of photosynthetic apparatus. Plant Physiol 44: 990–993

    PubMed  CAS  Google Scholar 

  • Granick S and Porter KR (1947) The structure of the spinach chloroplast as interpreted with the electron microscope. Am J Bot 34: 545–550

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Grebvy C, Axelsson L and Sundqvist C (1989) Light-independent plastid differentiation in the brown alga Laminaria saccharina (Phaeophyceae). Phycologia 28: 375–384

    Google Scholar 

  • Grossman AR, Schaefer MR, Chiang GG and Collier JL (1993) The phycobilisome, a light-harvesting complex responsive to environmental conditions. Microbiol Rev 57: 725–749

    PubMed  CAS  Google Scholar 

  • Guglielmi G, Cohen-Bazire G and Bryant DA (1981) The structure of Gloeobacter violaceus and its phycobili-somes. Arch Microbiol 129: 181–189

    CAS  Google Scholar 

  • 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: 301–305

    PubMed  CAS  Google Scholar 

  • Hall DH (1995) Electron microscopy and three-dimensional image reconstruction. Methods Cell Biol 48: 395–436

    PubMed  CAS  Google Scholar 

  • Han HM, Zuber B and Dubochet J (2008) Compression and crevasses in vitreous sections under different cutting conditions. J Microsc-Oxford 230: 167–171

    Google Scholar 

  • Heitz E (1936) Untersuchungen über den Bau der Plastiden I: die gerichteten Chlorophyllscheiben der Chloroplasten. Planta 26: 134–163

    Google Scholar 

  • Heslop-Harrison J (1963) Structure and morphogenesis of lamellar systems in grana-containing chloroplasts. Planta 60: 243–260

    Google Scholar 

  • Hess MW (2007) Cryopreparation methodology for plant cell biology. Method Cell Biol 79: 57–100

    CAS  Google Scholar 

  • 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: 605–614

    PubMed  CAS  Google Scholar 

  • 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: 1119–1122

    PubMed  CAS  Google Scholar 

  • Hoober JK, Boyd CO and Paavola LG (1991) Origin of thy-lakoid membranes in Chlamydomonas reinhardtii y-1 at 38°C. Plant Physiol 96: 1321–1328

    PubMed  CAS  Google Scholar 

  • Hoog JL and Antony C (2007) Whole-cell investigation of microtubule cytoskeleton architecture by electron tomography. Methods Cell Biol 79: 145–167

    PubMed  CAS  Google Scholar 

  • Horton P (1999) Are grana necessary for regulation of light harvesting? Aust J Plant Physiol 26: 659–669

    CAS  Google Scholar 

  • 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: 214–218

    CAS  Google Scholar 

  • Horton P and Ruban A (2005) Molecular design of the photosystem II light-harvesting antenna: photosynthesis and photoprotection. J Exp Bot 56: 365–373

    PubMed  CAS  Google Scholar 

  • 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: 4201–4206

    PubMed  CAS  Google Scholar 

  • Hsieh CE, Marko M, Frank J and Mannella CA (2002) Electron tomographic analysis of frozen-hydrated tissue sections. J Struct Biol 138: 63–73

    PubMed  Google Scholar 

  • 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: 1–13

    PubMed  CAS  Google Scholar 

  • 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. 175–183

    Google Scholar 

  • Izawa S and Good NE (1966) Effect of salts and electron transport on conformation of isolated chloroplasts. II. Electron microscopy. Plant Physiol 41: 544–552

    CAS  Google Scholar 

  • Jensen GJ and Briegel A (2007) How electron cryotomogra-phy is opening a new window onto prokaryotic ultrastructure. Curr Opin Struc Biol 17: 260–267

    CAS  Google Scholar 

  • Joliot P and Joliot A (2002) Cyclic electron transfer in plant leaf. Proc Natl Acad Sci USA 99: 10209–10214

    PubMed  CAS  Google Scholar 

  • Joliot P and Joliot A (2005) Quantification of cyclic and linear flows in plants. Proc Natl Acad Sci USA 102: 4913–4918

    PubMed  CAS  Google Scholar 

  • Jonas J (1982) Nuclear magnetic resonance at high pressure. Science 216: 1179–1184

    PubMed  CAS  Google Scholar 

  • 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: 6146–6153

    PubMed  CAS  Google Scholar 

  • Kanervo E, Suorsa M and Aro EM (2005) Functional flexibility and acclimation of the thylakoid membrane. Photo-chem Photobiol Sci 4: 1072–1080

    CAS  Google Scholar 

  • Kausche GA and Ruska H (1940) Zur Frage der Chloroplas-tenstruktur. Naturwissenschaften 28: 303–304

    CAS  Google Scholar 

  • 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: 181–201

    CAS  Google Scholar 

  • Kenrick P and Crane PR (1997) The origin and early evolution of plants on land. Nature 389: 33–39

    CAS  Google Scholar 

  • Kim EH, Chow WS, Horton P and Anderson JM (2005) Entropy-assisted stacking of thylakoid membranes. Bio-chim Biophys Acta 1708: 187–195

    CAS  Google Scholar 

  • 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: 1571–1578

    PubMed  CAS  Google Scholar 

  • 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. 258–271

    Google Scholar 

  • Komárek J and Cepák V (1998) Cytomorphological characters supporting the taxonomic validity of Cyanothece (Cyanoprokaryota). Plant Syst Evol 210: 25–39

    Google Scholar 

  • 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: 459–468

    PubMed  CAS  Google Scholar 

  • 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: 393–400

    PubMed  CAS  Google Scholar 

  • 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: 349–357

    PubMed  CAS  Google Scholar 

  • 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: 4238–4242

    PubMed  CAS  Google Scholar 

  • Kunkel DD (1982) Thylakoid centers: structures associated with the cyanobacterial photosynthetic membrane system. Arch Microbiol 133: 97–99

    Google Scholar 

  • 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: 38–42

    PubMed  Google Scholar 

  • Kutik J (1998) The development of chloroplast structure during leaf ontogeny. Photosynthetica 35: 481–505

    CAS  Google Scholar 

  • 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: 527–541

    PubMed  CAS  Google Scholar 

  • 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: 77–88

    CAS  Google Scholar 

  • Lembi CA and Lang NJ (1965) Electron microscopy of cart-eria and Chlamydomonas. Am J Bot 52: 464–477

    Google Scholar 

  • Lewin RA (2002) Prochlorophyta — a matter of class distinctions. Photosynth Res 73: 59–61

    PubMed  CAS  Google Scholar 

  • 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: 619–632

    PubMed  CAS  Google Scholar 

  • 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. 271–287

    Google Scholar 

  • 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: 129–138

    Google Scholar 

  • 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: 99–106

    Google Scholar 

  • Lopez-Juez E and Pyke KA (2005) Plastids unleashed: their development and their integration in plant development. Int J Dev Biol 49: 557–577

    PubMed  CAS  Google Scholar 

  • Lučić V, Förster F and Baumeister W (2005) Structural studies by electron tomography: from cells to molecules. Annu Rev Biochem 74: 833–865

    PubMed  Google Scholar 

  • Lüdemann HD (1996) Recent developments in high pressure high resolution NMR in liquids. Pol J Chem 70: 387–408

    Google Scholar 

  • 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: 613–615

    PubMed  CAS  Google Scholar 

  • Macagno ER, Levinthal C and Sobel I (1979) 3-Dimensional computer reconstruction of neurons and neuronal assemblies. Annu Rev Biophys Bio 8: 323–351

    CAS  Google Scholar 

  • 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: 541–547

    PubMed  CAS  Google Scholar 

  • Mannella CA (2006) The relevance of mitochondrial membrane topology to mitochondrial function. Biochim Bio-phys Acta 1762: 140–147

    CAS  Google Scholar 

  • 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: 93–100

    PubMed  CAS  Google Scholar 

  • 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: 215–217

    PubMed  CAS  Google Scholar 

  • 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: 2399–2406

    PubMed  CAS  Google Scholar 

  • Mastronarde DN, Ladinsky MS and McIntosh JR (1997) Super-thin serial sectioning for high-resolution 3-D reconstruction of cellular structures. Microsc Microanal 3: 221–222

    Google Scholar 

  • 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. 49–64

    Google Scholar 

  • McCourt RM (1995) Green algal phylogeny. Trends Ecol Evol 10: 159–163

    PubMed  CAS  Google Scholar 

  • McDonald K (2007) Cryopreparation methods for electron microscopy of selected model systems. Method Cell Biol 79: 23–56

    CAS  Google Scholar 

  • 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: 40–56

    PubMed  CAS  Google Scholar 

  • McEwen BF and Marko M (1999) Three-dimensional transmission electron microscopy and its application to mitosis research. Methods Cell Biol 61: 81–111

    PubMed  CAS  Google Scholar 

  • McEwen BF and Marko M (2001) The emergence of electron tomography as an important tool for investigating cellular ultrastructure. J Histochem Cytochem 49: 553–563

    PubMed  CAS  Google Scholar 

  • 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: 1209–1213

    PubMed  CAS  Google Scholar 

  • Meisch HU, Becker LJM and Schwab D (1980) Ultrastructural changes in Chlorella fusca during iron-deficiency and vanadium treatment. Protoplasma 103: 273–280

    CAS  Google Scholar 

  • 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: 659–670

    PubMed  CAS  Google Scholar 

  • Menke W (1940a) Die Lamellarstruktur der Chloroplasten im ultravioletten Licht. Naturwissenesch 28: 158–159

    CAS  Google Scholar 

  • Menke W (1940b) Untersuchungen über den Feinbau des Protoplasmas mit dem Universal-Elektronenmikroskop. Protoplasma 35: 115–130

    CAS  Google Scholar 

  • Menke W (1960) Das allgemeine Bauprinzip des Lamel-larsystems der Chloroplasten. Experientia 16: 537–538

    Google Scholar 

  • Menke W (1962) Über die Chloroplasten von Anthoceros punctatus. Zeit Naturforsch 16: 334–336

    Google Scholar 

  • Menke W (1966) The structure of the chloroplasts. In Goodwin TE (ed) Biochemistry of Chloroplasts, Vol 1. Academic Press, New York, pp. 3–18

    Google Scholar 

  • Merchant S and Sawaya MR (2005) The light reactions: A guide to recent acquisitions for the picture gallery. Plant Cell 17: 648–663

    PubMed  CAS  Google Scholar 

  • Meyer A (1883) Das Chlorophyllkorn in chemischer, morphologischer und biologischer Beziehung, Arthur Felix Leipzig

    Google Scholar 

  • Michel M, Hillmann T and Müller M (1991) Cryosection-ing of plant-material frozen at high-pressure. J Microsc-Oxford 163: 3–18

    Google Scholar 

  • 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: 577–586

    PubMed  Google Scholar 

  • 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: 1225–1238

    PubMed  CAS  Google Scholar 

  • Misteli T and Warren G (1995) Mitotic disassembly of the Golgi apparatus in vivo. J Cell Sci 108: 2715–2727

    PubMed  CAS  Google Scholar 

  • 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: 2277–2291

    PubMed  CAS  Google Scholar 

  • Monaghan P, Perusinghe N and Müller M (1998) High-pressure freezing for immunocytochemistry. J Microsc-Oxford 192: 248–258

    CAS  Google Scholar 

  • 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. 175–191

    Google Scholar 

  • 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 

  • 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: 1558–1564

    Google Scholar 

  • Mühlethaler K and Frey-Wyssling A (1959) Entwicklung und Struktur der Proplastiden. J Biophys Biochem Cytol 6: 507–512

    Google Scholar 

  • 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: 100–117

    PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • 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. 289–309

    Google Scholar 

  • Mullineaux CW and Emlyn-Jones D (2005) State transitions: an example of acclimation to low-light stress. J Exp Bot 56: 389–393

    PubMed  CAS  Google Scholar 

  • Murakami S and Packer L (1971) Role of cations in organization of chloroplast membranes. Arch Biochem Biophys 146: 337–347

    PubMed  CAS  Google Scholar 

  • Murata N (1969) Control of excitation transfer in photosynthesis. I. Light-induced change of chlorophyll a fluorescence in Porphyridium cruentum. Biochim Biophys Acta 172: 242–251

    PubMed  CAS  Google Scholar 

  • 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: 81–90

    CAS  Google Scholar 

  • Murphy GE, Leadbetter JR and Jensen GJ (2006) In situ structure of the complete Treponema primitia flagellar motor. Nature 442: 1062–1064

    PubMed  CAS  Google Scholar 

  • Mustárdy L (1996) Development of thylakoid membrane stacking. In: Ort DR and Yocum CF (eds) Oxygenic Photosynthesis: The Light Reactions. Kluwer, Dordrecht, pp. 59–68

    Google Scholar 

  • Mustárdy L and Garab G (2003) Granum revisited. A three-dimensional model — where things fall into place. Trends Plant Sci 8: 117–122

    PubMed  Google Scholar 

  • Mustárdy LA and Jánossy AGS (1979) Evidence of helical thylakoid arrangement by scanning electron-microscopy. Plant Sci Lett 16: 281–284

    Google Scholar 

  • 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: 2153–2162

    PubMed  CAS  Google Scholar 

  • 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: 137–145

    PubMed  CAS  Google Scholar 

  • Nelson N and Ben-Shem A (2004) The complex architecture of oxygenic photosynthesis. Nat Rev Mol Cell Bio 5: 971–982

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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: 1467–1473

    PubMed  CAS  Google Scholar 

  • Nicastro D, Frangakis AS, Typke D and Baumeister W (2000) Cryo-electron tomography of neurospora mitochondria. J Struct Biol 129: 48–56

    PubMed  CAS  Google Scholar 

  • 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: 15889–15894

    PubMed  CAS  Google Scholar 

  • Nierzwicki-Bauer SA, Balkwill DL and Stevens SE (1983) 3-Dimensional ultrastructure of a unicellular cyanobacte-rium. J Cell Biol 97: 713–722

    PubMed  CAS  Google Scholar 

  • 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: 298–313

    PubMed  Google Scholar 

  • 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: 521–551

    CAS  Google Scholar 

  • 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: 553–584

    CAS  Google Scholar 

  • 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: 2017–2031

    PubMed  Google Scholar 

  • 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: 125–143

    PubMed  Google Scholar 

  • 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: 1591–1606

    PubMed  CAS  Google Scholar 

  • Palmer JD (2000) Molecular evolution — A single birth of all plastids? Nature 405: 32–33

    PubMed  CAS  Google Scholar 

  • Paolillo DJ Jr (1970) The three-dimensional arrangement of intergranal lamellae in chloroplasts. J Cell Sci 6: 243–255

    PubMed  Google Scholar 

  • Paolillo DJ Jr and Falk RH (1966) The ultrastructure of grana in mesophyll plastids of Zea mays. Am J Bot 53: 173–180

    Google Scholar 

  • Paolillo DJ, Mackay NC and Graffius JR (1969) Structure of grana in flowering plants. Am J Bot 56: 344–347

    Google Scholar 

  • Penczek P, Marko M, Buttle K and Frank J (1995) Double-tilt electron tomography. Ultramicroscopy 60: 393–410

    PubMed  CAS  Google Scholar 

  • Pendland JC and Aldrich HC (1973) Ultrastructural organization of chloroplast thylakoids of green-alga Oocystis marssonii. J Cell Biol 57: 306–314

    PubMed  CAS  Google Scholar 

  • Penttila A, McDowell EM and Trump BF (1975) Effects of fixation and post-fixation treatments on volume of injured cells. J Histochem Cytochem 23: 251–270

    PubMed  CAS  Google Scholar 

  • 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: 469–480

    PubMed  CAS  Google Scholar 

  • 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: 368–376

    Google Scholar 

  • 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: 1030–1038

    CAS  Google Scholar 

  • 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. 1–12

    Google Scholar 

  • Porta D, Rippka R and Hernandez-Marine M (2000) Unusual ultrastructural features in three strains of Cyanothece (cyanobacteria). Arch Microbiol 173: 154–163

    PubMed  CAS  Google Scholar 

  • 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: 895–909

    PubMed  CAS  Google Scholar 

  • Reddy KJ, Haskell JB, Sherman DM and Sherman LA (1993) Unicellular, aerobic nitrogen-fixing cyanobacteria of the genus Cyanothece. J Bacteriol 175: 1284–1292

    PubMed  CAS  Google Scholar 

  • Rippka R, Waterbury J and Cohen-Bazire G (1974) Cyano-bacterium which lacks thylakoids. Arch Microbiol 100: 419–436

    CAS  Google Scholar 

  • Robertson D and Laetsch WM (1974) Structure and function of developing barley plastids. Plant Physiol 54: 148–159

    PubMed  CAS  Google Scholar 

  • 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: 247–252

    PubMed  Google Scholar 

  • 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: 2–12

    PubMed  CAS  Google Scholar 

  • 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: 110–114

    PubMed  CAS  Google Scholar 

  • Scheuring S and Sturgis JN (2005) Chromatic adaptation of photosynthetic membranes. Science 309: 484–487

    PubMed  CAS  Google Scholar 

  • 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: 1690–1693

    PubMed  CAS  Google Scholar 

  • 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: 11293–11297

    PubMed  CAS  Google Scholar 

  • Schimper AFW (1883) Uber die Entwicklung der Chloro-phyllkorner und Farbkorper. Bot Zeitung 41: 105–114, 121–131, 137–146, 153–162

    Google Scholar 

  • Schimper AFW (1885) Untersuchungen über die Chloro-phyllkorner und die Ihnen Homologen Gebilde. Jahrbucher fur Wissenschaftliche Botanik 16: 1–247

    Google Scholar 

  • Schnepf E (1980) Types of plastids: their development and interconversions. In: Reinert J (ed) Chloroplasts. SpringerVerlag, Berlin, pp. 1–28

    Google Scholar 

  • 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: 836–856

    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 

  • 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: 2580–2586

    PubMed  CAS  Google Scholar 

  • 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: 1473–1476

    PubMed  CAS  Google Scholar 

  • 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: 957–966

    CAS  Google Scholar 

  • 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: 60–156

    Google Scholar 

  • Snyders S and Kohorn BD (1999) TAKs, thylakoid membrane protein kinases associated with energy transduction. J Biol Chem 274: 9137–9140

    PubMed  CAS  Google Scholar 

  • Snyders S and Kohorn BD (2001) Disruption of thylakoid-associated kinase 1 leads to alteration of light harvesting in Arabidopsis. J Biol Chem 276: 32169–32176

    PubMed  CAS  Google Scholar 

  • Sprey B (1973) Licbtinduzierte Entwiclkung von Etioplas-ten zu Chloroplasten: Induktion und Regulation der Membranbildung. Berlin Kernforsch Fülich Nr. 1019 BO

    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 (1986) Chloroplast structure and supramo-lecular organization of photosynthetic membranes. In Staehelin LA and Arntzen CJ (eds) Photosynthesis III. Springer-Verlag, Berlin, pp. 1–84

    Google Scholar 

  • Staehelin LA (2003) Chloroplast structure: from chlorophyll granules to supra-molecular architecture of thylakoid membranes. Photosynth Res 76: 185–196

    PubMed  CAS  Google Scholar 

  • Stanier G (1988) Fine structure of cyanobacteria. Methods Enzymol 167: 157–172

    Google Scholar 

  • Stanier RY and Cohen-Bazire G (1977) Phototrophic prokaryotes: the cyanobacteria. Annu Rev Microbiol 31: 225–274

    PubMed  CAS  Google Scholar 

  • Steinbrecht RA and Müller M (1987) Cryotechniques. In: Steinbrecht RA and Zierolds K (eds) Biological Electron Microscopy. Springer-Verlag, Berlin, pp. 149–172

    Google Scholar 

  • Steinmann E and Sjostrand FS (1955) The ultrastructure of chloroplasts. Exp Cell Res 8: 15–23

    PubMed  CAS  Google Scholar 

  • Stillinger FH and Rahman A (1974) Molecular-dynamics study of liquid water under high compression. J Chem Phys 61: 4973–4980

    CAS  Google Scholar 

  • 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: 119–130

    PubMed  CAS  Google Scholar 

  • tolz JF (2007) Bacterial Intracellular Membranes. Wiley, New York

    Google Scholar 

  • Studer D, Hennecke H and Müller M. (1992) High-pressure freezing of soybean nodules leads to an improved preservation of ultrastructure. Planta 188: 155–163

    Google Scholar 

  • Stys D (1995) Stacking and separation of photosystem I and photosystem II in plant thylakoid membranes: a physico-chemical view. Physiol Plant 95: 651–657

    CAS  Google Scholar 

  • Subramaniam S, Bartesaghi A, Liu J, Bennett AE and Sougrat R (2007) Electron tomography of viruses. Curr Opin Struc Biol 17: 596–602

    CAS  Google Scholar 

  • 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: 643–654

    PubMed  CAS  Google Scholar 

  • 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: 807–814

    PubMed  CAS  Google Scholar 

  • 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: 167–175

    CAS  Google Scholar 

  • 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: 324–330

    CAS  Google Scholar 

  • 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: 4485–4493

    PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • 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: 305–319

    CAS  Google Scholar 

  • 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: 259–270

    PubMed  CAS  Google Scholar 

  • van Donselaar E, Posthuma G, Zeuschner D, Humbel BM and Slot JW (2007) Immunogold labeling of cryosections from high-pressure frozen cells. Traffic 8: 471–485

    PubMed  Google Scholar 

  • van Harreveld A and Crowell J (1964) Electron microscopy after rapid freezing on a metal surface and substitution fixation. Anat Rec 149: 381–386

    Google Scholar 

  • Voeltz GK and Prinz WA (2007) Sheets, ribbons and tubules — how organelles get their shape. Nat Rev Mol Cell Biol 8: 258–264

    PubMed  CAS  Google Scholar 

  • von Mohl H (1837) Untersuchungen über anatomische Verhältnisse des Chlorophylls. University of Tübingen, Germany

    Google Scholar 

  • von Wettstein D (1959) The effect of genetic factors on the submicroscopic structures of the chloroplast. J Ultrastruct Res 3: 234–240

    Google Scholar 

  • Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid membranes. Biochim Biophys Acta 1541: 91–101

    PubMed  CAS  Google Scholar 

  • 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: 3594–3604

    PubMed  CAS  Google Scholar 

  • Webb DT (1982) Structure and ultrastructure of plastids in light-and dark-grown Zamia floridana DC. seedling roots in vitro. New Phytol 91: 721–725

    Google Scholar 

  • Wehrmeyer W (1964) Zur Klärung der strukturellen Variabilität der Chloroplastengrana des Spinats in Profil und Aufsicht. Planta 62: 272–293

    Google Scholar 

  • 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: 122–143

    Google Scholar 

  • Westphal S, Soll J and Vothknecht UC (2001) A vesicle transport system inside chloroplasts. FEBS Lett 506: 257–261

    PubMed  CAS  Google Scholar 

  • Westphal S, Soll J and Vothknecht UC (2003) Evolution of chloroplast vesicle transport. Plant Cell Physiol 44: 217–222

    PubMed  CAS  Google Scholar 

  • 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: 325–357

    PubMed  CAS  Google Scholar 

  • Wildon DC and Mercer FV (1963) The ultrastructure of the vegetative cell of the blue-green algae. Aust J Biol Sci 16: 585–596

    Google Scholar 

  • 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: 566–568

    CAS  Google Scholar 

  • Wollman FA (2001) State transitions reveal the dynamics and flexibility of the photosynthetic apparatus. EMBO J 20: 3623–3630

    PubMed  CAS  Google Scholar 

  • Xiong J, Fischer WM, Inoue K, Nakahara M and Bauer CE (2000) Molecular evidence for the early evolution of photosynthesis. Science 289: 1724–1730

    PubMed  CAS  Google Scholar 

  • 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: 495–507

    CAS  Google Scholar 

  • 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: 190–201

    CAS  Google Scholar 

  • 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: 2961–2969

    PubMed  CAS  Google Scholar 

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Acknowledgments

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).

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Correspondence to Reinat Nevo or Dana Charuvi .

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Nevo, R., Chuartzman, S.G., Tsabari, O., Reich, Z., Charuvi, D., Shimoni, E. (2009). Architecture of Thylakoid Membrane Networks. In: Wada, H., Murata, N. (eds) Lipids in Photosynthesis. Advances in Photosynthesis and Respiration, vol 30. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-2863-1_14

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