Electron tomography of plant thylakoid membranes

Journal of Experimental Botany

Volumn 62, Issue 7, 2011, Pages 2393-2402

  Daum, Bertram ^a   Kühlbrandt, Werner ^a  

^a MAX PLANCK INSTITUTE OF BIOPHYSICS   (Germany)

Author keywords

cF1Fo ATP synthase; chloroplast; electron cryotomography; photosystem II; plastoglobules; thylakoid membrane; thylakoid ultrastructure

Indexed keywords

VEGETABLE PROTEIN;

ARTICLE; ELECTRON TOMOGRAPHY; METABOLISM; PLANT; THYLAKOID; ULTRASTRUCTURE;

ELECTRON MICROSCOPE TOMOGRAPHY; PLANT PROTEINS; PLANTS; THYLAKOIDS;

EID: 79955396906     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/err034     Document Type: Article

References (79)

1. Al-Amoudi A, Chang JJ, Leforestier A, McDowall A, Salamin LM, Norlen LPO, Richter K, Blanc NS, Studer D, Dubochet J. 2004. Cryo-electron microscopy of vitreous sections. EMBO Journal 23, 3583-3588. (Pubitemid 39336280)
2. Albertsson PA. 2001. A quantitative model of the domain structure of the photosynthetic membrane. Trends in Plant Science 6, 349-354.
3. Allen RD, Schroeder CC, Fok AK. 1989. An investigation of mitochondrial inner membranes by rapid-freeze deep-etch techniques. Journal of Cell Biology 108, 2233-2240. (Pubitemid 19168916)
4. Anderson JM. 1981. Consequences of spatial separation of photosystem-1 and photosystem-2 in thylakoid membranes of higherplant chloroplasts. FEBS Letters 124, 1-10.
5. Andersson B, Anderson JM. 1980. Lateral heterogeneity in the distribution of chlorophyll-protein complexes of the thylakoid membranes of spinach-chloroplasts. Biochimica et Biophysica Acta 593, 427-440.
6. Armond PA, Staehelin LA, Arntzen CJ. 1977. Spatial relationship of photosystem-I, photosystem-II, and light-harvesting complex in chloroplast membranes. Journal of Cell Biology 73, 400-418.
7. Arvidsson PO, Sundby C. 1999. A model for the topology of the chloroplast thylakoid membrane. Australian Journal of Plant Physiology 26, 687-694.
8. Austin JR, Frost E, Vidi PA, Kessler F, Staehelin LA. 2006. Plastoglobules are lipoprotein subcompartments of the chloroplast that are permanently coupled to thylakoid membranes and contain biosynthetic enzymes. The Plant Cell 18, 1693-1703. (Pubitemid 44025553)
9. Austin JR, Staehelin LA. 2011. Three-dimensional architecture of grana and stroma thylakoids of higher plants as determined by electron tomography. Plant Physiology (in press).
10. Barber J. 1980. An explanation for the relationship between saltinduced thylakoid stacking and the chlorophyll fluorescence changes associated with changes in spillover of energy from photosystem-II to photosystem-I. FEBS Letters 118, 1-10.
11. Barber J. 1982. Influence of surface-charges on thylakoid structure and function. Annual Review of Plant Physiology and Plant Molecular Biology 33, 261-295.
12. Bá rcena M, Koster A 2009. Electron tomography in life science. Seminars in Cell and Developmental Biology, 20, 920-930.
13. Baumeister W, Grimm R, Walz J. 1999. Electron tomography of molecules and cells. Trends in Cell Biology 9, 81-85. (Pubitemid 29151799)
14. Ben-Harush K, Maimon T, Patla I, Villa E, Medalia O. 2010. Visualizing cellular processes at the molecular level by cryo-electron tomography. Journal of Cell Science 123, 7-12.
15. Boekema EJ, van Breemen JFL, van Roon H, Dekker JP. 2000. Arrangement of photosystem II supercomplexes in crystalline macrodomains within the thylakoid membrane of green plant chloroplasts. Journal of Molecular Biology 301, 1123-1133.
16. Brangeon J, Mustá rdy L. 1979. The ontogenetic assembly of intrachloroplastic lamellae viewed in 3-dimension. Biologie Cellulaire 36, 71-80.
17. Brumfeld V, Charuvi D, Nevo R, Chuartzman S, Tsabari O, Ohad I, Shimoni E, Reich Z. 2008. A note on three-dimensional models of higher-plant thylakoid networks. The Plant Cell 20, 2546-2549. (Pubitemid 352844573)
18. Caffarri S, Kouril R, Kereiche S, Boekema EJ, Croce R. 2009. Functional architecture of higher plant photosystem II supercomplexes. The EMBO Journal 28, 3052-3063.
19. Chow WS. 1984. The extent to which the spatial separation between photosystems-I and photosystems-II associated with granal formation limits noncyclic electron flow in isolated lettuce chloroplasts. Archives of Biochemistry and Biophysics 232, 162-171.
20. Chow WS, Kim EH, Horton P, Anderson JM. 2005. Granal stacking of thylakoid membranes in higher plant chloroplasts: the physicochemical forces at work and the functional consequences that ensue. Photochemical and Photobiological Sciences 4, 1081-1090. (Pubitemid 41811373)
21. Chow WS, Telfer A, Chapman DJ, Barber J. 1981. State 1-State 2 transition in leaves and its association with ATP-induced chlorophyll fluorescence quenching. Biochimica et Biophysica Acta 638, 60-68.
22. Couoh-Cardel SJ, Uribe-Carvajal S, Wilkens S, Garcia-Trejo JJ. 2010. Structure of dimeric F1F0-ATP synthase. Journal of Biological Chemistry 285, 36447-36455.
23. Daum B, Nicastro D, Austin JR, McIntosh JR, Kühlbrandt W. 2010. Arrangement of photosystem II and ATP synthase in chloroplast membranes of spinach and pea. The Plant Cell 22, 1299-1312.
24. Dekker JP, Boekema EJ. 2005. Supramolecular organization of thylakoid membrane proteins in green plants. Biochimica et Biophysica Acta 1706, 12-39. (Pubitemid 40044704)
25. Deruere J, Romer S, Dharlingue A, Backhaus RA, Kuntz M, Camara B. 1994. Fibril assembly and carotenoid overaccumulation in chromoplasts-a model for supramolecular lipoprotein structures. The Plant Cell 6, 119-133.
26. Dubochet J, Adrian M, Chang JJ, Homo JC, Lepault J, Mcdowall AW, Schultz P. 1988. Cryo-electron microscopy of vitrified specimens. Quarterly Reviews of Biophysics 21, 129-228.
27. Dudkina NV, Heinemeyer J, Keegstra W, Boekema EJ, Braun HP. 2005. Structure of dimeric ATP synthase from mitochondria: an angular association of monomers induces the strong curvature of the inner membrane. FEBS Letters 579, 5769-5772. (Pubitemid 41455662)
28. Dudkina NV, Kouril R, Bultema JB, Boekema EJ. 2010a. Imaging of organelles by electron microscopy reveals protein-protein interactions in mitochondria and chloroplasts. FEBS Letters 584, 2510-2515.
29. Dudkina NV, Oostergetel GT, Lewejohann D, Braun HP, Boekema EJ. 2010b. Row-like organization of ATP synthase in intact mitochondria determined by cryo-electron tomography. Biochimica et Biophysica Acta 1797, 272-277.
30. Falk H, Sitte P. 1963. Zellfeinbau Bei Plasmolyse.1. Der Feinbau Der Elodea-Blattzellen. Protoplasma 57, 290-303.
31. Frank J. 2006. Electron tomography: methods for three-dimensional visualization of structures in the cell. Berlin: Springer.
32. Ghosh S, Hudak KA, Dumbroff EB, Thompson JE. 1994. Release of photosynthetic protein catabolites by blebbing from thylakoids. Plant Physiology 106, 1547-1553. (Pubitemid 24986584)
33. Hansmann P, Sitte P. 1982. Composition and molecular structure of chromoplast globules of Viola tricolor. Plant Cell Reports 1, 111-114.
34. Heslop Harrison J. 1963. Structure and morphogenesis of lamellar systems in grana-containing chloroplasts. 1. Membrane structure and lamellar architecture. Planta 60, 243-260.
35. Horton P, Black MT. 1980. Activation of adenosine 5'-triphosphateinduced quenching of chlorophyll fluorescence by reduced plastoquinone-the basis of state-I-state-II transitions in chloroplasts. FEBS Letters 119, 141-144.
36. Kaup MT, Froese CD, Thompson JE. 2002. A role for diacylglycerol acyltransferase during leaf senescence. Plant Physiology 129, 1616-1626. (Pubitemid 34923225)
37. Kessler F, Schnell D, Blobel G. 1999. Identification of proteins associated with plastoglobules isolated from pea (Pisum sativum L.) chloroplasts. Planta 208, 107-113.
38. Kirchhoff H, Haase W, Wegner S, Danielsson R, Ackermann R, Albertsson PA. 2007. Low-light-induced formation of semicrystalline photosystem II arrays in higher plant chloroplast. Biochemistry 46, 11169-11176. (Pubitemid 47505211)
39. Kouril R, Oostergetel GT, Boekema EJ. 2011. Fine structure of granal thylakoid membrane organization using cryo electron tomography. Biochimica et Biophysica Acta in press.
40. Kreuz K, Dehesh K, Apel K. 1986. The light-dependent accumulation of the P700 chlorophyll alpha-protein of the photosystem-I reaction center in barley-evidence for translational control. European Journal of Biochemistry 159, 459-467.
41. Leis A, Rockel B, Andrees L, Baumeister W. 2009. Visualizing cells at the nanoscale. Trends in Biochemical Sciences 34, 60-70.
42. Lichtenthaler HK. 1968. Plastoglobuli and fine structure of plastids. Endeavour 27, 144-149.
43. Lichtenthaler HK, Tevini M. 1970. Distribution of pigments, plastid quinones and plastoglobuli in different particle fractions obtained from sonicated spinach chloroplasts. Zeitschrift für Pflanzenphysiologie 62, 33-50.
44. Machold O, Meister A, Sagromsky H, Hoyerhansen G, Wettstein DV. 1977. Composition of photosynthetic membranes of wild-type barley and chlorophyll b-less mutants. Photosynthetica 11, 200-206.
45. Menke W. 1960. Das Allgemeine Bauprinzip des Lamellarsystems der Chloroplasten. Experientia 16, 537-538.
46. Menke W. 1962. Structure and chemistry of plastids. Annual Review of Plant Physiology and Plant Molecular Biology 13, 27-44.
47. Miller KR, Staehelin LA. 1976. Analysis of thylakoid outer surfacecoupling factor is limited to unstacked membrane regions. Journal of Cell Biology 68, 30-47.
48. Mustá rdy L, Buttle K, Steinbach G, Garab G 2008. The threedimensional network of the thylakoid membranes in plants: quasihelical model of the granum-stroma assembly. The Plant Cell, 20, 2552-2557 (Pubitemid 352844575)
49. Mustá rdy L, Garab G, 2003, Granum revisited. A three-dimensional model-where things fall into place. Trends in Plant Science, 8, 117-122. (Pubitemid 36726467)
50. Mustá rdy LA, Janossy AGS, 1979. Evidence of helical thylakoid arrangement by scanning electron-microscopy. Plant Science Letters, 16, 281-284.
51. Nelson N, Ben-Shem A. 2004. The complex architecture of oxygenic photosynthesis. Nature Reviews Molecular Cell Biology 5, 971-982. (Pubitemid 39611534)
52. Nevo R, Chuartzman SG, Tsabari O, Reich Z. 2009. Architecture of thylakoid membrane networks. In: Wada H, Murata N, eds. Lipids in photosynthesis: essential and regulatory functions. Berlin: Springer, 295-328.
53. Nield J, Barber J. 2006. Refinement of the structural model for the photosystem II supercomplex of higher plants. Biochimica et Biophysica Acta 1757, 353-361. (Pubitemid 43993853)
54. Norlen L, Oktem O, Skoglund U. 2009. Molecular cryo-electron tomography of vitreous tissue sections: current challenges. Journal of Microscopy-Oxford 235, 293-307.
55. Paolillo DJ. 1970. The three-dimensional arrangement of intergranal lamellae in chloroplasts. Journal of Cell Science 6, 243-355.
56. Paumard P, Vaillier J, Coulary B, Schaeffer J, Soubannier V, Mueller DM, Brethes D, di Rago JP, Velours J. 2002. The ATP synthase is involved in generating mitochondrial cristae morphology. EMBO Journal 21, 221-230. (Pubitemid 34137284)
57. Pierson J, Sani M, Tomova C, Godsave S, Peters PJ. 2009. Toward visualization of nanomachines in their native cellular environment. Histochemistry and Cell Biology 132, 253-262.
58. PozuetaRomero J, Rafia F, Houlne G, Cheniclet C, Carde JP, Schantz ML, Schantz R. 1997. A ubiquitous plant housekeeping gene, PAP, encodes a major protein component of bell pepper chromoplasts. Plant Physiology 115, 1185-1194. (Pubitemid 28378778)
59. Schermelleh L, Heintzmann R, Leonhardt H. 2010. A guide to super-resolution fluorescence microscopy. Journal of Cell Biology 190, 165-175.
60. Shimoni E, Rav-Hon O, Ohad I, Brumfeld V, Reich Z. 2005. Three-dimensional organization of higher-plant chloroplast thylakoid membranes revealed by electron tomography. The Plant Cell 17, 2580-2586.
61. Staehelin LA. 1975. Chloroplast membrane structure-intramembranous particles of different sizes make contact in stacked membrane regions. Biochimica et Biophysica Acta 408, 1-11.
62. Staehelin LA. 1986. Chloroplast structure and supramolecular organization of photosynthetic membranes. In: Staehelin LA, Arntzen CJ, eds. Photosynthesis III. Photosynthetic membranes and light harvesting systems. Wallingford, UK: CABI Publishing, 1-84.
63. Staehelin LA. 2003. Chloroplast structure: from chlorophyll granules to supra-molecular architecture of thylakoid membranes. Photosynthesis Research 76, 185-196. (Pubitemid 37060525)
64. Standfuss J, Terwisscha van Scheltinga AC, Lamborghini M, Kühlbrandt W. 2005. Mechanisms of photoprotection and nonphotochemical quenching in pea light-harvesting complex at 2.5 A° resolution. EMBO Journal 24, 919-928. (Pubitemid 40470141)
65. Steinmüller D, Tevini M. 1985. Composition and function of plastoglobuli. 1. Isolation and purification from chloroplasts and chromoplasts. Planta 163, 201-207.
66. Strauss M, Hofhaus G, Schröder RR, Kühlbrandt W. 2008. Dimer ribbons of ATP synthase shape the inner mitochondrial membrane. EMBO Journal 27, 1154-1160. (Pubitemid 351508145)
67. Tevini M, Herm K, Leonhardt HD. 1977. Lipids and function of etiochloroplasts after UV, blue and red light-illumination. Biochemical Society Transactions 5, 95-98. (Pubitemid 8058475)
68. Tevini M, Steinmüller D. 1985. Composition and function of plastoglobuli. 2. Lipid-composition of leaves and plastoglobuli during beech leaf senescence. Planta 163, 91-96.
69. Tocheva E, Li Z, Jensen G. 2010. Electron cryotomography. Cold Spring Harbor Perspectives in Biology 2, a003442.
70. Trissl HW, Wilhelm C. 1993. Why do thylakoid membranes from higher-plants form grana stacks. Trends in Biochemical Sciences 18, 415-419. (Pubitemid 23316620)
71. van Roon H, van Breemen JFL, de Weerd FL, Dekker JP, Boekema EJ. 2000. Solubilization of green plant thylakoid membranes with n-dodecyl-alpha, d-maltoside. Implications for the structural organization of the photosystem II, photosystem I, ATP synthase and cytochrome b(6)f complexes. Photosynthesis Research 64, 155-166. (Pubitemid 32180229)
72. Vidi PA, Kanwischer M, Baginsky S, Austin JR, Csucs G, Dormann P, Kessler F, Brehelin C. 2006. Tocopherol cyclase (VTE1) localization and vitamin E accumulation in chloroplast plastoglobule lipoprotein particles. Journal of Biological Chemistry 281, 11225-11234. (Pubitemid 43855548)
73. Wehrmeyer W. 1964a. Über Membranbildungsprozesse im Chloroplasten. 2. Zur Entstehung der Grana durch Membranüberschiebung. Planta 63, 13-30.
74. Wehrmeyer W. 1964b. Zur Klá rung der Strukturellen Variabilitat der Chloroplastengrana des Spinats in Profil und Aufsicht. Planta 62, 272-293.
75. Weier TE, Drever H, Thomson WW, Stocking CR. 1963. The grana as structural units in chloroplasts of mesophyll of Nicotiana rustica and Phaseolus vulgaris. Journal of Ultrastructure Research 8, 122-143.
76. Wollenberger L, Stefansson H, Yu SG, Albertsson PA. 1994. Isolation and characterization of vesicles originating from the chloroplast grana margins. Biochimica et Biophysica Acta 1184, 93-102. (Pubitemid 24048863)
77. Yao K, Paliyath G, Humphrey RW, Hallett FR, Thompson JE. 1991a. Identification and characterization of nonsedimentable lipid protein microvesicles. Proceedings of the National Academy of Sciences, USA 88, 2269-2273. (Pubitemid 21916397)
78. Yao KN, Paliyath G, Thompson JE. 1991b. Nonsedimentable microvesicles from senescing bean cotyledons contain gel phaseforming phospholipid degradation products. Plant Physiology 97, 502-508. (Pubitemid 21914248)
79. Ytterberg AJ, Peltier JB, van Wijk KJ. 2006. Protein profiling of plastoglobules in chloroplasts and chromoplasts. A surprising site for differential accumulation of metabolic enzymes. Plant Physiology 140, 984-997. (Pubitemid 43956251)