Structure, Composition, Functional Organization and Dynamic Properties of Thylakoid Membranes

  • L. Andrew Staehelin
  • Georg W. M. van der Staay
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 4)


Chloroplasts are semi-autonomous organelles comprised of two envelope membranes, an aqueous matrix known as stroma, and internal membranes called thylakoids. All of the light-harvesting and energy-transducing functions are located in the thylakoids, which form a physically continuous membrane system that encloses an aqueous compartment, the thylakoid lumen. With few exceptions thylakoids are differentiated into stacked grana and non-stacked stroma membrane regions. A model of the three-dimensional relationship between grana and stroma thylakoids is presented. The membrane continuum is formed by a lipid bilayer that contains unique types of lipids. The principal functions of thylakoids are the trapping of light energy and the transduction of this energy into the chemical energy forms, ATP and NADPH. During this process, water is oxidized and oxygen is released. These functions are performed by five large protein complexes: Photosystem I with bound antennae, Photosystem II with bound antennae, light-harvesting complex II, cytochrome b 6 f, and ATP synthase. The roles of these complexes in photosynthetic electron transport and ATP synthesis are discussed. The differentiation of thylakoids into grana and stroma membrane regions is a morphological reflection of an underlying non-random distribution of the five complexes between the two types of membrane domains. The most prominent effect of membrane stacking is the physical segregation of most Photosystem II to stacked grana membranes, and of most Photosystem I to unstacked stroma membranes. The evolutionary roots and the functional implications of this non-random organization of thylakoid membrane components are discussed in some detail. The final section of this chapter describes how thylakoid membranes adapt to long-term and short-term changes in the light-environment. Long-term light changes cause alterations in the ratios of the different types of protein complexes in turn to optimize the use of available light energy. In contrast, short-term light changes modulate the organization of membrane components and serve primarily to protect the photosystems and only secondarily to optimize the turnover of the electron transport chain.


Chl – chlorophyll Cyt – cytochrome DGDG – digalactosyldiacylglycerol EFs – exoplasmic fracture face of stacked membranes EFu – exoplasmic fracture faces of unstacked membranes LHC – light-harvesting complex MGDG – monogalactosyldiacylglycerol P680– special pair of chlorophylls in the reaction center of Photosystem II P700 – special pair of chlorophylls in the reaction center of Photosystem I PC – phosphatidylcholine PFs – protoplasmic fracture face of stacked membranes PFu – protoplasmic fracture face of unstacked membranes PG–phosphatidylglycerol PQ–plastoquinone PS I – Photosystem I PS II – Photosystem II RC – reaction center SQDG – sulfoquinovosyldiacylglycerol 


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  1. Albertsson PA, Andreasson E and Svensson P (1990) The domain organization of the plant thylakoid membrane. FEBS Lett 273: 36–40PubMedCrossRefGoogle Scholar
  2. Allen JF (1992) Protein phosphorylation in regulation of photosynthesis. Biochim Biophys Acta 1098: 275–335PubMedGoogle Scholar
  3. Allen KD, Duysen ME and Staehelin LA (1988) Biogenesis of thylakoid membranes is controlled by light intensity in the conditional chlorophyll b-deficient CD3 mutant of wheat. J Cell Biol 107: 907–919PubMedCrossRefGoogle Scholar
  4. Allred DR and Staehelin LA (1986) Spatial organization of the cytochrome b 6 f complex within chloroplast thylakoid membranes. Biochim Biophys Acta 849: 94–103PubMedGoogle Scholar
  5. Almog O, Shoham G and Nechushtai R (1992) Photosystem I: composition, organization and structure. In: Barber J (ed) The Photosystems: Structure, Function and Molecular Biology, pp 443–469. Elsevier, AmsterdamGoogle Scholar
  6. Anderson JM (1989) The grana margins of plant thylakoid membranes. Physiol Plant 76: 243–248Google Scholar
  7. Anderson JM (1992) Cytochrome-b 6 f complex–dynamic molecular organization, function and acclimation. Photosynth Res 34: 341–357CrossRefGoogle Scholar
  8. Anderson JM, Chow WS and Goodchild DJ (1988) Thylakoid membrane organisation in sun/shade acclimation. Austr J Plant Physiol 15: 11–26CrossRefGoogle Scholar
  9. Andreasson E, Svensson P, Weibull C and Albertsson P-A (1988) Separation and characterization of stroma and grana membranes-evidence for heterogeneity in antenna size of both Photosystem I and Photosystem II. Biochim Biophys Acta 936: 339–350Google Scholar
  10. Armond PA, Staehelin LA and Arntzen CJ (1977) Spatial relationship of Photosystem I, Photosystem II, and the light-harvesting complex in chloroplast membranes. J Cell Biol 73: 400–418PubMedCrossRefGoogle Scholar
  11. Aro EM, Virgin I and Andersson B (1993) Photoinhibition of photosystem 2–inactivation, protein damage and turnover. Biochim Biophys Acta 1143: 113–134PubMedGoogle Scholar
  12. Barbato R, Friso G, Rigoni F, Vecchia FD and Giacometti GM (1992) Structural changes and lateral redistribution of Photosystem-II during donor side photoinhibition of thylakoids. J Cell Biol 119: 325–335PubMedCrossRefGoogle Scholar
  13. Barber J and Andersson B (1992) Too much of a good thing: Light can be bad for photosynthesis. Trends Biochem Sci 17: 61–66PubMedCrossRefGoogle Scholar
  14. Bassi R, Pineau B, Dainese P and Marquardt J (1993) Carotenoid-binding proteins of Photosystem II. Eur J Biochem 212: 297–303PubMedCrossRefGoogle Scholar
  15. Bennett J (1991) Protein phosphorylation in green plant chloroplasts. Ann Rev Plant Physiol Plant Mol Biol 42: 281–311Google Scholar
  16. Björkman O and Ludlow MM (1972) Characterization of the light climate on the floor of a Queensland rainforest. Carnegie Inst Washington Yearbook 71: 85–94Google Scholar
  17. Boardman NK, Anderson JM and Goodchild DJ (1978) Chlorophyll-protein complexes and structure of mature and developing chloroplasts. Curr Top Bioenerg 8: 36–109Google Scholar
  18. Boekema EJ, Schmidt G, Grüber P and Berden JA (1988) Structure of the ATP synthase from chloroplasts and mitochondria. Z Naturforsch 43c: 219–225Google Scholar
  19. Boekema E, Wynn RM and Malkin R (1990) The structure of spinach Photosystem I studied by electron microscopy. Biochim Biophys Acta 1017: 49–56Google Scholar
  20. Boekema EJ, Boonstra AF, Dekker JP and Rögner M (1994) Electron microscopic structural analysis of Photosystem I, Photosystem II, and the cytochrome-b 6 f complex from green plants and cyanobacteria. J Bioenerg Biomemb 26: 17–29Google Scholar
  21. Boffey SA and Leech RM (1982) Chloroplast DNA levels and the control of chloroplast division in light-grown wheat leaves. Plant Physiol 69: 1387–1391PubMedGoogle Scholar
  22. Bryant DA (1992) Molecular biology of Photosystem I. In: Barber J (ed) The Photosystems: Structure, Function and Molecular Biology, pp 501–549. Elsevier, AmsterdamGoogle Scholar
  23. Butler WL (1977) Chlorophyll fluorescence: A probe for electron transfer and energy transfer. In: Trebst A and Avron M (eds) Photosynthesis I: Photosynthetic Electron Transfer and Photophosphorylation, pp 149–167. Springer-Verlag, BerlinGoogle Scholar
  24. Chapman RL and Staehelin LA (1986) Freeze-fracture (-etch) electron microscopy. In: Aldrich HC and Todd WJ (eds) Ultrastructure Techniques for Microorganisms, pp 213–240. Plenum Publishing, New YorkGoogle Scholar
  25. Dahlin C and Ryberg H (1986) Accumulation of phytoene in plastoglobuli of SAN-9789 (Norflurazon)-treated dark grown wheat. Physiol Plant 68: 39–45Google Scholar
  26. de Boer D and Weisbeek P (1993) Import and routing of chloroplast proteins. In: Sundquist C and Ryberg M (eds) Pigment-Protein Complexes in Plastids, pp 311–334. Academic Press, San DiegoGoogle Scholar
  27. Demmig-Adams B (1990) Carotenoids and photoprotection in plants: A role for the xanthophyll zeaxanthin. Biochim Biophys Acta 1020: 1–24Google Scholar
  28. Demmig-Adams B and Adams WW (1992) Photoprotection and other responses of plants to high light stress. Ann Rev Plant Physiol Plant Molec Biol 43: 599–626CrossRefGoogle Scholar
  29. Douce R and Joyard J (1979) Structure and function of the plastid envelope. Adv Bot Res 7: 1–116Google Scholar
  30. Dubacq JP and Trémolières A (1983) Occurrence and function of phosphatidylglycerol containing Δ3-trans-hexadecenoic acid in photosynthetic lamellae. Physiol Vég 21: 293–312Google Scholar
  31. Dunahay TG and Staehelin LA (1985) Isolation of Photosystem I complexes from octylglucoside/SDS solublized spinach thylakoids. Plant Physiol 78: 606–613PubMedGoogle Scholar
  32. Dunahay TG and Staehelin LA (1987) Immunolocalization of the Chl a/b light harvesting complex and CP29 under conditions favoring phosphorylation and dephosphorylation of thylakoid membranes (state 1-state 2 transition). In: Biggins J (ed) Progress in Photosynthesis Research, Vol. 2, pp 701–704. Martinus Nijhoff, DordrechtGoogle Scholar
  33. Erickson JM and Rochaix JD (1992) The molecular biology of Photosystem II. In: Barber J (ed) The Photosystems: Structure, Function and Molecular Biology, pp 101–177. Elsevier, AmsterdamGoogle Scholar
  34. Funk C, Schröder WP, Green BR, Renger G and Andersson B (1994) The intrinsic 22 kDa protein is a chlorophyll-binding subunit of Photosystem II. FEBS Lett 342: 261–266PubMedCrossRefGoogle Scholar
  35. Gal A, Hauska G, Herrmann R and Ohad I (1990) Interaction between light harvesting chlorophyll-a/b protein (LHCII) kinase and cytochrome b 6 f complex. In vitro control of kinase activity. J Biol Chem 265: 19742–19749PubMedGoogle Scholar
  36. Gilmore AM and Yamamoto HY (1993) Linear models relating xanthophylls and lumen activity to non-photochemical fluorescence quenching. Evidence that antheraxanthin explains zeaxanthin-independent quenching. Photosynth Res 35: 67–78CrossRefGoogle Scholar
  37. Gounaris K and Barber J (1983) Monogalactosydiacylglycerol: The most abundant polar lipids in nature. Trends Biochem Sci 8: 378–381CrossRefGoogle Scholar
  38. Graan T and Ort DR (1986) Quantitation of 2,5-dibromo-3-methyl-6-isopropyl-p-benzoquinone binding sites in chloroplast membranes: Evidence for a functional dimer of the cytochrome b 6 f complex. Arch Biochem Biophys 248: 445–451PubMedCrossRefGoogle Scholar
  39. Green BR, Shen DR, Aebersold R and Pichersky E (1992) Identification of the polypeptides of the major light-harvesting complex of Photosystem II (LHCII) with their genes in tomato. FEBS Lett 305: 18–22PubMedCrossRefGoogle Scholar
  40. Haehnel W, Ratajczak R and Robenek H (1989) Lateral distribution and diffusion of plastocyanin in chloroplast thylakoids. J Cell Biol 108: 1397–1405PubMedCrossRefGoogle Scholar
  41. Hennig J and Herrmann RG (1986) Chloroplast ATP synthase of spinach contains nine nonidentical subunit species, six of which are encoded by plastid chromosomes in two operons in a phylogenetically conserved arrangement. Mol Gen Genet 203: 117–128CrossRefGoogle Scholar
  42. Hope AB (1993) The chloroplast cytochrome bf complex–a critical focus on function. Biochim Biophys Acta 1143: 1–22PubMedGoogle Scholar
  43. Horton P and Ruban AV (1992) Regulation of Photosystem II. Photosynth Res 34: 375–385CrossRefGoogle Scholar
  44. Horton P. Ruban A V and Walters RG (1994) Regulation of light harvesting in green plants. Plant Physiol 106: 415–420PubMedGoogle Scholar
  45. Jagendorf AT and Michales A (1990) Rough thylakoids: translation on photosynthetic membranes. Plant Sci 71: 137–145CrossRefGoogle Scholar
  46. Jansson S (1994) The light-harvesting chlorophyll a/b-binding proteins. Biochim Biophys Acta 1184: 1–19PubMedGoogle Scholar
  47. Jansson S, Pichersky E, Bassi R, Green BR, Ikeuchi M, Melis A, Simpson DJ, Spangfort M, Staehelin LA and Thornber JP (1992) A nomenclature for the genes encoding the chlorophyll a/b-binding proteins of higher plants. Plant Mol Biol Reporter 10: 242–253Google Scholar
  48. Kim JH, Glick RE and Melis A (1993) Dynamics of photosystem stoichiometry adjustment by light quality in chloroplasts. Plant Physiol 102: 181–190PubMedGoogle Scholar
  49. Krupa Z, Huner NPA, Williams JP, Maissan E and James DR (1987) Development at cold-hardening temperatures: The structure and composition of purified rye light harvesting complex II. Plant Physiol 84: 19–24PubMedGoogle Scholar
  50. Kühlbrandt W, Wang DN and Fujiyoshi Y (1994) Atomic model of plant light-harvesting complex by electron crystallography. Nature 367: 614–621PubMedGoogle Scholar
  51. 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: 527–541PubMedCrossRefGoogle Scholar
  52. Lee W-J and Whitmarsh J (1989) Photosynthetic apparatus of pea thylakoid membranes: Response to growth light intensity. Plant Physiol 89: 932–940PubMedGoogle Scholar
  53. Lichtenthaler HK (1968) Plastoglobuli and the fine structure of plastids. Endeavour 27: 144–149Google Scholar
  54. Lichtenthaler HK and Schindler C (1992) Studies on the photoprotective function of zeaxanthin at high-light conditions. In: Murata M (ed) Research in Photosynthesis, Vol IV, pp 517–520. Kluwer Academic Publishers, DordrechtGoogle Scholar
  55. Lyon MK, Marr KM and Furcinitti PS (1993) Formation and characterization of two-dimensional crystals of Photosystem II. J Struct Biol 110: 133–140PubMedCrossRefGoogle Scholar
  56. Marquardt J and Bassi R (1993) Chlorophyll-proteins from maize seedlings grown under intermittent light conditions–their stoichiometry and pigment content. Planta 191: 265–273CrossRefGoogle Scholar
  57. Mattoo A and Edelman M (1987) Intramembrane translocation and posttranslational palmitoylation of the chloroplast 32-kDa herbicide-binding protein. Proc Natl Acad Sci USA 84: 1497–1501PubMedGoogle Scholar
  58. McCarty RE and Racker E (1966) Effect of a coupling factor and its antiserum on photophosphorylation and hydrogen ion transport. Brookhaven Symp Biol 19: 202–214PubMedGoogle Scholar
  59. 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: 40–56PubMedCrossRefGoogle Scholar
  60. Melis A (1991) Dynamics of photosynthetic membrane composition and function. Biochim Biophys Acta 1058: 87–106Google Scholar
  61. Miller KR and Staehelin LA (1976) Analysis of the thylakoid outer surface: Coupling factor is limited to unstacked membrane regions. J Cell Biol 68: 30–47PubMedCrossRefGoogle Scholar
  62. Mörschel E and Schatz GH (1987) Correlation of Photosystem II complexes with exoplasmatic freeze-fracture particles of thylakoids of the cyanobacterium Synechococcus sp. Planta 172: 145–154Google Scholar
  63. Mörschel E and Staehelin LA (1983) Reconstitution of cytochrome b 6 f and CF0-CF1 ATP synthetase complexes into phospholipid and galactolipid liposomes. J Cell Biol 97: 301–310PubMedGoogle Scholar
  64. Murphy DJ (1986) Structural properties and molecular organization of acyl lipids of photosynthetic membranes. In: Staehelin LA and Arntzen CJ (eds) Photosynthesis III: Photosynthetic Membranes and Light-Harvesting Systems, pp 713–726. Springer-Verlag, BerlinGoogle Scholar
  65. Murphy DJ and Woodrow IE (1983) Lateral heterogeneity in the distribution of thylakoid membrane lipid and protein components and its implication for the molecular organization of photosynthetic membranes. Biochim Biophys Acta 725: 104–112Google Scholar
  66. Nalin CM and Nelson N (1987) Structure and biogenesis of chloroplast coupling factor CF0/CF1-ATP synthase. Curr Topics Bioenerg 15: 273–294Google Scholar
  67. Nußberger S, Dörr K, Wang DN and Kühlbrandt W (1993) Lipid-Protein interactions in crystals of plant light-harvesting complex. J Mol Biol 234: 347–356PubMedGoogle Scholar
  68. Olive J and Vallon O (1991) Structural organization of the thylakoid membrane: Freeze-fracture and immunocytochemical analysis. J Electron Microscopy Technique 18: 360–374Google Scholar
  69. Ort DR and Whitmarsh J (1990) Inactive Photosystem II centers: A resolution of discrepancies in Photosystem II quantitation? Photosynth Res 23: 101–104CrossRefGoogle Scholar
  70. Paolillo D (1970) The three dimensional arrangement of integral lamellae in chloroplasts. J Cell Sci 6: 243–255PubMedGoogle Scholar
  71. Seibert M, DeWit M and Staehelin LA (1987) Structural localization of the O2-evolving apparatus to multimeric (tetrameric) particles on the lumenal surface of freeze-etched photosynthetic membranes. J Cell Biol 105: 2257–2265PubMedCrossRefGoogle Scholar
  72. Senge MO (1993) Recent advances in the biosynthesis and chemistry of the chlorophylls. Photochem Photobiol 57: 189–206Google Scholar
  73. Siegenthaler PA and Rawyler A (1986) Acyl lipids in thylakoid membranes: Distribution and involvement in photosynthetic functions. In: Staehelin LA and Arntzen CJ (eds) Photosynthesis III: Photosynthetic Membranes and Light-Harvesting Systems, pp 693–705. Springer Verlag, BerlinGoogle Scholar
  74. Simpson D (1979) Freeze-fracture studies on barley membranes III. Location of the light harvesting chlorophyll-protein. Carlsberg Res Commun 44: 305–336Google Scholar
  75. Simpson D (1982) Freeze-fracture studies on barley plastid membranes V. Viridis n34, a Photosystem I mutant. Carlsberg Res Commun 47: 215–225Google Scholar
  76. Simpson D (1986) Freeze-fracture studies of mutant barley chloroplast membranes. In: Staehelin LA and Arntzen CJ (eds) Photosynthesis III: Photosynthetic Membranes and Light-Harvesting Systems, pp 665–674. Springer Verlag, BerlinGoogle Scholar
  77. Simpson D and Robinson S (1984) Freeze-fracture ultrastructure of thylakoid membranes in chloroplasts from manganese-deficient plants. Plant Physiol 74: 735–741PubMedCrossRefGoogle Scholar
  78. Simpson DJ and von Wettstein D (1989) The structure and function of the thylakoid membrane. Carlsberg Res Comm 54: 55–65CrossRefGoogle Scholar
  79. Somerville C and Browse J (1991) Plant lipids: Metabolism, mutants, and membranes. Science 252: 80–87PubMedGoogle Scholar
  80. Sprague SG (1987) Structural and functional consequences of galactolipids on thylakoid membrane organization. J Bioenerg Biomembr 19: 691–703PubMedCrossRefGoogle Scholar
  81. Sprague SG, Camm EL, Green BR and Staehelin LA (1985) Reconstitution of light-harvesting complexes and Photosystem II cores into galactolipid and phospholipid liposomes. J Cell Biol 100: 552–557PubMedCrossRefGoogle Scholar
  82. Staehelin LA (1986) Chloroplast structure and supramolecular organization of photosynthetic membranes. In: Staehelin LA and Arntzen CJ (eds) Photosynthesis III: Photosynthetic Membranes and Light-Harvesting Systems, pp 1–84. Springer-Verlag, BerlinGoogle Scholar
  83. Staehelin LA and Arntzen CJ (1983) Regulation of chloroplast membrane function: Protein phosphorylation changes the spatial organization of membrane components. J Cell Biol 97: 1327–1337PubMedCrossRefGoogle Scholar
  84. Staehelin LA and DeWit M (1984) Correlation of structure and function of chloroplast membranes at the supramolecular level. J Cell Biochem 24: 261–269PubMedCrossRefGoogle Scholar
  85. Staehelin LA, Armond PA and Miller KR (1977) Chloroplast membrane organization at the supramolecular level and its functional implications. Brookhaven Symp Biol 28: 278–315Google Scholar
  86. Sundby C and Andersson B (1985) Temperature-induced reversible migration along the thylakoid membrane of Photosystem II regulates its association with LHC II. FEBS Lett 191: 24–28CrossRefGoogle Scholar
  87. Sundby C and Larsson C (1985) Transbilayer organization of the thylakoid membrane. Biochim Biophys Acta 813: 61–67Google Scholar
  88. Süss K-H, Arkona C, Manteuffel R and Adler K (1993) Calvin cycle multienzyme complexes are bound to chloroplast thylakoid membranes of higher plants in situ. Proc Natl Acad Sci USA 90: 5514–5518PubMedGoogle Scholar
  89. Terashima I and Inoue Y (1985) Palisade tissue chloroplasts and spongy tissue chloroplasts in spinach: Biochemical and ultrastructural differences. Plant Cell Physiol 26: 63–75Google Scholar
  90. Terashima I and Takenaka A (1986) Organization of photosynthetic system of dorsiventral leaves as adapted to the irradiation from the adaxial side. In: Marcells R, Clijsters H and van Pouke M (eds) Biological Control of Photosynthesis, pp 219–230. Martinus Nijhoff, DordrechtGoogle Scholar
  91. Thornber JP, Peter GF, Morishige DT, Gomez S, Anandan S, Welty BA, Lee A, Kerfeld C, Takeuchi T and Preiss S (1993) Light harvesting in Photosystem I and Photosystem II. Biochem Soc Trans 21: 15–18PubMedGoogle Scholar
  92. Trissl HW and Wilhelm C (1993) Why do thylakoid membranes from higher plants form grana stacks? Trends Biochem Sci 18: 415–419PubMedCrossRefGoogle Scholar
  93. Vallon O, Bulte L, Dainese P, Olive J, Bassi R and Wollman F-A (1991) Lateral redistribution of cytochrome b 6 f complexes along thylakoid membranes upon state transitions. Proc Natl Acad Sci USA 88: 8262–8266PubMedGoogle Scholar
  94. Vermaas W (1993) Molecular-biological approaches to analyze Photosystem II. Ann Rev Plant Physiol Plant Mol Biol 44: 457–481CrossRefGoogle Scholar
  95. Webb MS and Green BR (1991) Biochemical and biophysical properties of thylakoid acyl lipids. Biochim Biophys Acta 1060: 133–158Google Scholar
  96. Williams WP (1977) The two photosystems and their interaction. In: Barber J (ed) Primary Process of Photosynthesis, pp 99–144. Elsevier, AmsterdamGoogle Scholar
  97. Williams WP and Allen JF (1987) State 1-state 2 changes in higher plants and algae. Photosynth Res 13: 19–45CrossRefGoogle Scholar
  98. Wollenberger L, Stefansson H, Yu SG and Albertsson PA (1994) Isolation and characterization of vesicles originating from the chloroplast grana margins. Biochim Biophys Acta 1184: 93–102Google Scholar
  99. Wollman F-A and Lemaire C (1988) Studies on kinase-controlled state transitions in Photosystem II and b 6 f mutants from Chlamydomonas reinhardtii which lack quinone-binding protein. Biochim Biophys Acta 933: 85–94Google Scholar

Copyright information

© Kluwer Academic Publishers 1996

Authors and Affiliations

  • L. Andrew Staehelin
    • 1
  • Georg W. M. van der Staay
    • 1
  1. 1.Department of Molecular, Cellular and Developmental BiologyUniversity of Colorado at BoulderBoulderUSA

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