Skip to main content

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

  • Chapter
Oxygenic Photosynthesis: The Light Reactions

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 4))

Summary

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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 259.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 329.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 329.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Similar content being viewed by others

References

  • Albertsson PA, Andreasson E and Svensson P (1990) The domain organization of the plant thylakoid membrane. FEBS Lett 273: 36–40

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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: 907–919

    Article  PubMed  CAS  Google Scholar 

  • Allred DR and Staehelin LA (1986) Spatial organization of the cytochrome b 6 f complex within chloroplast thylakoid membranes. Biochim Biophys Acta 849: 94–103

    PubMed  CAS  Google Scholar 

  • 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, Amsterdam

    Google Scholar 

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

    CAS  Google Scholar 

  • Anderson JM (1992) Cytochrome-b 6 f complex–dynamic molecular organization, function and acclimation. Photosynth Res 34: 341–357

    Article  CAS  Google Scholar 

  • Anderson JM, Chow WS and Goodchild DJ (1988) Thylakoid membrane organisation in sun/shade acclimation. Austr J Plant Physiol 15: 11–26

    Article  Google Scholar 

  • 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: 339–350

    CAS  Google Scholar 

  • 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: 400–418

    Article  PubMed  CAS  Google Scholar 

  • Aro EM, Virgin I and Andersson B (1993) Photoinhibition of photosystem 2–inactivation, protein damage and turnover. Biochim Biophys Acta 1143: 113–134

    PubMed  CAS  Google Scholar 

  • 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: 325–335

    Article  PubMed  CAS  Google Scholar 

  • Barber J and Andersson B (1992) Too much of a good thing: Light can be bad for photosynthesis. Trends Biochem Sci 17: 61–66

    Article  PubMed  CAS  Google Scholar 

  • Bassi R, Pineau B, Dainese P and Marquardt J (1993) Carotenoid-binding proteins of Photosystem II. Eur J Biochem 212: 297–303

    Article  PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Björkman O and Ludlow MM (1972) Characterization of the light climate on the floor of a Queensland rainforest. Carnegie Inst Washington Yearbook 71: 85–94

    Google Scholar 

  • Boardman NK, Anderson JM and Goodchild DJ (1978) Chlorophyll-protein complexes and structure of mature and developing chloroplasts. Curr Top Bioenerg 8: 36–109

    Google Scholar 

  • Boekema EJ, Schmidt G, Grüber P and Berden JA (1988) Structure of the ATP synthase from chloroplasts and mitochondria. Z Naturforsch 43c: 219–225

    Google Scholar 

  • Boekema E, Wynn RM and Malkin R (1990) The structure of spinach Photosystem I studied by electron microscopy. Biochim Biophys Acta 1017: 49–56

    CAS  Google Scholar 

  • 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: 17–29

    CAS  Google Scholar 

  • Boffey SA and Leech RM (1982) Chloroplast DNA levels and the control of chloroplast division in light-grown wheat leaves. Plant Physiol 69: 1387–1391

    CAS  PubMed  Google Scholar 

  • Bryant DA (1992) Molecular biology of Photosystem I. In: Barber J (ed) The Photosystems: Structure, Function and Molecular Biology, pp 501–549. Elsevier, Amsterdam

    Google Scholar 

  • 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, Berlin

    Google Scholar 

  • 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 York

    Google Scholar 

  • Dahlin C and Ryberg H (1986) Accumulation of phytoene in plastoglobuli of SAN-9789 (Norflurazon)-treated dark grown wheat. Physiol Plant 68: 39–45

    CAS  Google Scholar 

  • 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 Diego

    Google Scholar 

  • Demmig-Adams B (1990) Carotenoids and photoprotection in plants: A role for the xanthophyll zeaxanthin. Biochim Biophys Acta 1020: 1–24

    CAS  Google Scholar 

  • 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: 599–626

    Article  CAS  Google Scholar 

  • Douce R and Joyard J (1979) Structure and function of the plastid envelope. Adv Bot Res 7: 1–116

    CAS  Google Scholar 

  • Dubacq JP and Trémolières A (1983) Occurrence and function of phosphatidylglycerol containing Δ3-trans-hexadecenoic acid in photosynthetic lamellae. Physiol Vég 21: 293–312

    CAS  Google Scholar 

  • Dunahay TG and Staehelin LA (1985) Isolation of Photosystem I complexes from octylglucoside/SDS solublized spinach thylakoids. Plant Physiol 78: 606–613

    CAS  PubMed  Google Scholar 

  • 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, Dordrecht

    Google Scholar 

  • 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, Amsterdam

    Google Scholar 

  • 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: 261–266

    Article  PubMed  CAS  Google Scholar 

  • 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: 19742–19749

    PubMed  CAS  Google Scholar 

  • 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: 67–78

    Article  CAS  Google Scholar 

  • Gounaris K and Barber J (1983) Monogalactosydiacylglycerol: The most abundant polar lipids in nature. Trends Biochem Sci 8: 378–381

    Article  CAS  Google Scholar 

  • 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: 445–451

    Article  PubMed  CAS  Google Scholar 

  • 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: 18–22

    Article  PubMed  CAS  Google Scholar 

  • Haehnel W, Ratajczak R and Robenek H (1989) Lateral distribution and diffusion of plastocyanin in chloroplast thylakoids. J Cell Biol 108: 1397–1405

    Article  PubMed  CAS  Google Scholar 

  • 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: 117–128

    Article  CAS  Google Scholar 

  • Hope AB (1993) The chloroplast cytochrome bf complex–a critical focus on function. Biochim Biophys Acta 1143: 1–22

    PubMed  CAS  Google Scholar 

  • Horton P and Ruban AV (1992) Regulation of Photosystem II. Photosynth Res 34: 375–385

    Article  CAS  Google Scholar 

  • Horton P. Ruban A V and Walters RG (1994) Regulation of light harvesting in green plants. Plant Physiol 106: 415–420

    PubMed  CAS  Google Scholar 

  • Jagendorf AT and Michales A (1990) Rough thylakoids: translation on photosynthetic membranes. Plant Sci 71: 137–145

    Article  CAS  Google Scholar 

  • Jansson S (1994) The light-harvesting chlorophyll a/b-binding proteins. Biochim Biophys Acta 1184: 1–19

    PubMed  CAS  Google Scholar 

  • 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: 242–253

    CAS  Google Scholar 

  • Kim JH, Glick RE and Melis A (1993) Dynamics of photosystem stoichiometry adjustment by light quality in chloroplasts. Plant Physiol 102: 181–190

    PubMed  CAS  Google Scholar 

  • 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: 19–24

    CAS  PubMed  Google Scholar 

  • Kühlbrandt W, Wang DN and Fujiyoshi Y (1994) Atomic model of plant light-harvesting complex by electron crystallography. Nature 367: 614–621

    PubMed  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

    Article  PubMed  CAS  Google Scholar 

  • Lee W-J and Whitmarsh J (1989) Photosynthetic apparatus of pea thylakoid membranes: Response to growth light intensity. Plant Physiol 89: 932–940

    CAS  PubMed  Google Scholar 

  • Lichtenthaler HK (1968) Plastoglobuli and the fine structure of plastids. Endeavour 27: 144–149

    CAS  Google Scholar 

  • 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, Dordrecht

    Google Scholar 

  • Lyon MK, Marr KM and Furcinitti PS (1993) Formation and characterization of two-dimensional crystals of Photosystem II. J Struct Biol 110: 133–140

    Article  PubMed  CAS  Google Scholar 

  • Marquardt J and Bassi R (1993) Chlorophyll-proteins from maize seedlings grown under intermittent light conditions–their stoichiometry and pigment content. Planta 191: 265–273

    Article  CAS  Google Scholar 

  • 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: 1497–1501

    PubMed  CAS  Google Scholar 

  • McCarty RE and Racker E (1966) Effect of a coupling factor and its antiserum on photophosphorylation and hydrogen ion transport. Brookhaven Symp Biol 19: 202–214

    PubMed  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

    Article  PubMed  CAS  Google Scholar 

  • Melis A (1991) Dynamics of photosynthetic membrane composition and function. Biochim Biophys Acta 1058: 87–106

    CAS  Google Scholar 

  • Miller KR and Staehelin LA (1976) Analysis of the thylakoid outer surface: Coupling factor is limited to unstacked membrane regions. J Cell Biol 68: 30–47

    Article  PubMed  CAS  Google Scholar 

  • 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: 145–154

    Google Scholar 

  • 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: 301–310

    PubMed  Google Scholar 

  • 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, Berlin

    Google Scholar 

  • 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: 104–112

    CAS  Google Scholar 

  • Nalin CM and Nelson N (1987) Structure and biogenesis of chloroplast coupling factor CF0/CF1-ATP synthase. Curr Topics Bioenerg 15: 273–294

    CAS  Google Scholar 

  • Nußberger S, Dörr K, Wang DN and Kühlbrandt W (1993) Lipid-Protein interactions in crystals of plant light-harvesting complex. J Mol Biol 234: 347–356

    PubMed  Google Scholar 

  • Olive J and Vallon O (1991) Structural organization of the thylakoid membrane: Freeze-fracture and immunocytochemical analysis. J Electron Microscopy Technique 18: 360–374

    CAS  Google Scholar 

  • Ort DR and Whitmarsh J (1990) Inactive Photosystem II centers: A resolution of discrepancies in Photosystem II quantitation? Photosynth Res 23: 101–104

    Article  CAS  Google Scholar 

  • Paolillo D (1970) The three dimensional arrangement of integral lamellae in chloroplasts. J Cell Sci 6: 243–255

    PubMed  Google Scholar 

  • 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: 2257–2265

    Article  PubMed  CAS  Google Scholar 

  • Senge MO (1993) Recent advances in the biosynthesis and chemistry of the chlorophylls. Photochem Photobiol 57: 189–206

    CAS  Google Scholar 

  • 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, Berlin

    Google Scholar 

  • Simpson D (1979) Freeze-fracture studies on barley membranes III. Location of the light harvesting chlorophyll-protein. Carlsberg Res Commun 44: 305–336

    CAS  Google Scholar 

  • Simpson D (1982) Freeze-fracture studies on barley plastid membranes V. Viridis n34, a Photosystem I mutant. Carlsberg Res Commun 47: 215–225

    Google Scholar 

  • 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, Berlin

    Google Scholar 

  • Simpson D and Robinson S (1984) Freeze-fracture ultrastructure of thylakoid membranes in chloroplasts from manganese-deficient plants. Plant Physiol 74: 735–741

    Article  CAS  PubMed  Google Scholar 

  • Simpson DJ and von Wettstein D (1989) The structure and function of the thylakoid membrane. Carlsberg Res Comm 54: 55–65

    Article  CAS  Google Scholar 

  • Somerville C and Browse J (1991) Plant lipids: Metabolism, mutants, and membranes. Science 252: 80–87

    CAS  PubMed  Google Scholar 

  • Sprague SG (1987) Structural and functional consequences of galactolipids on thylakoid membrane organization. J Bioenerg Biomembr 19: 691–703

    Article  PubMed  CAS  Google Scholar 

  • 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: 552–557

    Article  PubMed  CAS  Google Scholar 

  • 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, Berlin

    Google Scholar 

  • Staehelin LA and Arntzen CJ (1983) Regulation of chloroplast membrane function: Protein phosphorylation changes the spatial organization of membrane components. J Cell Biol 97: 1327–1337

    Article  PubMed  CAS  Google Scholar 

  • Staehelin LA and DeWit M (1984) Correlation of structure and function of chloroplast membranes at the supramolecular level. J Cell Biochem 24: 261–269

    Article  PubMed  CAS  Google Scholar 

  • Staehelin LA, Armond PA and Miller KR (1977) Chloroplast membrane organization at the supramolecular level and its functional implications. Brookhaven Symp Biol 28: 278–315

    Google Scholar 

  • 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: 24–28

    Article  CAS  Google Scholar 

  • Sundby C and Larsson C (1985) Transbilayer organization of the thylakoid membrane. Biochim Biophys Acta 813: 61–67

    CAS  Google Scholar 

  • 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: 5514–5518

    PubMed  Google Scholar 

  • Terashima I and Inoue Y (1985) Palisade tissue chloroplasts and spongy tissue chloroplasts in spinach: Biochemical and ultrastructural differences. Plant Cell Physiol 26: 63–75

    CAS  Google Scholar 

  • 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, Dordrecht

    Google Scholar 

  • 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: 15–18

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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: 8262–8266

    PubMed  CAS  Google Scholar 

  • Vermaas W (1993) Molecular-biological approaches to analyze Photosystem II. Ann Rev Plant Physiol Plant Mol Biol 44: 457–481

    Article  CAS  Google Scholar 

  • Webb MS and Green BR (1991) Biochemical and biophysical properties of thylakoid acyl lipids. Biochim Biophys Acta 1060: 133–158

    CAS  Google Scholar 

  • Williams WP (1977) The two photosystems and their interaction. In: Barber J (ed) Primary Process of Photosynthesis, pp 99–144. Elsevier, Amsterdam

    Google Scholar 

  • Williams WP and Allen JF (1987) State 1-state 2 changes in higher plants and algae. Photosynth Res 13: 19–45

    Article  CAS  Google Scholar 

  • 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: 93–102

    CAS  Google Scholar 

  • 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: 85–94

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1996 Kluwer Academic Publishers

About this chapter

Cite this chapter

Staehelin, L.A., van der Staay, G.W.M. (1996). Structure, Composition, Functional Organization and Dynamic Properties of Thylakoid Membranes. In: Ort, D.R., Yocum, C.F., Heichel, I.F. (eds) Oxygenic Photosynthesis: The Light Reactions. Advances in Photosynthesis and Respiration, vol 4. Springer, Dordrecht. https://doi.org/10.1007/0-306-48127-8_2

Download citation

  • DOI: https://doi.org/10.1007/0-306-48127-8_2

  • Publisher Name: Springer, Dordrecht

  • Print ISBN: 978-0-7923-3683-9

  • Online ISBN: 978-0-306-48127-7

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics