Skip to main content
Log in

Photosystem II solubilizes as a monomer by mild detergent treatment of unstacked thylakoid membranes*

  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

We studied the aggregation state of Photosystem II in stacked and unstacked thylakoid membranes from spinach after a quick and mild solubilization with the non-ionic detergent n-dodecyl-α,D-maltoside, followed by analysis by diode-array-assisted gel filtration chromatography and electron microscopy. The results suggest that Photosystem II (PS II) isolates either as a paired, appressed membrane fragment or as a dimeric PS II-LHC II supercomplex upon mild solubilization of stacked thylakoid membranes or PS II grana membranes, but predominantly as a core monomer upon mild solubilization of unstacked thylakoid membranes. Analysis of paired grana membrane fragments reveals that the number of PS II dimers is strongly reduced in single membranes at the margins of the grana membrane fragments. We suggest that unstacking of thylakoid membranes results in a spontaneous disintegration of the PS II-LHC II supercomplexes into separated PS II core monomers and peripheral light-harvesting complexes.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Albertsson P-Å (2001) A quantitative model of the domain structure of the photosynthetic membrane. Trends Plant Sci 6: 349-354

    Article  PubMed  CAS  Google Scholar 

  • Aro E-M, Virgin I and Andersson B (1993) Photoinhibition of Photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143: 113-134

    Article  PubMed  CAS  Google Scholar 

  • Baena-González E, Barbato R and Aro E-M (1999) Role of phosphorylation in the repair cycle and oligomeric structure of Photosystem II. Planta 208: 196-204

    Article  Google Scholar 

  • Bald D, Kruip J and Rögner M (1996) Supramolecular architecture of cyanobacterial membranes: how is the phycobilisome connected with the photosystems? Photosynth Res 49: 103-118

    Article  CAS  Google Scholar 

  • Bassi R and Dainese P (1992) A supramolecular light-harvesting complex from chloroplast Photosystem II membranes. Eur J Biochem 204: 317-326

    Article  PubMed  CAS  Google Scholar 

  • Bassi R, Marquardt J and Lavergne J (1995) Biochemical and functional properties of Photosystem II in agranal membranes from maize mesophyll and bundle-sheath chloroplasts. Eur J Biochem 233: 709-719

    Article  PubMed  CAS  Google Scholar 

  • Berthold DA, Babcock GT and Yocum CF (1981) A highly resolved, oxygen-evolving Photosystem II preparation from spinach thylakoid membranes. EPR and electron transport properties. FEBS Lett 134: 231-234

    Article  CAS  Google Scholar 

  • Boekema EJ, Hankamer B, Bald D, Kruip J, Nield J, Boonstra AF, Barber J and Rögner M (1995) Supramolecular structure of the Photosystem II complex from green plants and cyanobacteria. Proc Natl Acad Sci USA 92: 175-179

    Article  PubMed  CAS  Google Scholar 

  • Boekema EJ, van Roon H and Dekker JP (1998) Specific association of Photosystem II and light-harvesting complex II in partially solubilized Photosystem II membranes. FEBS Lett 424: 95-99

    Article  PubMed  CAS  Google Scholar 

  • Boekema EJ, van Roon H, Calkoen F, Bassi R and Dekker JP (1999a) Multiple types of association of Photosystem II and its light-harvesting antenna in partially solubilized Photosystem II membranes. Biochemistry 38: 2233-2239

    Article  PubMed  CAS  Google Scholar 

  • Boekema EJ, van Roon H, van Breemen JFL and Dekker JP (1999b) Supramolecular organization of Photosystem II and its light-harvesting antenna in partially solubilized Photosystem II membranes. Eur J Biochem 266: 444-452

    Article  PubMed  CAS  Google Scholar 

  • Boekema EJ, van Breemen JFL, van Roon H and Dekker JP (2000a) Conformational changes in Photosystem II supercomplexes upon removal of extrinsic subunits. Biochemistry 39: 12907-12915

    Article  PubMed  CAS  Google Scholar 

  • Boekema EJ, van Breemen JFL, van Roon H and Dekker JP (2000b) Arrangement of Photosystem II supercomplexes in crystalline macrodomains within the thylakoid membranes of green plants. J Mol Biol 301: 1123-1133

    Article  PubMed  CAS  Google Scholar 

  • Boekema EJ, Jensen PE, Schlodder E, van Breemen JFL, van Roon H, Scheller HV and Dekker JP (2001) Green plant Photosystem I binds light-harvesting complex I on one side of the complex. Biochemistry 40: 1029-1036

    Article  PubMed  CAS  Google Scholar 

  • Boichenko VA (1998) Action spectra and functional antenna sizes of Photosystems I and II in relation to the thylakoid membrane organization and pigment composition. Photosynth Res 58: 163-174

    Article  CAS  Google Scholar 

  • Choquet Y and Vallon O (2000) Synthesis, assembly and degradation of thylakoid membrane proteins. Biochimie 82: 615-634

    Article  PubMed  CAS  Google Scholar 

  • Eshaghi S, Andersson B and Barber J (1999) Isolation of a highly active PS II-LHC II supercomplex from thylakoid membranes by a direct method. FEBS Lett 446: 23-26

    Article  PubMed  CAS  Google Scholar 

  • Eshaghi S, Turcsányi E, Vass I, Nugent J, Andersson B and Barber J (2000) Functional characterization of the PS II-LHC II supercomplex isolated by a direct method from spinach thylakoid membranes. Photosynth Res 64: 179-187

    Article  PubMed  CAS  Google Scholar 

  • Ghanotakis DF and Yocum CF (1990) Photosystem II and the oxygen-evolving complex. Ann Rev Plant Physiol Plant Mol Biol 41: 255-276

    Article  CAS  Google Scholar 

  • Hankamer B, Barber J and Boekema EJ (1997) Structure and membrane organization of Photosystem II in green plants. Ann Rev Plant Physiol Plant Mol Biol 48: 641-671

    Article  CAS  Google Scholar 

  • Hankamer B, Morris E, Nield J, Carne A and Barber J (2001) Subunit positioning and transmembrane helix organization in the core dimer of Photosystem II. FEBS Lett 504: 142-151

    Article  PubMed  CAS  Google Scholar 

  • Kruse O, Zheleva D and Barber J (1997) Stabilization of photosystem two dimers by phosphorylation: implication for the regulation of the turnover of D1 protein. FEBS Lett 408: 276-280

    Article  PubMed  CAS  Google Scholar 

  • Kruse O, Hankamer B, Konczak C, Gerle C, Morris E, Radunz A, Schmid GH and Barber J (2000) Phosphatidylglycerol is involved in the dimerization of Photosystem II. J Biol Chem 275: 6509-6514

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Nield J, Orlova EV, Morris EP, Gowen B, van Heel M and Barber J (2000) 3D map of the plant Photosystem II supercomplex obtained by cryoelectron microscopy and single particle analysis. Nat Struct Biol 7: 44-47

    Article  PubMed  CAS  Google Scholar 

  • Peter GF and Thornber JP (1991a) Biochemical composition and organization of higher plant Photosystem II light-harvesting pigment-proteins. J Biol Chem 266: 16745-16754

    PubMed  CAS  Google Scholar 

  • Peter GF and Thornber JP (1991b) Biochemical evidence that the higher plant Photosystem II core complex is organized as a dimer. Plant Cell Physiol 32: 1237-1250

    CAS  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 

  • Shi L-X, Lorkovic ZJ, Oelmüller R and Schröder WP (2000) The low molecular mass PsbWprotein is involved in the stabilization of the dimeric Photosystem II complex in Arabidopsis thaliana. J Biol Chem 275: 37945-37950

    Article  PubMed  CAS  Google Scholar 

  • Staehelin LA (1976) Reversible particle movements associated with unstacking and restacking of chloroplast membranes in vitro. J Cell Biol 71: 136-158

    Article  PubMed  CAS  Google Scholar 

  • Staehelin LA and van der Staay GWM (1996) Structure, composition, functional organization and dynamic properties of thylakoid membranes. In: Ort DR and Yocum CF (eds) Oxygenic Photosynthesis: The Light Reactions, pp 11-30. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • van Amerongen H and Dekker JP (2002) Light-harvesting in Photosystem II. In: Green BR and Parson WW (eds) Light-Harvesting Antennas in Photosynthesis, Kluwer Academic Publishers, Dordrecht, The Netherlands (in press)

    Google Scholar 

  • van Grondelle R, Dekker JP, Gillbro T and Sundström V (1994) Energy transfer and trapping in photosynthesis. Biochim Biophys Acta 1187: 1-65

    Article  Google Scholar 

  • van Roon H, van Breemen JFL, de Weerd FL, Dekker JP and Boekema EJ (2000) Solubilization of green plant thylakoid membranes with n-dodecyl-?,D-maltoside. Implications for the structural organization of the Photosystem II, Photosystem I, ATP synthase and cytochrome b 6 f complexes. Photosynth Res 64: 155-166

    Article  PubMed  CAS  Google Scholar 

  • Wollman F-A, Minai L and Nechustai R (1999) The biogenesis and assembly of photosynthetic proteins in thylakoid membranes. Biochim Biophys Acta 1411: 21-85

    Article  PubMed  CAS  Google Scholar 

  • Yakushevska AE, Jensen PE, Keegstra W, van Roon H, Scheller HV, Boekema EJ and Dekker JP (2001) Supermolecular organization of Photosystem II and its associated light-harvesting antenna in Arabidopsis thaliana. Eur J Biochem 268: 6020-6028

    Article  PubMed  CAS  Google Scholar 

  • Zouni A, Witt HT, Kern J, Fromme P, Krauss N, SaengerWand Orth P (2001) Crystal structure of Photosystem II from Synechococcus elongatus at 3.8 angstrom resolution. Nature 409: 739-743

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jan P. Dekker.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dekker, J.P., Germano, M., van Roon, H. et al. Photosystem II solubilizes as a monomer by mild detergent treatment of unstacked thylakoid membranes* . Photosynthesis Research 72, 203–210 (2002). https://doi.org/10.1023/A:1016188818591

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1016188818591

Navigation