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Interaction of Photosystem 2-LHC2 Supercomplexes in Adjacent Layers of Stacked Chloroplast Thylakoid Membranes

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Photosynthetica

Abstract

Two Types of photosystem 2-light-harvesting complex 2 (PS2-LHC2) supercomplexes with similar pigment and protein composition were isolated directly from thylakoid membranes by sucrose density gradient centrifugation. Electron microscopy and single particle image analysis revealed the first Type as single unpaired PS2-LHC2 supercomplexes, whereas the second Type was characterized as pairs of two PS2-LHC2 supercomplexes attached together by their stromal sides. Unstacking of thylakoid membranes resulted in a spontaneous disintegration of the paired supercomplexes into single unpaired particles. A model of the organisation of the pigment-protein complexes in grana region is proposed.

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References

  • Allen, J.F., Forsberg, J.: Molecular recognition in thylakoid structure and function.-Trends Plant Sci. 6: 317-326, 2001.

    Google Scholar 

  • Andersson, B., Anderson, J.M.: Lateral heterogeneity in the dis-tribution of chlorophyll-protein complexes of the thylakoid membranes of spinach chloroplasts.-Biochim. biophys. Acta 593: 427-440, 1980.

    Google Scholar 

  • Barber, J.: Membrane surface charges and potentials in relation to photosynthesis. - Biochim. biophys. Acta 594: 253-308, 1980.

    Google Scholar 

  • Barber, J., Mills, J.: Control of chlorophyll fluorescence by the diffuse double layer.-FEBS Lett. 68: 288-292, 1976.

    Google Scholar 

  • Barber, J., Nield, J., Morris, E.P., Zheleva, D., Hankamer, B.: The structure, function and dynamics of photosystem two.-Physiol. Plant. 100: 817-827, 1997.

    Google Scholar 

  • Boekema, E.J., Hankamer, B., Bald, D., Kruip, J., Nield, J., Boonstra, A.F., Barber, J., Rögner, M.: Supramolecular struc-ture of the photosystem II complex from green plants and cyanobacteria.-Proc. nat. Acad. Sci. USA 92: 175-179, 1995.

    Google Scholar 

  • Boekema, E.J., Jensen, P.E., Schlodder, E., van Breemen, J.F.L., van Roon, H., Scheller, V.H., Dekker, J.P.: Green plant photosystem I binds light-harvesting complex I on one side of the complex.-Biochemistry 40: 1029-1036, 2001.

    Google Scholar 

  • Boekema, E.J., Nield, J., Hankamer, B., Barber, J.: Localization of the 23-kDa subunit of the oxygen evolving complex of photosystem II by electron-microscopy.-Eur. J. Biochem. 252: 268-276, 1998a.

    Google Scholar 

  • Boekema, E.J., van Breemen, J.F.L., van Roon, H., Dekker, J.P.: Arrangement of photosystem II supercomplexes in crys-talline macrodomains within the thylakoid membrane of green plant chloroplasts.-J. mol. Biol. 301: 1123-1133, 2000.

    Google Scholar 

  • Boekema, E.J., van Roon, H., Calkoen, F., Bassi, R., Dekker, J.P.: Multiple Types of association of photosystem II and its light-harvesting antenna in partially solubilized photosystem II membranes.-Biochemistry 38: 2233-2239, 1999.

    Google Scholar 

  • Boekema, E.J., van Roon, H., Dekker, J.P.: Specific association of photosystem II and light-harvesting complex II in partially solubilized photosystem II membranes.-FEBS Lett. 424: 95-99, 1998b.

    Google Scholar 

  • Bumba, L., Vácha, F.: Electron microscopy in structural studies of Photosystem II.-Photosynth. Res. 77: 1-19, 2003.

    Google Scholar 

  • Chow, W.S., Miller, C., Anderson, J.M.: Surface charges, the heterogenous lateral distribution of the two photosystems, and thylakoid stacking.-Biochim. biophys. Acta 1057: 69-77, 1991.

    Google Scholar 

  • Eshaghi, S., Andersson, B., Barber, J.: Isolation of a highly active PS2-LHC2 supercomplex from thylakoid membranes by a direct method.-FEBS Lett. 446: 23-26, 1999.

    Google Scholar 

  • Frank, J., Radermacher, M., Penczek, P., Zhu, J., Li, Y.H., Ladjadj, M., Leith, A.: SPIDER and WEB: Processing and vi-sualization of images in 3D electron microscopy and related fields.-J. struct. Biol. 116: 190-199, 1996.

    Google Scholar 

  • Green, B.R., Durnford, D.G.: The chlorophyll-carotenoid pro-teins of oxygenic photosynthesis.-Annu. Rev. Plant Physiol. Plant mol. Biol. 47: 685-714, 1996.

    Google Scholar 

  • Gross, E.L., Zimmermann, R.J., Hormats, G.F.: The effect of mono-and divalent cations on the quantum yields for electron transport in chloroplasts.-Biochim. biophys. Acta 440: 59-67, 1976.

    Google Scholar 

  • Hankamer, B., Barber, J., Boekema, E.J.: Structure and mem-brane organization of photosystem II in green plants.-Annu. Rev. Plant Physiol. Plant mol. Biol. 48: 641-671, 1997a.

    Google Scholar 

  • Hankamer, B., Morris, E.P., Nield, J., Carne, A., Barber, J.: Subunit positioning and transmembrane helix organisation in the core dimer of photosystem II.-FEBS Lett. 504: 142-151, 2001a.

    Google Scholar 

  • Hankamer, B., Morris, E., Nield, J., Gerle, C., Barber, J.: Three-dimensional structure of the photosystem II core dimer of higher plants determined by electron microscopy.-J. struct. Biol. 135: 262-269, 2001b.

    Google Scholar 

  • Hankamer, B., Nield, J., Zheleva, D., Boekema, E., Jansson, S., Barber, J.: Isolation and biochemical characterization of mo-nomeric and dimeric photosystem II complexes from spinach and their relevance to the organization of photosystem II in vivo.-Eur. J. Biochem. 243: 422-429, 1997b.

    Google Scholar 

  • Harauz, G., Boekema, E., van Heel, M.: Statistical image analysis of electron micrographs of ribosomal subunits.-Methods Enzymol. 164: 35-49, 1988.

    Google Scholar 

  • Harrer, R., Bassi, R., Testi, M.G., Schafer, C.: Nearest-neighbor analysis of a photosystem II complex from Marchantia polymorpha L. (liverwort), which contains reaction center and antenna proteins.-Eur. J. Biochem. 255: 196-205, 1998.

    Google Scholar 

  • Izawa, S., Good, N.E.: Effect of salts and electron transport on the conformation of isolated chloroplasts. II. Electron micro-scopy.-Plant Physiol. 41: 544-552, 1966.

    Google Scholar 

  • Jennings, R.C., Forti, G.: The influence of magnesium on the chlorophyll fluorescence yield of isolated chloroplasts.-Biochim. biophys. Acta 347: 299-310, 1974.

    Google Scholar 

  • Kamiya, N., Shen, J.R.: Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-angstrom resolution.-Proc. nat. Acad. Sci. USA 100: 98-103, 2003.

    Google Scholar 

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

    Google Scholar 

  • Laemmli, U.K.: Cleavage of structural proteins during the as-sembly of the head of bacteriophage T4.-Nature 227: 680-685, 1970.

    Google Scholar 

  • Murata, N.: Control of excitation transfer in photosynthesis. II. Magnesium ion-dependent distribution of excitation energy between two pigment systems in spinach chloroplasts.-Biochim. biophys. Acta 189: 171-181, 1969.

    Google Scholar 

  • Mustardy, L., Garab, G.: Granum revisited. A three-dimensional model-where things fall into place.-Trends Plant Sci. 8: 117-122, 2003.

    Google Scholar 

  • Nield, J., Orlova, E.V., Morris, E.P., Gowen, B., van Heel, M., Barber, J.: 3D map of the plant photosystem II supercomplex obtained by cryoelectron microscopy and single particle ana-lysis.-Nature struct. Biol. 7: 44-47, 2000.

    Google Scholar 

  • Scheller, H.V., Jensen, P.E., Haldrup, A., Lunde, C., Knoetzel, J.: Role of subunits in eukaryotic Photosystem I.-Biochim. biophys. Acta 1507: 41-60, 2001.

    Google Scholar 

  • Schmid, V.H.R., Potthast, S., Wiener, M., Bergauer, V., Paulsen, H., Storf, S.: Pigment binding of photosystem I light-harvesting proteins.-J. biol. Chem 277: 37307-37314, 2002.

    Google Scholar 

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

    Google Scholar 

  • Telfer, A., Nicolson, J., Barber, J.: Cation control of chloroplast structure and chlorophyll a fluorescence yield and its rele-vance to the intact chloroplast.-FEBS Lett. 65: 77-83, 1976.

    Google Scholar 

  • Vácha, F., Vácha, M., Bumba, L., Hashizume, K, Tani, T.: Inner structure of intact chloroplasts observed by a low tem-perature laser scanning microscope.-Photosynthetica 38: 493-496, 2000.

    Google Scholar 

  • van Heel, M., Frank, J.: Use of multivariate statistics in ana-lyzing the images of biological macromolecules.-Ultra-microscopy 6: 187-194, 1981.

    Google Scholar 

  • Yakushevska, A.E., Jensen, P.E., Keegstra, W., van Roon, H., Scheller, H.V., Boekema, E.J., Dekker, J.P.: Supermolecular organization of photosystem II and its associated light-har-vesting antenna in Arabidopsis thaliana.-Eur. J. Biochem. 268: 6020-6028, 2001.

    Google Scholar 

  • Zouni, A., Witt, H.T., Kern, J., Fromme, P., Krauss, N., Saenger, W., Orth, P.: Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution.-Nature 409: 739-743, 2001.

    Google Scholar 

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Bumba, L., Hušák, M. & Vácha, F. Interaction of Photosystem 2-LHC2 Supercomplexes in Adjacent Layers of Stacked Chloroplast Thylakoid Membranes. Photosynthetica 42, 193–199 (2004). https://doi.org/10.1023/B:PHOT.0000040590.10919.02

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