Abstract
Cyanobacteria, as the most simple organisms to perform oxygenic photosynthesis differ from higher plants especially with respect to the thylakoid membrane structure and the antenna system used to capture light energy. Cyanobacterial antenna systems, the phycobilisomes (PBS), have been shown to be associated with Photosystem 2 (PS 2) at the cytoplasmic side, forming a PS 2-PBS-supercomplex, the structure of which is not well understood. Based on structural data of PBS and PS 2, a model for such a supercomplex is presented. Its key features are the PS 2 dimer as prerequisite for formation of the supercomplex and the antiparallel orientation of PBS-cores and the two PS 2 monomers which form the ‘contact area’ within the supercomplex. Possible consequences for the formation of ‘superstructures’ (PS 2-PBS rows) within the thylakoid membrane under so-called ‘state 1’ conditions are discussed. As there are also indications for specific functional connections of PBS with Photosystem 1 (PS 1) under so-called ‘state 2’ conditions, we show a model which reconciles the need for a structural interaction between PBS and PS 1 with the difference in structural symmetry (2-fold rotational symmetry of PBS-cores, 3-fold rotational symmetry of trimeric PS 1). Finally, the process of dynamic coupling and uncoupling of PBS to PS 1 and PS 2, based on the presented models, shows analogies to mechanisms for the regulation of photosynthetic electron flow in higher plants-despite the very different organization of their thylakoid membranes in comparison to cyanobacteria.
Similar content being viewed by others
Abbreviations
- APC:
-
allophycocyanin
- b 6 f :
-
cytochrome b 6 f complex
- CP:
-
chlorophyll protein
- FNR:
-
ferredoxin-NADP+-oxidoreductase
- LD:
-
linkerprotein-domain
- LHC:
-
light-harvesting complex
- Pc:
-
plastocyanin
- PC:
-
phycocyanin
- PD:
-
phycobiliprotein-domain
- PS 1:
-
Photosystem 1
- PS 2:
-
Photosystem 2
- PBS:
-
phycobilisome
References
Åkerlund, H-E (1993) Function and organization of Photosystem 2. In: Sundgvist, C and Ryberg, M (eds) Pigment-Protein Complexes in Plastids: Synthesis and Assembly, pp 419–446. Academic Press, San Diego, CA
Allen, JF (1992) Protein phosphorylation in regulation of photosynthesis. Biochim Biophys Acta 1098: 275–335
Allen, JF, Sanders, CE and Holmes, NG (1985) Correlation of membrane protein phosphorylation with excitation energy distribution in the cyanobacterium Synechococcus 6301. FEBS Lett 193: 271–275
Allen, JF, Alexciev, K and Hakansson, G (1995) Regulation by redox signalling. Curr Biol 5: 869–872
Almog, O, Shoham, G, Michaeli, D and Nechustai, R (1991) Monomeric and trimeric forms of the Photosystem 1 reaction center of Mastigocladus laminosus: Crystallization and preliminary characterization. Proc Natl Acad Sci USA 88: 5312–5316
Andersen, B, Scheller, HV and Moller, BL (1992) The PS 1-E-subunit of Photosystem 1 binds Ferredoxin:NADP+ oxidoreductase. FEBS Lett 311: 169–173
Anderson, LK and Eiserling, J (1986) Asymmetrical core structure in phycobilisomes of the cyanobacterium Synechocystis 6701. J Mol Biol 191: 441–451
Andrée, S, Spittel, M and Weis, E (1995) Distribution, organisation and functional state of PS 1, PS 2 and LHC-complexes in tylakoids after LHC2 phosphorylation. In: Mathis, P (ed) Photosynthesis: From Light to Biosphere, Vol III, pp 233–236. Kluwer Academic Publishers, Dordrecht
Apt, KE, Collier, JL and Grossman, AR (1995) Evolution of phycobiliproteins. J Mol Biol 248: 79–96
Barber, J and Andersson, B (1994) Revealing the blueprint of photosynthesis. Nature 370: 31–34
Barber, J and De LasRivas, J (1993) A functional model for the role of cytochrome b559 in the protection against donor and acceptor side photoinhibition. Proc Natl Acad Sci USA 90: 10942–10946
Bassi, R, Magaldi, AG, Tognon, G, Giacometti, GM and Miller, KR (1989) Two-dimensional crystals of the Photosystem 2 reaction center complex from higher plants. Eur J Cell Biol 50: 84–93
Bassi, R, Manquardt, J and Lavergne, J (1995) Biochemical and functional properties of Photosystem 2 in agranal membranes from maize mesophyll and bundle sheath chloroplasts. Eur J Biochem 233: 709–719
Bendall, DS and Manasse, RS (1995) Cyclic photophosphorylation and electron transport. Biochim Biophys Acta 1229: 23–38
Boekema, EJ, Dekker, JP, vanHeel, MG, Rögner, M, Saenger, W, Witt, I and Witt, HT (1987) Evidence for a trimeric organization of the Photosystem 1 complex from the thermophilic cyanobacterium Synechococcus sp. FEBS Lett 217: 283–286
Boekema, EJ, Hankamer, B, Bald, D, Kruip, J, Baonstra, AF, Barber, J and Rögner, M (1995) Supramolecular structure of the Photosystem 2 complex from green plants and cyanabacteria. Proc Natl Acad Sci USA 92: 175–179
Bricker, T (1990) The structure and function of CPa1 and CPa2 in Photosystem 2. Photosynth Res 24: 1–13
Bricker, T (1992) Oxygen evolution in the absence of the 33 kDa manganese-stabilizing protein. Biochemistry 31: 4623–4628
Bryant, DA (1988) Genetic analysis of phycobilisome biosynthesis, assembly, structure, and function in the cyanobacterium Synechoccoccus PCC 7002. In: Stevens, SE and Bryant, DA (ed) Light Energy Transduction in Photosynthesis: Higher Plant and Bacterial Models, pp 62–90. The American Society of Plant Physiologists, Rockville, MD
Bryant, DA (1991) Cyanobacterial phycobilisomes; progress towards a complete structural and functional analysis via molecular genetics. In: Bogorad, L and Vasil, K (eds) The Photosynthetic Apparatus; Molecular Biology and Operation, pp 257–300, Academic Press, New York
Burnap, RL and Sherman, LA (1991) Deletion mutagenesis in Synechocystis sp. PCC 6803 indicates that the Mn-stabilizing of Photosystem 2 is not essential for oxygen evolution. Biochemistry 30: 440–446
Capuano, V, Thomas, JC, Tandeau de Marssac, N and Houmard, J (1991) The anchor polypeptide of cyanobacterial phycobilisomes. J Biol Chem 266: 7239–7247
Capuano, V, Thomas, JC, Tandeau de Marssac, N and Houmard, J (1993) An in vivo approach to define the role of the LCM: The key polypeptide of cyanobacterial phycobilisomes. J Biol Chem 268: 8277–8283
Chereskin, BM, Clement-Metral, J and Gantt, E (1985) Characterization of a purified PS 2-phycobitisome particle preparation from Porphyridium cruentum. Plant Physiol 77: 626–629
Chitnis, VP and Chitnis, PR (1993) PsaL subunit is required for the formation of Photosystem 1 trimers in the cyanobacterium Synechocystis sp. PCC 6803. FEBS Lett 336: 330–334
Cleland, RE and Bendall, DS (1992) Photosystem 1 cyclic electron transport: Measurements of ferredoxin-plastoquinone reductase activity. Photosynth Res 34: 409–418
Cramer, WA, Tae, G, Furbacher, PN and Boettger, MI (1993) The enigmatic cytochrome b-599 of oxygenic photosynthesis. Physiologica Plantarum 88: 705–711
Dainese, P, Santini, C, Ghiretti-Magaldi, A, Marquardt, J, Tidu, V, Mauro, S, Bergantino, E and Bassi, R (1992) The organisation of pigment-protein within Photosystem 2. In: Murata, N (ed) Research in Photosynthesis, Vol II, pp 13–20. Kluwer Academic Publishers, Dordrecht
Dehus, R (1992) The manganese and calcium ions of photosynthetic oxyen evolution. Biochim Biophys Acta 1102: 269–352
Deisenhofer, J, Epp, O, Miki, K, Huber, R and Michel, H (1985) Structure of the protein subunits in the photosynthetic reaction center of Rhodopseudomonas viridis at 3 Å resolution. Nature 318: 618–624
Dekker, JP, Boekema, EJ, Witt, HT and Rögner, M (1988) Refined purification and further characterization of oxygen-evolving and Tris-treated Photosystem 2 particles from the thermophilic cyanobacterium Synechococcus sp. Biochim Biophys Acta 936: 307–318
Dekker, JP, Betts, SD, Yacum, CF and Boekema, EJ (1990) Characterization by electron microscopy of isolated particles and two-dimensional crystals of the CP47-D1-D2-cytochrome b-559 complex of Photosystem 2. Biochemistry 29: 3220–3225
Diner, BA, Nixon, PJ and Farchaus, JW (1991) Site-directed mutagenesis of photosynthetic reaction centers. Curr Opin Struct Biol 1: 546–554
Ford, RC and Holzenburg, A (1988) Investigation of the structure of trimeric and monomeric Photosystem I reaction center complexes. EMBO J 7: 2287–2293
Fueglistaller, P, Ruembeli, R, Suter, F and Zuber, H (1984) Minor polypeptides from the phycobilisome of the cyanobacterium Mastigocladus laminosus. Isolation, characterization and aminoacid sequences of a colourless 8,9 kDa polypeptide and of a 16.2 kDa phycobiliprotein. Z Physiol Chemie 365: 1085–1096
Fueglistaller, P, Mimuro, M, Suter, F and Zuber, H (1987) Allophycocyanin complexes of the phycobilisome from Mastigocladus laminosus: Influence of the linker polypeptide LC 8.9 on the spectral properties of the phycobiliprotein subunits. Biol Chem 368: 353–367
Fujita, Y, Murakami, A, Aizawa, K and Ohki, K (1994) Short-term and long-term adaptations of the photosynthetic apparatus: Homeostatic properties of thylakoids. In: Bryant, DA (ed) The Molecular Biology of Cyanobacteria, pp 677–692. Kluwer Academic Publishers, Dordrecht
Gantt, E (1994) Supramolecular membrane organization. In: Bryant, DA (ed) The Molecular Biology of Cyanobacteria, pp 119–138. Kluwer Academic Publishers, Dordrecht
Gantt, E and Conti, SF (1966) Granules associated with the chloroplast lamellae of Porphyridium cruentvm. J Cell Biol 54: 313–324
Gantt, E and Lipschul, CA (1973) Energy transfer in phycobilisomes from phycoerythrin to allophycocyanin. Biochim Biophys Acta 292: 858–861
Ghirardi, ML, Mahajan, S, Sopory, SK, Edelman, M and Mattoo, AK (1993) Photosystem 2 reaction center particles from Spirodela stroma lamellae. J Biol Chem 268: 5357–5360
Glazer, AN (1984) Phycobilisome, a macromolecular complex optimized for light energy transfer. Biochim Biophys Acta 768: 29–51
Glazer, AN, Gindt, YM, Chan, CF and Sauer, K (1994) Selective disruption of energy flow from phycobilisomes to Photosystem 1. Photosynth Res 40: 167–173
Gleiter, HM, Haag, E, Shen, J-R, Eaton-Rye, JJ, Seeliger, AG, Inoue, Y, Vermaas, WFJ and Renger, G (1995) Involvement of the CP47 protein in stabilization and photoactivation of a functional water-oxidizing complex in the cyanobacterium Synechocystis sp. PCC 6803. Biochemistry 34: 6847–6856
Golbeck, JH (1994) Photosystem 1 in cyanobacteria. In: Bryant, DA (ed) The Molecular Biology of Cyanobacteria, pp 319–360. Kluwer Academic Publishers, Dordrecht
Grossman, AR, Schaefer, MR, Chiang, G and Collier, JL (1993) The phycobilisome, a light-harvesting complex responsive to environmental conditions. Microbiol Rev 57: 725–749
Hankamer, B, Morris, E, Zheleva, D and Barber, J (1995) Biochemical characterization and structural analysis of monomeric and dimeric Photosystem 2 core preparations. In: Mathis, P (ed) Photosynthesis: From Light to Biosphere, Vol IIII, pp 365–368. Kluwer Academic Publishers, Dordrecht
Hladik, J and Sofrova, D (1991) Does the trimeric form of Photosystem 1 reaction center of cyanobacteria exist in vivo. Photosynth Res 29: 171–175
Holzenburg, A, Bewley, MC, Wilson, FH, Nicholson, WV and Ford, RC (1993) Three-dimensional structure of Photosystem 2. Nature 363: 470–472
Houmard, J, Capuano, V, Colombano, MV, Coursin, T and Tandeau de Marsac, N (1990) Molecular characterization of the terminal energy acceptor of cyanobacterial phycobilisomes. Proc Natl Acad Sci USA 87: 2152–2156
Ikeuchi, M, Shen, JR, Vermaas, WFJ, Pakrasi, HB, Diner, BA, Nixon, PJ, Kuriyama, A, Hirano, A and Inoue, Y (1992) Topography of Photosystem 2 complex. In: Murata, N (ed) Research in Photosynthesis Vol II. pp 175–178. Kluwer Academic Publishers, Dordrecht
Isono, T and Katoh, T (1987) Subparticles of Anabaena phycobilisomes. Arch Biochem Biophys 256: 371–324
Jansson, S (1993) The light-harvesting chlorophyll a/b-binding proteins. Biochim Biophys Acta 1184: 1–19
Joliot, P, Verméglio, A and Joliot, A (1993) Supramolecular membrane protein assemblies in photosynthesis and respiration. Biochim Biophys Acta 1141: 151–174
Kallas, T (1994) The cytochrome b6f complex. In: Bryant, DA (ed) The Molecular Biology of Cyanobacteria, pp 259–317. Kluwer Academic Publishers, Dordrecht
Krauss, N, Hinrichs, W, Witt, I, Fromme, P, PrilzkowVII, Dauter, Z, Betzel, C, Wilson, KS, Witt, HT and Saenger, W (1993) Three-dimensional structure of system 1 of photosynthesis at 6 Å resolution. Nature 361: 326–331
Krishtalik, LI, Tae, G-S, Cherepanov, DA and Cramer, WA (1993) The redox properties of cytochromes b imposed by the membrane electrostatic environment. Biophys J 65: 184–195
Kruip, J, Boekema, EJ, Bald, D, Boonstra, AF and Rögner, M (1993) Isolation and structural characterization of monomeric and trimeric Photosystem 1 complexes (P700*FA/FB and P700*FX) from the cyanobacterium Synechocystis PCC 68I73. J Biol Chem 268: 23353–23360
Kruip, J, Bald, D, Boekema, EJ and Rögner, M (1994) Evidence for the existence of trimeric and monomeric Photosystem 1 complexes in thylakoid membranes from cyanobacteria. Photosynth Res 40: 279–286
Kruip, J, Bald, D, Hankamer, B, Nield, J, Boonstra, AF, Barber, J, Boekema, EJ and Rögner, M (1995) Localization of subunits in PS 1, PS 2 and a PS 2/light-harvesting-supercomplex. In: Mathis, P (ed) Photosynthesis: From Light to Biosphere, Vol III, pp 405–408. Kluwer Academic Publishers, Dordrecht
Lange, W, Schatz, GH, Wilhelm, C and Mörschel, E (1990a) The supramolecular structure of the light-harvesting system of cyanobacteria and red algae. In: Baltscheffsky, M (ed) Current Research in Photosynthesis, Vol 2, pp 105–108. Kluwer Academic Publishers, Dordrecht
Lange, W, Wilhelm, C, Wehrmeyer, W and Mörschel, E (1990b) The supramolecular structure of Photosystem 2 — phycobilisome — complexes of Porphyridium Cruentum. Bot Acta 103: 250–257
Lelong, C, Boekema, EJ, Kruip, J, Bottin, H, Rögner, M and Sétif, P (1996) Characterization of a redox active cross-linked complex between cyanobacterial Photosystem 1 and soluble ferredoxin. EMBO J 15(9): 2160–2168
Lundell, DJ and Glazer, AN (1981) Allophycocyanin B: a common β-subunit in allophycocyanin B maximum wavelength 670 nanometers and allophycocyanin maximum wavelength 650 nanometers. J Biol Chem 256: 12600–12606
Lundell, DJ and Glazer, AN (1983) Molecular architecture of a light-harvesting antenna. Quartemany interactions in the Synechococcus 6301 phycobilisome core as revealed by partial tryptic digestion and circular dichroism studies. J Biol Chem 258: 8706–8713
Lundell, DJ, Yamanaka, G and Glazer, AN (1981) A terminal energy acceptor of the phycobilisome: The 75,000 dalton polypeptide of Synechococcus 6301 phycobilisomes — a new biliprotein. J Cell Biol 91: 315–319
Lyon, MK, Marr, KM and Furcinitti, PS (1993) Formation and characterization of two-dimensional crystals of Photosystem 2. J Struct Biol 110: 13–140
Marr, KM, Mastronarde, DN, Lyon, MK (1996) Two-dimensional crystals of Photosystem 2: Biochemical characterization, cryo-electron microscopy and localization of the D1 and Cytochrome b559 polypeptides. J Cell Biol 132: 823–833
McNamara, VP, Gounaris, K and Whitmarsh, J (1995) Stabilization of the high potential form of cytochrome b-559 of Photosystem 2 by calcium or lack of oxygen. In: Mathis, P (ed) Photosynthesis: From Light to Biosphere, Vol 11, pp 527–530. Kluwer Academic Publishers, Dordrecht
McIlhinney, RAJ (1990) The fats of life: The importance and function of protein acylation. Trends Biochem Sci 15: 387–391
Melis, A (1991) Dynamics of photosynthetic membrane composition and function. Biochim Biophys Acta 1058: 87–106
Metzger, H (1994) Inside job. Curr Biol 4: 377–379
Michel, H and Deisenhafer, J (1988) Relevance of the photosynthetic reaction center from purple bacteria to the structure of Photosystem 2. Biochemistry 27: 1–7
Miller, KR and Jacob, JS (1991) Surface structure of the Photosystem 2 complex. In: Baily, GW (ed) Proceedings of the 49th Annual Meeting of the Electron Microscopy Society of America, pp 196–197. San Francisco Press, San Francisco
Mörschel, E and Rhiel, E (1987) Phycobilisomes and thylakoids: The light-harvesting system of cyanobacteria and red algae. In: Harris, JR and Horne, RW (eds) Membranous Structures, pp 209–254. Academic Press, London
Mörschel, E and Schatz, GH (1987) Correlation of Photosystem 2 complexes with exoplasmatic freeze-fracture particles of thylakoids of the cyanobacterium Synechococcus sp. Planta 172: 145–154
Mullineaux, CW (1992) Excitation energy transfer from phycobilisomes to Photosystem 1 in a cyanobacterium. Biochim Biophys Acta 1100: 285–292
Mullineaux, CW (1994) Excitation energy transfer from phycobilisomes to Photosystem 1 in a cyanobacterial mutant lacking Photosystem 2. Biochim Biophys Acta 1184: 71–77
Mullineaux, CW and Halzwarth, AR (1991) Kinetics of exciton energy transfer in the cyanobacterial phycobilisome-Photosystem 2 complex. Biochim Biophys Acta 1098: 68–78
Murphy, DJ and Woodrow, IG (1983) Lateral heterogeneity in the distribution of thylakoid membrane lipid and protein component's and its implications for the molecular organization of photosynthetic membranes. Biochim Biophys Acta 725: 104–112
Mustardy, L, Cunningham, FX and Gantt, E (1992) Photosynthetic membrane topography: Quantitative in situ localization of Photosystem 1 and 2. Proc Natl Acad Sci USA 89: 10021–10025
Nakazato, K, Toyoshima, C, Enami, I and Inoue, Y (1996) Two-dimensional crystallization and cryoelectron microscopy of Photosystem 2. J Mol Biol 257: 225–232
Nilsson, F, Simpson, DJ, Jansson, C and Andersson, B (1992) Ultrastructural and biochemical characterization of a Synechocystis 6803 mutant with inactivated psbA genes. Arch Biochem Biophys 295: 340–347
Ohta, H, Yoshida, N, Sano, M, Hirano, M, Nakazato, K and Enami, I (1995) Evidence for electrostatic interactions of the loop A on CP47 with the extrinsic 33 kDa protein. In: Mathis, P (ed) Photosynthesis: From Light to Biosphere, Vol II, pp 361–364. Kluwer Academic Publishers, Dordrecht
Olive, J, M'Bina, I, Vernotte, C, Astier, C and Wollman, FA (1986) Randomization of the EF particles in thylakoid membranes of Synechocystis 6714 upon transition from state 1 to state 2. FEBS Lett 208: 308–312
Ortega, JM, Hervas, M and Losada, M (1995) A possible role for cytochrome b-559 in photosynthesis. In: Mathis, P (ed) Photosynthesis: From Light to Biosphere, Vol II, pp 697–700. Kluwer Academic Publishers, Dordrecht
Peter, GF and Thornber, JP (1991) Biochemical evidence that the higher plant Photosystem 2 core complex is organized as a dimer. Plant Cell Physiol 32: 1237–1250
Redlinger, T and Gantt, E (1982) A Mr 95,000 polypeptide in Porphyridium cruentum phycobilisomes and thylakoids: Possible function in linkage of phycobilisomes to thylakoids and in energy transfer. Proc Natl Acad Sci USA 79: 5542–5546
Reuter, W and Wehrmeyer, W (1990) Core substructure of Mastigocladus laminosus phycobilisomes: The central part of the tricylindrical core-APCM-contains the anchor peptide and no allophycocyanin B. Arch Microbiol 153: 111–117
Rögner, M, Dekker, JP, Boekema, EJ and Witt, HT (1987) Size, shape and mass of the oxygen-evolving Photosystem 2 complex from the thermophilic cyanobacterium Synechococcus sp. FEBS Lett 219: 207–211
Rögner, M, Mühlenhoff, U, Boekema, EJ and Witt, HT (1990a) Mono-, di- and trimeric PS 1 reaction center complexes isolated from the thermophilic cyanobacterium Synechococcus sp.: Size, shape and activity. Biochim Biophys Acta 1015: 415–424
Rögner, M, Nixon, PJ and Diner, B (1990b) Purification and characterization of Photosystem 1 and Photosystem 2 core complexes from wild-type and phycocyanin-deficient strains of the cyanobacterium Synechocystis PCC 6803. J Biol Chem 265: 6189–6196
Rögner, M, Chisholm, DA and Diner, BA (1991) Site-directed mutagenesis of the psbC Gene of Photosystem 2: Isolation and functional characterization of CP43-less Photosystem 2 core complexes. Biochemistry 30: 5387–5395
Rögner, M, Boekema, EJ and Barber, J (1996) How does Photosystem 2 split water? The structural basis of efficient energy conversion. Trends Biochem Sci 21: 44–49
Santini, C, Tidu, V, Tognon, G, Magaldi, A and Bassi, R (1994) Three-dimensional structure of the higherplant Photosystem 2 reaction centre and evidence for its dimeric organization in vivo. Eur J Biochem 221: 307–315
Sayre, RT and Wroebel-Boerner, EA (1994) Molecular topology of the Photosystem 2 chlorophyll a binding protein, CP43: Topology of a thylakoid membrane protein. Photosynth Res 40: 1–19
Scherer, S (1990) Do photosynthetic and respiratory electron transport chains share redox proteins? Trends Biochem Sci 15: 458–462
Schluchter, WM and Bryant, DA (1992) Molecular characterization of ferredoxin-NADP+ oxidoreductase in cyanobacteria: Cloning and sequence of the petH gene of Synechoccoccus PCC 7002 and studies on the gene product. Biochemistry 31: 3092–3102
Seibert, M (1995) Reflections on the nature and function of the Photosystem 2 reaction centre. Aust J Plant Physiol 22: 161–166
Shen, G, Boussiba, S and Vermaas, WFJ (1993) Synechocystis sp. PCC 6803 strains lacking Photosystem 1 and phycobilisome function. The Plant Cell 5: 1853–1863
Sherman, DM, Troyan, TA and Sherman, LA (1994) Localization of membrane proteins in the cyanobacterium Synechococcus sp. PCC 7942. Plant Physiol 106: 251–262
Sidler, WA (1994) Phycobilisome and phycobilisome structures. In: Bryant, DA (ed) The Molecular Biology of Cyanobacteria, pp 139–216. Kluwer Academic Publishers, Dordrecht
Su, X, Fraenkel, PG and Bogorad, L (1992) Excitation energy transfer phycocyanin to chlorophyll in an apcA-defective mutant of Synechocystis sp. PCC 6803. J Biol Chem 267: 22944–22950
Thompson, LK, Miller, A-F, Buser, CA, dePaula, JC and Brudvig, GW (1989) characterization of the multiple forms of cytochrome b-559 in Photosystem 2. Biochemistry 28: 8048–8056
Trissl, HW and Wilhelm, C (1993) Why do thylakoid membranes from higher plants form grana stacks? Trends Biochem Sci 18: 415–419
Tsiotis, G, Haase, W, Müller, S and Engel, A (1995) Evidence for the existence of trimeric Photosystem 1 in the cyanobacterial membranes by recombinant antibodies fragments. In: Mathis, P (ed) Photosynthesis: From Light to Biosphere, Vol II, pp 175–178, Kluwer Academic Publishers, Dordrecht
Valiela, I (1995) Marine Ecological Processes, pp 3–29. Springer-Verlag, Heidelberg
Vermaas, WFJ (1993) Molecular biology approaches to analyze Photosystem 2 structure and function. Ann Rev Plant Physiol Plant Mol Biol 44: 457–481
Vermaas, WFJ, Styring, S, Schröder, WP and Andersson, B (1993) Photosynthetic water oxidation: The protein framework. Photosynth Res 38: 249–263
Westermann, M, Emst, A, Brass, S, Böger, P and Wehrmeyer, W (1994) Ultrastructure of cell wall and photosynthetic apparatus of the phycobilisome-less Synechocystis sp. strain BO 8402 and phycobilisome-containing derivative strain BO 9201. Arch Microbiol 162: 222–232
Wolfe, GR, Cunningham, FX, Durnford, D, Green, B and Gantt, E (1994) Evidence for a common origin of chloroplasts with light-harvesting complexes of different pigmentation. Nature 367: 566–568
Yu, L, Zhao, J, Mühlenhoff, U, BDA and Golbeck, JH 1993 PsaE is required for in vivo cyclic electron flow around Photosystem 1 in the cyanobacterium Synechococcus sp. PCC 7002. Plant Physiol 103: 171–180
Zhao, J, Zhou, J and Bryant, DA (1992) Energy transfer processes in phycobilisomes as deduced from analysis of mutants of Synechococcus sp. PCC 7002. In: Murata, N (ed) Research in Photosynthesis, Vol 1, pp 25–32. Kluwer Academic Publishers, Dordrecht
Zilinskas, BA and Greenwald, LS (1986) Phycobilisome structure and function. Photosynth Res 10: 7–35
Zilinskas, BA and Howell, DA (1986) The immunologically conserved phycobilisome-thylakoid linker polypeptide. Plant Physiol 80: 829–833
Zuber, H (1986) Structure of light-harvesting antenna complexes of photosynthetic bacteria and red algae. Trends Biochem Sci 11: 414–419
Author information
Authors and Affiliations
Additional information
Dedicated to Prof. Dr. Horst Senger on the occasion of his 65th birthday.
Rights and permissions
About this article
Cite this article
Bald, D., Kruip, J. & Rögner, M. Supramolecular architecture of cyanobacterial thylakoid membranes: How is the phycobilisome connected with the photosystems?. Photosynth Res 49, 103–118 (1996). https://doi.org/10.1007/BF00117661
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00117661