Summary
In this chapter the structure and function of the extrinsic proteins of Photosystem II (PS II) are examined. Higher plants and green algae contain the 33 kDa manganese-stabilizing protein and the 24 kDa and the 16 kDa extrinsic proteins while the cyanobacteria contain the same manganese-stabilizing protein, cytochrome c550, and the 12 kDa extrinsic protein. These proteins serve as enhancers of O2 evolution, optimizing PS II activity at physiological calcium and chloride concentrations. They shield the manganese cluster from exogenous reductants and reactants in the surrounding aqueous phase. A number of molecular, biochemical, and structural studies have been used to probe the structures and functions of these proteins within the photosystem. We will discuss the proposed functional roles for these components, their structure (as deduced from biochemical and X-ray crystallographic studies) and the location of their proposed binding domains within the PS II complex.
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References
Abramowicz DA and Dismukes GC (1984) Manganese proteins isolated from spinach thylakoid membranes and their role in O2 evolution. II. A binuclear manganese-containing 34 kDa protein, a probable component of the water dehydrogenase system. Biochim Biophys Acta 765: 318–328
Adelroth P, Lindberg K and Andreasson L-E (1995) Studies of Ca+2 binding in spinach Photosystem II using 45Ca+2. Biochemistry 34: 9021–9027
Adir N (1999) Crystallization of the oxygen-evolving reaction centre of Photosystem II in nine different detergent mixtures. Acta Crystal 55: 891–894
Ahmed A, Tajmir-Riahi HA and Carpentier R (1995) A quantitative secondary structure analysis of the 33 kDa extrinsic protein of Photosystem II by FTIR spectroscopy. FEBS Lett 363: 65–68
Akerlund H-E, Jansson C and Andersson B (1982) Reconstitution of photosynthetic water splitting in inside-out thylakoid vesicles and identification of a participating polypeptide. Biochim Biophys Acta 681: 1–10
Anati R and Adir N (2000) Crystallization of dimers of the manganese-stabilizing protein of Photosystem II. Photosynth Res 64: 167–177
Andersson B, Larsson C, Jansson C, Ljungberg U and Akerlund H-E (1984) Immunological studies on the organization of proteins in photosynthetic oxygen evolution. Biochim Biophys Acta 766: 21–26
Balsera M, Arellano JB, Gutierrez JR, Heredia P, Revuelta JL and De Las Rivas J (2003) Structural analysis of the psbQ protein of Photosystem II by Fourier transform infrared and circular dichroic spectroscopy and by bioinformatic methods. Biochemistry 42: 1000–1007
Bernier M and Carpentier R (1995) The action of mercury on the binding of the extrinsic polypeptides associated with the water oxidizing complex of Photosystem II. FEBS Lett 360: 251–254
Betts S, Ross JR, Hall KU, Pichersky E and Yocum CF (1996a) Functional reconstitution of Photosystem II with recombinant manganese-stabilizing proteins containing mutations that remove the disulfide bridge. Biochim Biophys Acta 1274: 135–142
Betts SD, Ross JR, Pichersky E and Yocum CF (1996b) Cold-sensitive assembly of a mutant manganese-stabilizing protein caused by a val to ala replacement. Biochemistry 35: 6302–6307
Berts SD, Ross JR, Pichersky E and Yocum CF (1997) Mutation Val235 Ala weakens binding of the 33-kDa manganese stabilizing protein of Photosystem II to one of two sites. Biochemistry 36: 4047–4053
Berts SD, Lydakis-Simantiris N, Ross JR and Yocum CF (1998) The carboxyl-terminal tripeptide of the manganese-stabilizing protein is required for quantitative assembly into Photosystem II and for high rates of oxygen evolution activity. Biochemistry 37: 14230–14236
Biesiadke J, Loll B, Kern J, Irrgang K-D and Zouni A (2004) Crystal structure of cyanobacterial Photosystem II at 3.2 Å resolution: A closer look at the Mn-cluster. Phys Chem Chem Phys 6: 4733–4736
Boekema EJ, Hankamer B, Bald D, Kruip J, Nield J, Boonstra AF, Barber J and Rogner M (1995a) Supramolecular structure of the Photosystem II complex from green plants and cyanobacteria. Proc Natl Acad Sci USA 92: 175–179
Boekema EJ, Hankamer B, Bald D, Kruip J, Nield J, Boonstra AF, Barber J and Rogner M (1995b) Supramolecular structure of the Photosystem II complex from green plants and cyanobacteria. Proc Natl Acad Sci USA 92: 175–179
Boekema EJ, Nield J, Hankamer B and Barber J (1998) Localization of the 23-kDa subunit of the oxygen-evolving complex of Photosystem II by electron microscopy. Eur J Biochem 252: 268–276
Boekema EJ, van Breeman JFL, van Roon H and Dekker JP (2000) Conformational changes in Photosystem II supercomplexes upon removal of extrinsic subunits. Biochemistry 39: 12907–12915
Borthakur D and Haselkorn R (1989) Nucleotide sequence of the gene encoding the 33 kDa water oxidizing polypeptide in Anabaena sp. strain PCC 7120 and its expression in E. coli. Plant Mol Biol 13: 427–439
Boussac A and Rutherford AW (1988) Nature of the inhibition of the oxygen-evolving enzyme of Photosystem II induced by NaCl washing and reversed by the addition of Ca+2 or Sr+2. FEBS Lett 236: 432–436
Boussac A, Kuhl H, Un S, Rogner M and Rutherford AW (1998) Effect of near-infrared light on the S2-state of the manganese complex of Photosystem II from Synechococcus elongatus. Biochemistry 37: 8995–9000
Bricker TM (1990) The structure and function of CPa-1 and CPa-2 in Photosystem II. Photosynth Res 24: 1–13
Bricker TM (1992) Oxygen evolution in the absence of the 33 kDa manganese-stabilizing protein. Biochemistry 31: 4623–4628
Bricker TM and Frankel LK (1987) Use of a monoclonal antibody in structural investigations of the 49 kDa polypeptide of Photosystem II. Arch Biochem Biophys 256: 295–301
Bricker TM and Frankel LK (1998) The structure and function of the 33 kDa extrinsic protein of Photosystem II. A critical review. Photosynth Res 56: 157–173
Bricker TM and Frankel LK (2002) The structure and function of CP47 and CP43 in Photosystem II. Photosynth Res 72: 131–146
Bricker TM and Frankel LK (2003) Carboxylate groups on the manganese-stabilizing protein are required for efficient binding of the 24 kDa protein to Photosystem II. Biochemistry 42: 2056–2061
Bricker TM, Odom WR and Queirolo CB (1988) Close association of the 33 kDa extrinsic protein with the apoprotein of CPa-1 in Photosystem II. FEBS Lett 231: 111–117
Bricker TM, Morvant J, Masri N, Sutton H and Frankel LK (1998) Isolation of a highly active Photosystem II preparation from Synechocystis 6803 using a histidine-tagged mutant of CP 47. Biochim Biophys Acta 1409: 50–57
Bricker TM, Young A, Frankel LK and Putnam-Evans C (2002) Introduction of the 305Arg to 305Ser mutation in the large extrinsic loop E of the CP43 protein of Synechocystis sp. PCC6803 leads to the loss of cytochrome c550 binding to Photosystem II. Biochim Biophys Acta 1556: 92–96
Burnap RL and Sherman LA (1991) Deletion mutagenesis in Synechocystis sp. PCC 6803 indicates that the Mn-stabilizing protein of Photosystem II is not essential for oxygen evolution. Biochemistry 30: 440–446
Burnap RL, Shen J-R, Jursinic PA, Inoue Y and Sherman LA (1992) Oxygen yield and thermoluminescence characteristics of a cyanobacterium lacking the manganese-stabilizing protein of Photosystem II. Biochemistry 31: 7404–7410
Burnap RL, Qian M, Shen J-R, Inoue Y and Sherman LA (1994) Role of disulfide linkage and putative intermolecular binding residues in the stability and binding of the extrinsic manganese-stabilizing proteins to the Photosystem II reaction center. Biochemistry 33: 13712–13718
Burnap RL, Qian M, Al-Khaldi S and Pierce C (1995) Photoactivation and S-state cycling kinetics in Photosystem II mutants in Synechocystis sp. PCC6803. In: Mathis P (ed) Photosynthesis: From Light to Biosphere, Vol II, pp 443–446. Kluwer Academic Publishers, Dordrecht
Burnap RL, Qian M and Pierce C (1996) The manganese-stabilizing protein of Photosystem II modifies the in vivo deactivation and photoactivation kinetics of the H2O oxidation complex in Synechocystis sp. PCC6803. Biochemistry 35: 874–882
Calderone V, Trabucco M, Vujicic A, Battistutta R, Giacometti GM, Andreucci F, Barbato R and Zanotti G (2003) Crystal structure of the PsbQ protein of Photosystem II from higher plants. EMBO Reports 4: 900–905
Campbell KA, Gregor W, Pham DP, Peloquin JM, Debus RJ and Britt RD (1998a) The 23 and 17 kDa proteins of Photosystem II modulate the magnetic properties of the S1-state manganese cluster. Biochemistry 37: 5039–5045
Campbell KA, Peloquin JM, Pham DP, Debus RJ and Britt RD (1998b) Parallel polarization EPR detection of an S−1-state ‘multiline’ EPR signal in Photosystem II particles from Synechocystis sp. PCC 6803. J Am Chem Soc 120: 447–448
Cheniae GM and Martin IF (1971) Effects of hydroxylamine on Photosystem II. I. Factors affecting the decay of O2 evolution. Plant Physiol 47: 568–575
Cole J, Boska M Blough NV and Sauer K (1986) Reversible and irreversible effects of alkaline pH on Photosystem II electron-transfer reactions. Biochim Biophys Acta 848: 41–47
Coleman WJ and Govindjee (1987) A model for the mechanism of chloride activation of oxygen evolution in Photosystem II. Photosynth Res 13: 199–223
de Paula JC, Li PM, Miller AF, Wu BW and Brudvig GW (1986) Effect of the 17-and 23-kilodalton polypeptides, calcium, and chloride on electron transfer in Photosystem II. Biochemistry 25: 6487–6494
Eaton-Rye JJ and Murata N (1989) Evidence that the amino-terminus of the 33 kDa extrinsic protein is required for binding to the Photosystem II complex. Biochim Biophys Acta 977: 219–226
Eaton-Rye JJ and Vermaas WFJ (1991) Oligonucleotide-directed mutagenesis of psbB, the gene encoding CP 47, employing a deletion strain of the cyanobacterium Synechocystis sp. PCC 6803. Plant Mol Biol 17: 1165–1177
Enami I, Satoh K and Katoh S (1987) Crosslinking between the 33 kDa extrinsic protein and the 47 kDa chlorophyll-carrying protein of the PS II reaction center core complex. FEBS Lett 226: 161–165
Enami I, Mochizuki Y, Takahashi S, Kakuno T, Horio T, Satoh K and Katoh S (1990) Evidence from crosslinking for the nearest neighbor relationships among the three extrinsic proteins of spinach Photosystem II complexes that are associated with oxygen evolution. Plant Cell Physiol 31: 725–729
Enami I, Kaneko M, Kitamura N, Koike H, Sonoike K, Inoue Y and Katoh S (1991) Total immobilization of the extrinsic 33 kDa protein in spinach Photosystem II membrane preparations. Protein stoichiometry and stabilization of oxygen evolution. Biochim Biophys Acta 1060: 224–232
Enami I, Murayama H, Ohta H, Kamo M, Nakazato K and Shen JR (1995) Isolation and characterization of a Photosystem II complex from the red alga Cyanidium caldarium: Association of cytochrome c550 and a 12 kDa protein with the complex. Biochim Biophys Acta 1232: 208–216
Enami I, Tohri A, Kamo M, Ohta H and Shen J-R (1997) Identification of domains on the 43 kDa chlorophyll-carrying protein (CP 43) that are shielded from tryptic attack by binding of the extrinsic 33 kDa protein with Photosystem II complex. Biochim Biophys Acta 1320: 17–26
Enami I, Kikuchi S, Fukuda T, Ohta H and Shen JR (1998) Binding and functional properties of four extrinsic proteins of Photosystem II from a red alga, Cyanidium caldarium, as studied by release-reconstitution experiments. Biochemistry 37: 2787–2793
Enami I, Yoshihara S, Tohri A, Okumura A, Ohta H and Shen JR (2000) Cross-reconstitution of various extrinsic proteins and Photosystem II complexes from cyanobacteria, red algae and higher plants. Plant Cell Physiol 41: 1354–1364
Engels DH, Lott A, Schmid GH and Pistorius EK (1994) Inactivation of the water oxidizing enzyme in manganese stabilizing protein-free mutant cells of the cyanobacterium Synechococcus PCC 7942 and Synechocystis PCC6803 during dark incubation and conditions leading to photoinactivation. Photosynth Res 42: 227–244
Ferreira KN, Iverson TM, Maghlaovi K, Barber J and Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303: 1831–1838
Frankel LK and Bricker TM (1990) Mapping of NHS-biotinylation sites and the epitope of the monoclonal antibody FAC2 on the apoprotein of CPa-1. In: Baltscheffsky M (ed) Current Research in Photosynthesis, Vol I, pp 639–642. Kluwer Academic Publishers, Dordrecht
Frankel LK and Bricker TM (1992) Interaction of CPa-1 with the manganese-stabilizing protein of photosystem II: Identification of domains on CPa-1 which are shielded from N-hydroxysuccinimide biotinylation by the manganese-stabilizing protein. Biochemistry 31: 11059–11063
Frankel L and Bricker TM (1995) Interaction of the 33-kDa extrinsic protein with Photosystem II: Identification of domains on the 33-kDa protein that are shielded from NHS—-biotinylation by Photosystem II. Biochemistry 34: 7492–7497
Frankel LK, Cruz JA and Bricker TM (1999) Carboxylate groups on the manganese-stabilizing protein are required for its efficient binding to Photosystem II. Biochemistry 38: 14275–14278
Frazao C, Enguita FJ, Coelho R, Sheldrick GM, Navarro JA, Hervas M, De la Rosa MA and Corrondo MA (2001) Crystal structure of low-potential cytochrome c549, from Synechocystis sp. PCC 6803 at 1.21 Å resolution. J Biol Inorg Chem 6: 324–332
Ghanotakis DF, Babcock GT and Yocum CF (1984a) Calcium reconstitutes high rates of oxygen evolution in polypeptide depleted Photosystem II preparations. FEBS Lett 167: 127–130
Ghanotakis DF, Topper JN, Babcock GT and Yocum CF (1984b) Water-soluble 17-kDa and 23-kDa polypeptides restore oxygen evolution activity by creating a high-affinity biding-site for Ca2+ on the oxidizing side of Photosystem II. FEBS Lett. 170: 169–173
Ghanotakis DF, Topper JN and Yocum CF (1984c) Structural organization of the oxidizing side of Photosystem II: Exogenous reductants reduce and destroy the Mn-complex in Photosystem II membranes depleted of the 17 and 23 kDa polypeptides. Biochim Biophys Acta 767: 524–531
Ghanotakis DF, Babcock GT and Yocum CF (1985) On the role of water-soluble polypeptides (17, 23 kDa) calcium and chloride in photosynthetic oxygen evolution. FEBS Lett 192: 1–3
Frazao C, Enguita FJ, Coelho R, Sheldrick GM, Navarro JA, Hervas M, De la Rosa MA and Corrondo MA (2001) Crystal structure of low-potential cytochrome c549 from Synechocystis sp. PCC 6803 at 1.21 Å resolution. J. Biol Inorg Chem 6: 324–332
Gleiter HM, Haag E, Shen J-R, Eaton-Rye JJ, Inoue Y and Vermaas WFJ (1994) Functional characterization of mutant strains of the cyanobacterium Synechocystis PCC 6803 lacking short domains within the large, lumen-exposed loop of the chlorophyll protein CP47 in Photosystem II. Biochemistry 33: 12063–12071
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
Haag E, Eaton-Rye JJ, Renger G and Vermaas WFJ (1993) Functionally important domains of the large hydrophilic loop of CP 47 as probed by oligonucleotide-directed mutagenesis in Synechocystis sp. PCC 6803. Biochemistry 32: 4444–4454
Hackett CS and Strittmatter P (1984) Covalent crosslinking of the active sites of vesicle-bound cytochrome b5 and NADH cytochrome b5 reductase. J Biol Chem 259: 3275–3282
Han K-C, Shen J-R, Ikeuchi M and Inoue Y (1994) Chemical crosslinking studies of extrinsic proteins in cyanobacterial Photosystem II. FEBS Lett 355: 121–124
Hasler L, Ghanotakis D, Fedtke B, Spyridaki A, Miller M, Muller SA, Engle A and Tsotis G (1997) Structural analysis of Photosystem II: Comparative studies of cyanobacterial and higher plant Photosystem II complexes. J Struct Biol 119: 273–283
Hayashi H, Fujimura Y, Mohanty PS and Murata N (1993) The role of CP 47 in the evolution of oxygen and the binding of the extrinsic 33-kDa protein to the core complex of Photosystem II as determined by limited proteolysis. Photosynth Res 36: 35–42
Ho KK, Ulrich EL, Krogmann DW and Gomez-Lojero C (1979) Isolation of photosynthetic catalysts from cyanobacteria. Biochim Biophys Acta 545: 236–248
Holten RW and Meyers J (1963) Cytochromes of a blue-green algae: Extraction of a c-type with a strongly negative redox potential. Science 142: 234–235
Holzenburg A, Flint TD, Shepard FH and Ford RC (1996) Photosystem II: Mapping the locations of the oxygen evolution-enhancing subunits by electron microscopy. Micron 27: 121–127
Homann PH and Madabusi LM (1993) Modification of the thermoluminescence properties of Ca+2-depleted Photosystem II membranes by the 23 kDa extrinsic polypeptide and by oligocarboxylic acids. Photosynth Res 35: 29–39
Hong SK, Pawlikowski SA, Van der Meulen KA and Yocum CF (2001) The oxidation state of the Photosystem II manganese cluster influences the structure of the manganese-stabilizing protein. Biochim Biophys Acta 1504: 262–274
Hutchison R, Betts SD, Yocum CF and Barry BA (1998) Conformational changes in the extrinsic manganese-stabilizing protein upon binding to the Photosystem II reaction center: An isotope editing and FTIR study. Biochemistry 37: 5643–5653
Hutchinson RS, Steenhuis JJ, Yocum CF, Razeghifard MR and Barry BB (1999) Deprotonation of the 33-kDa, extrinsic, manganese-stabilizing subunit accompanies photooxidation of the manganese in Photosystem II. J. Biol. Chem. 274: 31987–31995
Ifuku K, Nakatsu T, Kato H and Sato F (2003) Crystallization and preliminary crystallographic studies on the extrinsic 23 kDa protein in the oxygen-evolving complex of Photosystem II. Acta Crystal D 59: 1462–1463
Ikeuchi M, Koike H and Inoue Y (1989) N-terminal sequencing of Photosystem II low-molecular-mass proteins. 5 and 3.1 kDa components of the O2-evolving core complex from higher plants. FEBS Lett 242: 263–269
Ishikawa Y, Yamamoto Y, Otsubo M, Theg SM and Tamura N (2002) Chemical modification of amine groups on PS II protein(s) retards photoassembly of the photosynthetic water-oxidizing complex. Biochemistry 41: 1972–1980
Isogai Y, Yamamoto Y and Nishimura M (1985) Association of the 33 kDa polypeptide with the 43 kDa component in Photosystem II particles. FEBS Lett 187: 240–244
Jansen T, Rother C, Steppuhn J, Reinke H, Beyreuther K, Jansson C, Andersson B and Herrmann RG (1987) Nucleotide sequence of cDNA clones encoding the complete 23 kDa and 16 kDa precursor proteins associated with the oxygen-evolving complex from spinach. FEBS Lett 216: 234–240
Johnsson GN, Boussac A and Rutherford AW (1994) The origin of 40–50 °C thermoluminescence bands in Photosystem II. Biochim Biophys Acta 1184: 85–92
Kamiya N and Shen J-R (2003) Crystal structure of oxygen-evolving Photosystem II from Thermosynechococcus vulcanus at 3.7 Ångstrom resolution. Proc Natl Sci Acad USA 100: 98–103
Kang C, Chitinis PR, Smith S and Krogmann DW (1994) Cloning and sequence analysis of the gene encoding the low potential cytochrome c of Synechocystis PCC 6803. FEBS Letters 344: 5–9
Kashino Y, Lauber WM, Carroll JA, Wang Q, Whitmarsh J, Satoh K and Pakrasi HB (2002) Proteomic analysis of a highly active Photosystem II preparation from the cyanobacterium Synechocystis sp. PCC 6803 reveals the presence of novel polypeptides. Biochemistry 41: 8004–8012
Kavelaki K and Ghanotakis DF (1991) Effect of the manganese complex on the binding of the extrinsic proteins (17 kDa, 23 kDa and 33 kDa) of photosystem. Photosynth Res 29: 149–155
Kieselbach T, Bystedt M, Hynds P, Robinson C and Schroder WP (2000) A peroxidase homologue and novel plastocyanin located by proteomics to the Arabidopsis chloroplast thylakoid lumen. FEBS Lett 480: 271–276
Krogmann DW (1991) The low potential cytochrome c of cyanobacteria and algae. Biochim Biophys Acta 1058: 35–37
Kuhl H, Rogner M, Van Breemen JF and Boekema EJ (1999) Localization of cyanobacterial Photosystem II donor-side subunits by electron microscopy and the supramolecular or-ganization of Photosystem II in the thylakoid membrane. Eur J Biochem 266: 453–459
Kuwabara T and Murata N (1983) Characterization of 33-kilodalton, 24-kilodalton and 18-kilodalton proteins in the photosynthetic oxygen-evolving system of spinach. In: Inoue Y, Crofts AR, Govindjee, Murata N, Renger G and Satoh K (eds) The Oxygen-Evolving System of Photosynthesis, pp 223–228. Academic Press, Tokyo
Kuwabara T, Miyao M, Murata T and Murata N (1985) The function of the 33 kDa protein in the oxygen evolution system studied by reconstitution experiments. Biochim Biophys Acta 806: 283–289
Kuwabara T, Murata T, Miyao M and Murata N (1986) Partial degradation of the 18 kDa of the photosynthetic oxygen-evolving complex: A study of a binding site. Biochim Biophys Acta 850: 146–155
Lakshmi KV, Reifler MJ, Chisholm DA, Wang JY, Diner BA and Brudvig GW (2002) Correlation of the cytochrome c550 content of cyanobacterial Photosystem II with the EPR properties of the oxygen-evolving complex. Photosynth Res72(2): 175–189
Leuschner C and Bricker TM (1996) Interaction of the 33 kDa extrinsic protein with Photosystem II: Rebinding of the 33 kDa extrinsic protein to Photosystem II membranes which contain four, two, or zero manganese per Photosystem II reaction center. Biochemistry 35: 4551–4557
Li ZL and Burnap RL (2001) Mutations of arginine 64 within the putative calcium-binding interhelical a-b loop of the Photosystem II D1 protein disrupt binding of the manganese-stabilizing protein and cytochrome c550 in Synechocystis sp. PCC 6803. Biochemistry 40: 10350–10359
Lindberg K and Andreasson L-E (1996) A one-site, two-state model for the binding of anions in Photosystem II. Biochemistry 35: 14259–14267
Lydakis-Simantiris N, Betts SD and Yocum CF (1999a) Leucine 245 is a critical residue for folding and function of the manganese-stabilizing protein of Photosystem II. Biochemistry 38: 15528–15535
Lydakis-Simantiris N, Hutchison RS, Betts SD, Barry BA and Yocum CF (1999b) Manganese stabilizing protein of Photosystem II is a thermostable, natively unfolded polypeptide. Biochemistry 38: 404–414
Mayes SR, Cook KM, Self SJ, Zhang Z and Barber J (1991) Deletion of the gene encoding the Photosystem II 33 kDa protein from Synechocystis sp PCC 6803 does not inactivate water-splitting but increases vulnerability to photoinhibition. Biochim Biophys Acta 1060: 1–12
Mavankal G, McCain DC and Bricker TM (1986) Effects of chloride on paramagnetic coupling of manganese in calcium chloride-washed Photosystem II preparations. FEBS Lett 202: 235–239
Miller AF, De Paula JC and Brudvig GW (1987) Formation of the S2-state and structure of the manganese complex in Photosystem II lacking the extrinsic 33 kDa polypeptide. Photosynth Res 12: 205–218
Millner PA, Gogel G and Barber J (1987) Investigation of the spatial relationships between photosystem 2 polypeptides by reversible crosslinking and diagonal electrophoresis. Photosynth Res 13: 185–198
Miura K, Shimazu T, Motoki A, Kani S, Hirano M and Katoh S (1993) Nucleotide sequence of the Mn-stabilizing protein gene of the thermophilic cyanobacterium Synechococcus elongatus. Biochim Biophys Acta 1172: 357–360
Miura T, Shen J-R, Takahashi S, Kamo M, Nakamura E, Ohta H, Kamei A, Inoue Y, Domae N, Takio K, Nakazato K, Inoue Y and Enami I (1997) Identification of domains on the extrinsic 33-kDa protein possibly involved in electrostatic interaction with Photosystem II complex by means of chemical modification. J Biol Chem 272: 3788–3798
Miyao M and Murata N (1983) Partial disintegration and reconstitution of the photosynthetic oxygen evolution complex. Biochim Biophys Acta 725: 87–93
Miyao M and Murata N (1984a) Calcium-ions can be substituted for the 24 kDa polypeptide in photosynthetic oxygen evolution. FEBS Lett 168: 118–120
Miyao M and Murata N (1984b) Role of the 33 kDa polypeptide in preserving Mn in photosynthetic oxygen-evolution. FEBS Lett 170: 350–354.
Miyao M and Murata N (1989) The mode of binding of three extrinsic proteins of 33 kDa, 23 kDa and 18 kDa in the Photosystem II complex of spinach. Biochim Biophys Acta 977: 315–321
Miyao M, Murata M, Lavorel J, Maison-Petri B, Boussac A and Etienne A-L (1987) Effects of the 33 kDa protein on the S-state transitions in photosynthetic oxygen evolution. Biochim Biophys Acta 890: 151–159
Miyao M, Fujimura Y and Murata N (1988) Partial degradation of the extrinsic 23 kDa protein of the Photosystem II complex of spinach. Biochim Biophys Acta 936: 465–474
Morris EP, Hankamer B, Zheleva D, Friso G and Barber J (1997) The three-dimensional structure of a Photosystem II core complex determined by electron crystallography. Structure 5: 837–849
Motoki A, Usui M, Shimazu T, Hirano M and Katoh S (2002) A domain of the Mn-stabilizing protein from Synechococcus elongatus involved in functional binding to Photosystem II. J Biol Chem 277: 14747–14756
Murakami R, Ifuku K, Takabayashi A, Shikanai T, Endo T and Sato F (2002) Characterization of an Arabidopsis thaliana mutant with impaired psbO, one of two genes encoding extrinsic 33-kDa proteins in Photosystem II. FEBS Lett 523: 138–142
Murata N, Miyao M, Omata T, Matsunami H and Kuwabara T (1984) Stoichiometry of components in the photosynthetic oxygen evolution system of Photosystem II particles prepared with Triton X-100 from spinach chloroplast. Biochim Biophys Acta 765: 363–369
Navarro JA, Hervas M, De la Cerda B and De la Rosa MA (1995) Purification and physicochemical properties of the low potential cytochrome C549 from the cyanobacterium Synechocystis sp. PCC 6803. Arch Biochem Biophys 3186: 46–52
Nakatani HY (1984) Photosynthetic oxygen evolution does not require the participation of polypeptides of 16 and 24 kDa. Biochem Biophys Res Comm 120: 299–304
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
Nield J, Kruse O, Ruprecht J, da Fonseca P, Buchel C and Barber J (2000) Three-dimensional structure of Chlamydomonas reinhardtii and Synechococcus elongatus Photosystem II complexes allows for comparison of their oxygen-evolving complex organization. J Biol Chem 275: 27940–27946
Nishiyama Y, Hayashi H, Watanabe T and Murata N (1994) Photosynthetic oxygen evolution is stabilized by cytochrome c550 against heat inactivation in Synechococcus sp PCC 7002. Plant Physiol 105: 1313–1319
Nishiyama Y, Los DA, Hayashi H and Murata N (1997) Thermal protection of the oxygen-evolving machinery by PsbU, an extrinsic protein of Photosystem II, in Synechococcus species PCC 7002. Plant Physiol 115: 1473–1480
Nishiyama Y, Los DA and Murata N (1999) PsbU, a protein associated with Photosystem II, is required for the acquisition of cellular thermotolerance in Synechococcus species PCC 7002. Plant Physiol 120: 301–308
Odom WR and Bricker TM (1992) Interaction of CPa-1 with the manganese-stabilizing protein of Photosystem II: Identification of domains crosslinked by l-ethyl-3-[3-(dimethylamino) propyl]carbodiimide. Biochemistry 31: 5616–5620
Oh-Oka H, Tanaka S, Wada K, Kuwabara T and Murata N (1986) Complete amino acid sequence of 33 kDa protein isolated from spinach Photosystem II particles. FEBS Lett 197: 63–66
Ohta H, Yoshida N, Sano M, Hirano M, Nakazato K and Enami I (1995) Evidence for electrostatic interaction of the loop A on CP 47 with the extrinsic 33 kDa protein. In: Mathis P (ed) Photosynthesis: From Light to Biosphere, Vol II, pp 361–364. Kluwer Academic Publishers, Dordrecht
Ohta H, Okumura A, Okuyama S, Akiyama A, Iwai M, Yoshihara S, Shen JR, Kamo M and Enami I (1999) Cloning, expression of the psbU gene, and functional studies of the recombinant 12-kDa protein of Photosystem II from a red alga Cyanidium caldarium. Biochem Biophys Res Comm 260: 245–50
Ono T and Inoue Y (1984) Ca+2-dependant restoration of O2-evolving activity in CaCl2-washed PS II particles depleted of 33, 24, and 16 kDa polypeptides. FEBS Lett 168: 281–286
Ono T and Inoue Y (1985) S-state turnover in the O2-evolving system of CaCl2-washed Photosystem II particles depleted of three peripheral proteins as measured by thermoluminescence. Removal of 33 kDa protein inhibits S3 to S4 transition. Biochim Biophys Acta 806: 331–340
Ono TA and Inoue Y (1988) Discrete extraction of the calcium atom functional for oxygen evolution in higher plant Photosystem II by a simple low pH treatment. FEBS Lett 227: 147–152
Ono TA and Inoue Y (1989a) Removal of calcium by pH 3.0 treatment inhibits S2 to S3 transition in photosynthetic oxygen evolution system. Biochim Biophys Acta 973: 443–449
Ono TA and Inoue Y (1989b) Roles of calcium ion in oxygen evolution in higher plant Photosystem II: Effects of replacement of calcium ion site by other cations. Arch Biochem Biophys 275: 440–448
Ono TA and Inoue Y (1990) Abnormal redox reactions in the photosynthetic O2-evolving centers in NaCl/EDTA-washed PS II. A dark-stable EPR multiline signal and an unknown positive charge accumulator. Biochim Biophys Acta 1020: 269–277
Ono T, Zimmerman JL, Inoue Y and Rutherford AW (1986) EPR evidence for a modified S-state transition in chloride-depleted Photosystem II. Biochim Biophys Acta 851: 193–201
Ono T, Izawa S and Inoue Y (1992) Structural and functional modulation of the manganese cluster in Ca+2-depleted Photosystem II by binding of the 24 kDa extrinsic protein. Biochemistry 31: 7648–7655
Pazos F, Heredia P, Valencia A and de las Rivas J (2001) Threading structural model of the manganese-stabilizing protein PsbO reveals presence of two possible beta-sandwich domains. Proteins 45: 372–381
Philbrick JB, Diner BA and Zilinskas BA (1991) Construction and characterization of cyanobacterial mutants lacking the manganese-stabilizing protein of Photosystem II. J Biol Chem 266: 13370–13376
Popelkova H, Im MM, D’Auria J, Betts SD, Lydakis-Simantiris N and Yocum CF (2002a) N-terminus of the Photosystem II manganese-stabilizing protein: Effects of sequence elongation and truncation. Biochemistry 41: 2702–2711
Popelkova H, Im MM and Yocum CF (2002b) N-terminal truncations of manganese stabilizing protein identify two amino acid sequences required for binding of the eukaryotic protein to Photosystem II and reveal the absence of one binding-related sequence in cyanobacteria. Biochemistry 41: 10038–10045
Popelkova H, Wyman A and Yocum CF (2003a) Amino acid sequences and solution structures of manganese-stabilizing protein that affects reconstitution of Photosystem II activity. Photosynth Res 77: 21–34
Popelkova H, Im MM and Yocum CF (2003b) Binding of manganese-stabilizing protein to Photosystem II: Identification of essential N-terminal threonine residues and domains that prevent nonspecific binding. Biochemistry 42: 6193–6200
Putnam-Evans C and Bricker TM (1992) Site-directed mutagenesis of the CPa-1 protein of Photosystem II: Alteration of the basic residue pair 384,385R to 384,385G leads to a defect associated with the oxygen-evolving complex. Biochemistry 31: 11482–11488
Putnam-Evans C, Wu J, Burnap R, Whitmarsh J and Bricker TM (1996) Site-directed mutagenesis of the CP 47 protein of Photosystem II: Alteration of conserved charged residues in the domain 364E-444R. Biochemistry 35: 4046–4053
Qian M, Al-Khaldi S, Putnam-Evans C, Bricker TM and Burnap RL (1997) Photoassembly of the Photosystem II (Mn)4 cluster in site-directed mutants impaired in the binding of the manganese stabilizing protein. Biochemistry 36: 15244–15252
Rashid A and Carpentier R (1990) The 16 and 23 kDa extrinsic polypeptides and the associated Ca2+ and Cl modify atrazine interaction with the Photosystem II core complex. Photosynth Res 24: 221–227
Razeghifard MR, Wydrzynski T, Pace RJ and Burnap RL (1997) YZ reduction kinetics in the absence of the manganese-stabilizing protein of Photosystem II. Biochemistry 36: 14474–14478
Reifler MJ, Chisholm DA, Wang J, Diner BA and Brudvig GW (1998) Engineering and rapid purification of histidine-tagged Photosystem II from Synechocystis PCC 6803. In: Garab G (ed) Photosynthesis: Mechanisms and Effects, Vol II, pp 1189–1192. Kluwer Academic Publishers, Dordrecht
Sawaya MR, Krogmann DW, Serag A, Ho, Yeates TO and Kerfeld CA (2001) Structures of cytochrome c549, and cytochrome c6 from the cyanobacterium Arthrospira maxima. Biochemistry 40: 9215–9225
Schubert M, Petersson U-A, Hass BJ, Funk C and Schroder WP (2002) Proteome map of the chloroplast lumen of Arabidopsis thaliana. J Biol Chem 277: 8354–8365
Seidler A (1994) Introduction of a histidine tail at the N-terminus of a secretory protein expressed in E. coli. Protein Engineering 7: 1277–1280
Seidler A (1996a) Intermolecular and intramolecular interactions of the 33 kDa protein of Photosystem II. Eur J Biochem 242: 485–490
Seidler A (1996b) The extrinsic polypeptides of Photosystem II. Biochim Biophys Acta 1277: 35–60
Seidler A and Rutherford AW (1996) The role of the extrinsic 33 kDa protein in Ca2+ binding in Photosystem II. Biochemistry 35: 12104–121010
Seidler A, Roll K and Michel H (1992) Characterization of the 33 kDa protein of the oxygen-evolving complex of higher plants by site-directed mutagenesis. In: Murata N (ed) Research in Photosynthesis, Vol II, pp 409–412. Kluwer Academic Press, Dordrecht
Seidler A, Rutherford AW and Michel H (1996a) The extrinsic 33 kDa protein of Photosystem II: Improved expression plasmids and progress in mutational analysis. In: Mathis P (ed) Photosynthesis: From Light to Biosphere, Vol II, pp 259–263. Kluwer Academic Press, Dordrecht
Seidler A, Rutherford AW and Michel H (1996b) On the role of the N terminus of the extrinsic 33 kDa protein of Photosystem II. Plant Mol Biol 31: 183–188
Shen G, Eaton-Rye JJ and Vermaas WFJ (1993) Mutation of histidine residues in CP 47 leads to a destabilization of the Photosystem II complex and to impairment of light energy transfer. Biochemistry 32: 5109–5115
Shen J-R and Inoue Y (1993a) Cellular localization of cytochrome c550: Its specific association with cyanobacterial Photosystem II. J Biol Chem 268: 20408–20413
Shen J-R and Inoue Y (1993b) Binding and functional properties of two new extrinsic components, cytochrome c550 and a 12 kDa protein in cyanobacterial Photosystem II. Biochemistry 32: 1825–1832
Shen J-R, Ikeuchi M and Inoue Y (1992) Stoichiometric association of extrinsic cytochrome c550 and the 12 kDa protein with a highly purified oxygen-evolving PS II core complex from Synechococcus vulcanus. FEBS Lett 301: 145–149
Shen J-R, Burnap RL and Inoue Y (1995a) An independent role of cytochrome c550 in cyanobacterial Photosystem II as revealed by double-deletion mutagenesis of the psbO and psbV genes in Synechocystis sp. PCC 6803. Biochemistry 34: 12661–12668
Shen J-R, Vermaas WFJ and Inoue Y (1995b) The role of cytochrome c550 as studied through reverse genetics and mutant characterization in Synechocystis sp. PCC 6803. J Biol Chem 270: 6901–6907
Shen J-R, Qian M, Inoue Y and Burnap RL (1998) Functional characterization of Synechocystis sp. PCC 6803 ΔpsbU and ΔpsbV mutants reveals important roles of cytochrome c550 in cyanobacterial oxygen evolution. Biochemistry 37: 1551–1558
Shutova T, Irrgang K-D, Shubin V, Klimov VV and Renger G (1997) Analysis of pH-induced structural changes of the isolated extrinsic 33 kilodalton protein of Photosystem II. Biochemistry 36: 6350–6358
Stewart A and Bendall D (1978) Preparation of active fractions enriched in Photosystem I and Photosystem II from the thermophilic blue-green alga Phormidium laminosum. Biochem Soc Trans 6: 1040–1041
Stewart A and Bendall D (1979) Properties of oxygen-evolving photosystem-II particles from Phormidium laminosum, a thermophillic blue-green alga. Biochem J 194: 877–887
Stewart A and Bendall D (1980) Photosynthetic electron transport in a cell-free preparation from the thermophilic blue-green alga Phormidium laminosum. Biochem J 188: 351–61
Stewart A and Bendall D (1981) Properties of oxygen-evolving Photosystem-II particles from Phormidium laminosum, a thermophilic blue-green alga. Biochem J 194: 877–887
Stewart AC, Ljungberg U, Aukerlund H-and Anderson B (1985a) Studies on the polypeptide composition of the cyanobacterial oxygen-evolving complex. Biochim Biophys Acta 808: 353–362
Stewart AC, Siczkowski M and Ljungberg U (1985b) Glycerol stabilizes oxygen evolution and maintains binding of a 9 kDa polypeptide in Photosystem II particles from the cyanobacterium Phormidium laminosum. FEBS Lett 193: 175–179
Stoylova SS, Flint TD, Ford RC and Holzenburg A (1997) Projection structure of Photosystem II in vivo determined by cryoelectron crystallography. Micron 28: 439–446
Styring S, Miyao M and Rutherford AW (1987) Formation and flash-dependent oscillation of the S2-state multiline EPR signal in an oxygen-evolving Photosystem II preparation lacking the three extrinsic proteins in the oxygen-evolving system. Biochim Biophys Acta 767: 32–38
Svensson B, Tiede DM and Barry BA (2002) Small-angle X-ray scattering studies of the manganese-stabilizing protein in Photosystem II. J Phys Chem B 106: 8485–8488
Tanaka S and Wada K (1988) The status of cysteine residues in the 33 kDa protein of spinach Photosystem II complexes. Photosynth Res 17: 255–266
Tang XS, Chisholm DA, Dismukes GC, Brudvig GW and Diner BA (1993) Spectroscopic evidence from site directed mutants of Synechocystis PCC6803 in favor of a close interaction between histidine 189 and redox active tyrosine 160, both of polypeptide D2 of the Photosystem II reaction center. Biochemistry 32: 13742–13748
Vass I, Cool KM, Zsuzsanra D, Mayes SR and Barber J (1992) Thermoluminescence and flash oxygen characterization of the IC2 deletion mutant of Synechocystis sp. PCC 6803 lacking the Photosystem II 33 kda protein. Biochim Biophys Acta 1102: 195–201
Vermaas WFJ, Ikeuchi M and Inoue Y (1988) Protein composition of the Photosystem II core complex in genetically engineered mutants of the cyanobacterium Synechocystis PCC 6803. Photosynth Res 17: 97–113
Vermaas WFJ, Charite J and Shen G (1990) Glu-69 of the D2 Protein in Photosystem II is a potential ligand to Mn involved in photosynthetic oxygen evolution. Biochemistry 29: 5325–5332
Vrettos JS, Reifler MJ, Kievit O, Lakshmi KV, de Paula JC and Brudvig GW (2001) Factors that determine the unusually low reduction potential of cytochrome c550 in cyanobacterial Photosystem II. J Biol Inorg Chem 6: 708–716.
Wales R, Newman BJ, Pappin D and Gray JC (1989) The extrinsic 33 kDa protein of the oxygen-evolving complex of Photosystem II is a putative calcium-binding protein and is encoded by a multi-gene family in pea. Plant Mol Biol 12: 439–451
Webber AN and Gray JC (1989) Detection of calcium binding by Photosystem II polypeptides immobilized onto nitrocellulose membranes. FEBS Lett 249: 79–82
Wincencjusz H, Yocum CF and van Gorkom HJ (1998) S-state dependence of chloride binding affinities and exchange dynamics in the intact and polypeptide depleted O2 evolving complex of Photosystem II. Biochemistry 37: 8595–8604
Wincencjusz H, Yocum CF and van Gorkom HJ (1999) Activating anions that replace chloride in the oxygen-evolving complex of Photosystem II slow the kinetics of the terminal step in water oxidation and destabilize the S2 and S3 states. Biochemistry 38: 3719–3725
Xu Q and Bricker TM (1992) Structural organization of proteins on the oxidizing side of Photosystem II: Two molecules of the 33 kDa manganese-stabilizing protein per reaction center. J Biol Chem 267: 25816–25821
Xu Q, Nelson J and Bricker TM (1994) Secondary structure of the 33 kDa, extrinsic protein of Photosystem II: A far-UV circular dichroism study. Biochim Biophys Acta 1188: 427–431
Yamamoto Y and Kubota F (1987) Specific release of the extrinsic 18-kDa protein from spinach Photosystem II particles by the treatment with NaCl and methanol and its application for large scale purification of the three extrinsic proteins of Photosystem II without chromatography. Biochim Biophys Acta 893: 579–583
Yamamoto Y, Nakayama S, Cohn CL and Krogmann DW (1987) Highly efficient purification of the 33-, 24-, and 18-kDa proteins in spinach Photosystem II by butanol/water phase partitioning and high-performance liquid chromatography. Arch Biochem Biophys 255: 156–161
Yu Y, Li R, Xu CH, Ruan KC, Shen YK and Govindjee (2001) N-bromosuccinimide modification of tryptophan 241 at the c-terminus of the manganese-stabilizing protein of plant Photosystem II influences its structure and function. Physiol Plant 111: 108–115
Zhang H, Fischer G and Wydrzynski T (1995) An FTIR study of calcium interactions in Photosystem II. In: Mathis P (ed) Photosynthesis: From Light to Biosphere, Vol II, pp 447–450. Kluwer Academic Press, Dordrecht
Zhang H, Ishikawa Y, Yamamoto Y and Carpentier R (1998) Secondary structure and thermal stability of the extrinsic 23 kDa protein of Photosystem II studied by Fourier transform infrared spectroscopy. FEBS Lett 426: 347–351
Zhang H, Yamamoto Y, Ishikawa Y and Carpentier R (1999) Characterization of the secondary structure and thermostability of the extrinsic 16 kilodalton protein of spinach Photosystem II by Fourier transform infrared spectroscopy. J Mol Struct 513: 127–132
Zhang L-X, Liang H-G, Wang J, Li WR and Yu TZ (1996) Fluorescence and Fourier-transform infrared spectroscopic studies on the role of disulfide bond in the calcium binding in the 33 kDa protein of Photosystem II. Photosynth Res 48: 379–384
Zouni A, Witt H-T, Kern J, Fromme P, Krauss N, Saenger W and Orth P (2001) Crystal structure of Photosystem II from Synechococcus elongatus at 3.8Å resolution. Nature 409: 739–743
Zubrzycki IZ, Frankel LK, Russo PS and Bricker TM (1998) Hydrodynamic studies on the manganese-stabilizing protein of Photosystem II. Biochemistry 37: 13553–13558
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Bricker, T.M., Burnap, R.L. (2005). The Extrinsic Proteins of Photosystem II. In: Wydrzynski, T.J., Satoh, K., Freeman, J.A. (eds) Photosystem II. Advances in Photosynthesis and Respiration, vol 22. Springer, Dordrecht. https://doi.org/10.1007/1-4020-4254-X_6
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