Structural and functional aspects of the MSP (PsbO) and study of its differences in thermophilic versus mesophilic organisms

Photosynthesis Research

Volumn 98, Issue 1-3, 2008, Pages 365-389

  Williamson, Adele K ^a  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

Manganese stabilizing protein; Oxygen evolution; Photosystem II; Thermophile

Indexed keywords

PHOTOSYSTEM II MANGANESE STABILIZING PROTEIN; PHOTOSYSTEM II MANGANESE-STABILIZING PROTEIN; WATER;

ACCLIMATIZATION; AMINO ACID SEQUENCE; CHEMISTRY; COMPARATIVE STUDY; CYANOBACTERIUM; HEAT; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR GENETICS; PHOTOSYSTEM II; PROTEIN SECONDARY STRUCTURE; REVIEW; SPECIES DIFFERENCE; SPINACH;

ACCLIMATIZATION; AMINO ACID SEQUENCE; CYANOBACTERIA; EVOLUTION, MOLECULAR; HOT TEMPERATURE; MOLECULAR SEQUENCE DATA; PHOTOSYSTEM II PROTEIN COMPLEX; PROTEIN STRUCTURE, SECONDARY; SPECIES SPECIFICITY; SPINACIA OLERACEA; WATER;

ALGAE; EMBRYOPHYTA; THERMOSYNECHOCOCCUS ELONGATUS;

EID: 57849159299     PISSN: 01668595     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11120-008-9353-7     Document Type: Review

References (184)

1. 2+) Biochemistry 34 9021 9027
2. A Ahmed HA Tajmirriahi R Carpentier 1995 A quantitative secondary structure-analysis of the 33-kDa extrinsic polypeptide of Photosystem-II by FTIR spectroscopy FEBS Lett 363 65 68
3. Ahrling KA, Pace RJ, Evans MCW (2005) The catalytic manganese cluster: Implications for spectroscopy. In: Wydrzynski T, Satoh K (eds) Photosystem II the light-driven water: Plastoquinone oxidoreductase, vol 22. Springer, Dordrecht, pp 285-306
4. SF Al-Khaldi J Coker JR Shen RL Burnap 2000 Characterization of site-directed mutants in manganese-stabilizing protein (MSP) of Synechocystis sp pcc6803 unable to grow photoautotrophically in the absence of cytochrome c-550 Plant Mol Biol 43 33 41
5. MA Arnott RA Michael CR Thompson DW Hough MJ Danson 2000 Thermostability and thermoactivity of citrate synthases from the thermophilic and hyperthermophilic archaea, thermoplasma acidophilum and pyrococcus furiosus J Mol Biol 304 657 668
6. E Bae GN Phillips 2004 Structures and analysis of highly homologous psychrophilic, mesophilic, and thermophilic adenylate kinases J Biol Chem 279 28202 28208
7. E Bae GN Phillips 2005 Identifying and engineering ion pairs in adenylate kinases J Biol Chem 280 30943 30948
8. M Balsera JB Arellano JL Revuelta J De Las Rivas JA Hermoso 2005 The 1.49 angstrom resolution crystal structure of PsbQ from Photosystem II of spinacia oleracea reveals a ppii structure in the n-terminal region J Mol Biol 350 1051 1060
9. J Barber 2003 Photosystem II: The engine of life Q Rev Biophys 36 71 89
10. J Barber 2006 Photosystem II: An enzyme of global significance Biochem Soc Trans 34 619 631
11. Barber J (2006b) Structure of Photosystem II and its implications for understanding the water splitting reaction it catalyses. BBA-Bioenergetics 36-36
12. Barber J, Iwata S (2005) Refined X-ray structure of Photosystem II and its implications. In: Wydrzynski T, Satoh K (eds) Photosystem II the light-driven water: Plastoquinone oxidoreductase, vol 22. Springer, Dordrecht, pp 469-489
13. GS Bell RJM Russell H Connaris DW Hough MJ Danson GL Taylor 2002 Stepwise adaptations of citrate synthase to survival at life's extremes-from psychrophile to hyperthermophile Eur J Biochem 269 6250 6260
14. DA Berthold GT Babcock CF Yocum 1981 A highly resolved, oxygen-evolving Photosystem-II preparation from spinach thylakoid membranes-electron paramagnetic resonance and electron transport properties FEBS Lett 134 231 234
15. SD Betts TM Hachigian E Pichersky CF Yocum 1994 Reconstitution of the spinach oxygen-evolving complex with recombinant Arabidopsis manganese-stabilizing protein Plant Mol Biol 26 117 130
16. SD Betts JR Ross KU Hall E Pichersky CF Yocum 1996 Functional reconstitution of Photosystem II with recombinant manganese-stabilizing proteins containing mutations that remove the disulfide bridge BBA-Bioenergetics 1274 135 142
17. S Betts C HaasePettingell J King 1997 Mutational effects on inclusion body formation Adv Protein Chem 50 243 264
18. SD Betts N Lydakis-Simantiris JR Ross CF Yocum 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
19. J Biesiadka B Loll J Kern KD Irrgang A Zouni 2004 Crystal structure of cyanobacterial Photosystem II at 3.2 angstrom resolution: A closer look at the mn-cluster Phys Chem Chem Phys 6 4733 4736
20. O Bogin I Levin Y Hacham S Tel-Or M Peretz F Frolow Y Burstein 2002 Structural basis for the enhanced thermal stability of alcohol dehydrogenase mutants from the mesophilic bacterium clostridium beijerinckii: Contribution of salt bridging Protein Sci 11 2561 2574
21. DR Boutz D Cascio J Whitelegge LJ Perry TO Yeates 2007 Discovery of a thermophilic protein complex stabilized by topologically interlinked chains J Mol Biol 368 1332 1344
22. TM Bricker 1992 Oxygen evolution in the absence of the 33-kilodalton manganese-stabilizing protein Biochemistry 31 4623 4628
23. Bricker TM, Burnap RL (2005) The extrinsic proteins of Photosystem II. In: Wydrzynski T, Satoh K (eds) Photosystem II the light-driven water:Plastoquinone oxidoreductase, vol 22. Springer, Dordrecht, pp 95-120
24. TM Bricker LK Frankel 1998 The structure and function of the 33 kDa extrinsic protein of Photosystem II: A critical assessment Photosynth Res 56 157 173
25. RD Britt KA Campbell JM Peloquin ML Gilchrist CP Aznar MM Dicus J Robblee J Messinger 2004 Recent pulsed epr studies of the Photosystem II oxygen-evolving complex: Implications as to water oxidation mechanisms BBA-Bioenergetics 1655 158 171
26. SJJ Brouns H Wu J Akerboom AP Turnbull WM de Vos J van der Oost 2005 Engineering a selectable marker for hyperthermophiles J Biol Chem 280 11422 11431
27. 2 evolution Biochemistry 30 440 446
28. RL Burnap JR Shen PA Jursinic Y Inoue LA Sherman 1992 Oxygen yield and thermoluminescence characteristics of a cyanobacterium lacking the manganese-stabilizing protein of Photosystem-II Biochemistry 31 7404 7410
29. RL Burnap M Qian JR Shen Y Inoue LA Sherman 1994 Role of disulfide linkage and putative intermolecular binding residues in the stability and binding of the extrinsic manganese-stabilizing protein to the Photosystem-II reaction-center Biochemistry 33 13712 13718
30. JM Chen WE Stites 2004 Replacement of staphylococcal nuclease hydrophobic core residues with those from thermophilic homologues indicates packing is improved in some thermostable proteins J Mol Biol 344 271 280
31. Chow WS, Aro EM (2005) Photoinctivation and mechanisms of recovery. In: Wydrzynski T, Satoh K (eds) Photosystem II the light-driven water: Plastoquinone oxidoreductase, vol 22. Springer, Dordrecht, pp 627-648
32. T Collins MA Meuwis C Gerday G Feller 2003 Activity, stability and flexibility in glycosidases adapted to extreme thermal environments J Mol Biol 328 419 428
33. H Dau M Haumann 2005 Considerations on the mechanism of photosynthetic water oxidation-dual role of oxo-bridges between mn ions in (i) redox-potential maintenance and (ii) proton abstraction from substrate water Photosynth Res 84 325 331
34. H Dau M Haumann 2007 Eight steps preceding o-o bond formation in oxygenic photo synthesis-a basic reaction cycle of the Photosystem II manganese complex BBA-Bioenergetics 1767 472 483
35. J De Las Rivas J Barber 2004 Analysis of the structure of the PsbO protein and its implications Photosynth Res 81 329 343
36. J De Las Rivas P Heredia 1999 Structural predictions on the 33 kDa extrinsic protein associated to the oxygen evolving complex of photosynthetic organisms Photosynth Res 61 11 21
37. J De Las Rivas A Roman 2005 Structure and evolution of the extrinsic proteins that stabilize the oxygen-evolving engine Photochem Photobiol Sci 4 1003 1010
38. J De Las Rivas M Balsera J Barber 2004 Evolution of oxygenic photosynthesis: Genome-wide analysis of the OEC extrinsic proteins Trends Plant Sci 9 18 25
39. J De Las Rivas P Heredia A Roman 2007 Oxygen-evolving extrinsic proteins (PsbO, PQ, R): Bioinformatic and functional analysis BBA-Bioenergetics 1767 575 582
40. RJ Debus 2000 The polypeptides of Photosystem II and their influence on manganotyrosyl-based oxygen evolution Met Ions Biol Syst 37 657 711
41. Debus RJ (2006) The catalytic manganese cluster: Protein ligation. In: Wydrzynski TS, Satoh K (eds) Photosystem II the light-driven water: Plastoquinone oxidoreductase, vol. 22. Springer, Dordrecht, pp 261-284
42. D. In: Wydrzynski T, Satoh K (eds) Photosystem II the light-driven water: Plastoquinone oxidoreductase, vol 22. Springer, Dordrecht, pp 207-233
43. JJ Eaton-Rye 2005 Requirements for different combinations of the extrinsic proteins in specific cyanobacterial Photosystem II mutants Photosynth Res 84 275 281
44. I Enami M Kamo H Ohta S Takahashi T Miura M Kusayanagi S Tanabe A Kamei A Motoki M Hirano T Tomo K Satoh 1998 Intramolecular cross-linking of the extrinsic 33-kDa protein leads to loss of oxygen evolution but not its ability of binding to Photosystem II and stabilization of the manganese cluster J Biol Chem 273 4629 4634
45. I Enami S Kikuchi T Fukuda H Ohta JR Shen 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
46. I Enami S Yoshihara A Tohri A Okumura H Ohta JR Shen 2000 Cross-reconstitution of various extrinsic proteins and Photosystem II complexes from cyanobacteria, red algae and higher plants Plant Cell Physiol 41 1354 1364
47. DH Engels A Lott GH Schmid EK Pistorius 1994 Inactivation of the water-oxidizing enzyme in manganese-stabilizing protein-free mutant-cells of the cyanobacteria synechococcus pcc7942 and Synechocystis pcc6803 during dark incubation and conditions leading to photoactivation Photosynth Res 42 227 244
48. WF Ettinger SM Theg 1991 Physiologically active chloroplasts contain pools of unassembled extrinsic proteins of the photosynthetic oxygen-evolving enzyme complex in the thylakoid lumen J Cell Biol 115 321 328
49. KN Ferreira TM Iverson K Maghlaoui J Barber S Iwata 2004 Architecture of the photosynthetic oxygen-evolving center Science 303 1831 1838
50. PA Fields 2001 Review: Protein function at thermal extremes: balancing stability and flexibility Comp Biochem Physiol A-Mol Integr Physiol 129 417 431
51. PA Fields BD Wahlstrand GN Somero 2001 Intrinsic versus extrinsic stabilization of enzymes-the interaction of solutes and temperature on α(4)-lactate dehydrogenase orthologs from warm-adapted and cold-adapted marine fishes Eur J Biochem 268 4497 4505
52. K Finsinger I Scholz A Serrano S Morales L Uribe-Lorio M Mora A Sittenfeld J Weckesser WR Hess 2008 Characterization of true-branching cyanobacteria from geothermal sites and hot springs of costa rica Environ Microbiol 10 460 473
53. RC Ford MCW Evans 1983 Isolation of a Photosystem II preparation from higher-plants with highly enriched oxygen evolution activity FEBS Lett 160 159 164
54. E Freire 1995 Thermodynamics of partly folded intermediates in proteins Annu Rev Biophys Biomol Struct 24 141 165
55. P Fromme J Kern B Loll J Biesiadka W Saenger HT Witt N Krauss A Zouni 2002 Functional implications on the mechanism of the function of Photosystem II including water oxidation based on the structure of Photosystem II Philos T Roy Soc B 357 1337 1344
56. DF Ghanotakis GT Babcock CF Yocum 1984 Calcium reconstitutes high-rates of oxygen evolution in polypeptide depleted Photosystem-II preparations FEBS Lett 167 127 130
57. DF Ghanotakis GT Babcock CF Yocum 1984 Structural and catalytic properties of the oxygen-evolving complex-correlation of polypeptide and manganese release with the behavior of z+ in chloroplasts and a highly resolved preparation of the PS-II complex Biochim Biophys Acta 765 388 398
58. DF Ghanotakis JN Topper GT Babcock CF Yocum 1984 Water-soluble 17-kDa and 23-kDa polypeptides restore oxygen evolution activity by creating a high-affinity binding-site for Ca-2+ on the oxidizing side of Photosystem-II FEBS Lett 170 169 173
59. GN Grove GW Brudvig 1998 Calcium binding studies of Photosystem II using a calcium-selective electrode Biochemistry 37 1532 1539
60. Gugliemi G, Cohen-Bazire G, Brynat D (1981) The structure of Gloeobacter violaceus and its phycobilisomes. Arch Microbiol 129:181-189
61. KC Han JR Shen M Ikeuchi Y Inoue 1994 Chemical cross-linking studies of extrinsic proteins in cyanobacterial Photosystem-II FEBS Lett 355 121 124
62. 2 production by green algae: From bioengineering to bioreactor scale-up Physiol Plantarum 131 10 21
63. H Hashimoto T Inoue M Nishioka S Fujiwara M Takagi T Imanaka Y Kai 1999 Hyperthermostable protein structure maintained by intra and inter-helix ion-pairs in archaeal O-6-methylguanine-DNA methyltransferase J Mol Biol 292 707 716
64. M Haumann C Muller P Liebisch L Iuzzolino J Dittmer M Grabolle T Neisius W Meyer-Klaucke H Dau 2005 Structural and oxidation state changes of the Photosystem II manganese complex in four transitions of the water oxidation cycle (S-0 ->S-1, S-1 ->S-2, S-2 ->S-3, and S-3,S-4 ->S-0) characterized by X-ray absorption spectroscopy at 20 k and room temperature Biochemistry 44 1894 1908
65. M Haumann C Muller P Liebisch T Neisius H Dau 2005 A novel bioxas technique with sub-millisecond time resolution to track oxidation state and structural changes at biological metal centers J Synchrotron Radiat 12 35 44
66. T Henmi Y Yamamoto 2002 Light-induced reactive oxygen species damage the extrinsic 33 kDa protein of Photosystem II Plant Cell Physiol 43 S62 S62
67. T Henmi M Miyao-Tokutomi Y Yamamoto 2003 Damage to oec33 of Photosystem II under strong light stress conditions Plant Cell Physiol 44 S191 S191
68. T Henmi H Yamasaki S Sakuma Y Tomokawa N Tamura MR Shen Y Yamamoto 2003 Dynamic interaction between the d1 protein, CP43 and oec33 at the lumenal side of Photosystem II in spinach chloroplasts: Evidence from light induced cross-linking of the proteins in the donor-side photoinhibition Plant Cell Physiol 44 451 456
69. T Henmi M Miyao Y Yamamoto 2004 Release and reactive-oxygen-mediated damage of the oxygen-evolving complex subunits of PSII during photoinhibition Plant Cell Physiol 45 243 250
70. P Heredia J De Las Rivas 2003 Calcium-dependent conformational change and thermal stability of the isolated PsbO protein detected by FTIR spectroscopy Biochemistry 42 11831 11838
71. 2 evolving complex of Photosystem II vary independently during S-state turnover Biochemistry 39 4399 4405
72. 2 evolving mechanism of Photosystem II BBA-Bioenergetics 1503 197 209
73. W Hillier T Wydrzynski 2004 Substrate water interactions within the Photosystem II oxygen evolving complex Phys Chem Chem Phys 6 4882 4889
74. W Hillier J Messinger T Wydrzynski 1998 Kinetic determination of the fast exchanging substrate water molecule in the S-3 state of Photosystem II Biochemistry 37 16908 16914
75. W Hillier G Hendry RL Burnap T Wydrzynski 2001 Substrate water exchange in Photosystem II depends on the peripheral proteins J Biol Chem 276 46917 46924
76. F Ho S Styring 2007 Access channels and methanol binding site to the CaMn4 cluster in Photosystem II based on solvent accessibility simulations, with implications for substrate water access Photosynth Res 91 180 180
77. FM Ho S Styring 2008 Access channels and methanol binding site to the CaMn4 cluster in Photosystem II based on solvent accessibility simulations, with implications for substrate water access BBA-Bioenergetics 1777 140 153
78. RS Hutchison SD Betts CF Yocum BA Barry 1998 Conformational changes in the extrinsic manganese-stabilizing protein upon binding to the Photosystem II reaction center: An isotope editing and FTIR study Biophys J 74 A16 A16
79. RS Hutchison SD Betts CF Yocum BA Barry 1998 Conformational changes in the extrinsic manganese stabilizing protein can occur upon binding to the Photosystem II reaction center: An isotope editing and FTIR study Biochemistry 37 5643 5653
80. BS Ibrahim V Pattabhi 2004 Role of weak interactions in thermal stability of proteins Biochem Biophys Res Commun 325 1082 1089
81. K Ifuku T Nakatsu H Kato F Sato 2004 Crystal structure of the PsbP protein of Photosystem II from Nicotiana tabacum Embo Rep 5 362 367
82. Y Ishikawa WP Schroder C Funk 2005 Functional analysis of the PsbP-like protein (sll1418) in Synechocystis sp pcc 6803 Photosynth Res 84 257 262
83. H Ishikita W Saenger B Loll J Biesiadka EW Knapp 2006 Energetics of a possible proton exit pathway for water oxidation in Photosystem II Biochemistry 45 2063 2071
84. H Ishikita D Stehlik JH Golbeck EW Knapp 2006 Electrostatic influence of PsaC protein binding to the PsaA/PsaB heterodimer in Photosystem I Biophys J 90 1081 1089
85. R Jaenicke G Bohm 1998 The stability of proteins in extreme environments Curr Opin Struct Biol 8 738 748
86. A Karshikoff R Ladenstein 2001 Ion pairs and the thermotolerance of proteins from hyperthermophiles: A 'traffic rule' for hot roads Trends Biochem Sci 26 550 556
87. U Kebekus J Messinger G Renger 1995 Structural-changes in the water-oxidizing plex monitored via the ph-dependence of the reduction rate of redox state S-1 by hydrazine and hydroxylamine in isolated spinach thylakoids Biochemistry 34 6175 6182
88. J Kern J Biesiadka B Loll W Saenger A Zouni 2007 Structure of the Mn-4-ca cluster as derived from X-ray diffraction Photosynth Res 92 389 405
89. 2 evolution Biochim Biophys Acta 807 64 73
90. J Kruk K Burda M Jemiola-Rzeminska K Strzalka 2003 The 33 kDa protein of Photosystem II is a low-affinity calcium- and lanthanide-binding protein Biochemistry 42 14862 14867
91. C Leuschner TM Bricker 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
92. DB Levin L Pitt M Love 2004 Biohydrogen production: Prospects and limitations to practical application Int J Hydrogen Energy 29 173 185
93. 2+ binding properties of wild type and heterologously expressed PsbO protein from cyanobacterial Photosystem II Biochemistry 44 4691 4698
94. B Loll J Kern W Saenger A Zouni J Biesiadka 2005 Towards complete cofactor arrangement in the 3.0 angstrom resolution structure of Photosystem II Nature 438 1040 1044
95. KA Luke CL Higgins P Wittung-Stafshedel 2007 Thermodynamic stability and folding of proteins from hyperthermophilic organisms FEBS J 274 4023 4033
96. B Lundin S Thuswaldner T Shutova S Eshaghi G Samuelsson J Barber B Andersson C Spetea 2007 Subsequent events to GTP binding by the plant PsbO protein: Structural changes, GTP hydrolysis and dissociation from the Photosystem II complex BBA-Bioenergetics 1767 500 508
97. N Lydakis-Simantiris RS Hutchison SD Betts BA Barry CF Yocum 1999 Manganese stabilizing protein of Photosystem II is a thermostable, natively unfolded polypeptide Biochemistry 38 404 414
98. A Martin V Sieber FX Schmid 2001 In-vitro selection of highly stabilized protein variants with optimized surface J Mol Biol 309 717 726
99. SR Mayes KM Cook SJ Self ZH Zhang J Barber 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
100. SP Mayfield P Bennoun JD Rochaix 1987 Expression of the nuclear encoded oee1 protein is required for oxygen evolution and stability of Photosystem-II particles in chlamydomonas-reinhardtii EMBO J 6 313 318
101. 2-evolving complex of Photosystem-II Photosynth Res 38 449 453
102. 2 metabolism in chlamydomonas reinhardtii (unicellular green algae) Planta 226 1075 1086
103. Melis A, Seibert M, Ghirardi ML (2007) Hydrogen fuel production by transgenic microalgae. In: Leon R, Gaven A, Fernandez E (eds) Transgenic Microalgae as Green Cell Factories. Landes Bioscience, Austin, TX, vol 616, pp 108-121
104. x Ca structures for the catalytic site and spectroscopic data Phys Chem Chem Phys 6 4764 4771
105. J Messinger G Seaton T Wydrzynski U Wacker G Renger 1997 S-3 state of the water oxidase in Photosystem II Biochemistry 36 6862 6873
106. K Miura T Shimazu A Motoki S Kanai M Hirano S Katoh 1993 Nucleotide-sequence of the Mn-stabilizing protein gene of the thermophilic cyanobacterium Synechococcus elongatus Biochim Biophys Acta 1172 357 360
107. T Miura JR Shen S Takahashi M Kamo E Nakamura H Ohta A Kamei Y Inoue N Domae R Takio K Nakazato Y Inoue I Enami 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
108. M Miyao N Murata 1984 Calcium-ions can be substituted for the 24-kDa polypeptide in photosynthetic oxygen evolution FEBS Lett 168 118 120
109. M Miyao N Murata 1984 Effect of urea on Photosystem-II particles-evidence for an essential role of the 33 kDa polypeptide in photosynthetic oxygen evolution Biochim Biophys Acta 765 253 257
110. M Miyao N Murata 1984 Role of the 33-kDa polypeptide in preserving Mn in the photosynthetic oxygen-evolution system and its replacement by chloride-ions FEBS Lett 170 350 354
111. M Miyao N Murata 1989 The mode of binding of 3 extrinsic proteins of 33-kDa, 23-kDa and 18-kDa in the Photosystem-II complex of spinach Biochim Biophys Acta 977 315 321
112. M Miyao N Murata J Lavorel B Maisonpeteri A Boussac AL Etienne 1987 Effect of the 33-kDa protein on the S-state transitions in photosynthetic oxygen evolution Biochim Biophys Acta 890 151 159
113. TR Morgan JA Shand SM Clarke JJ Eaton-Rye 1998 Specific requirements for cytochrome c-550 and the manganese-stabilizing protein in photoautotrophic strains of Synechocystis sp. PCC 6803 with mutations in the domain gly-351 to thr-436 of the chlorophyll-binding protein CP47 Biochemistry 37 14437 14449
114. A Motoki M Usui T Shimazu M Hirano S Katoh 2002 A domain of the manganese-stabilizing protein from Synechococcus elongatus involved in functional binding to Photosystem II J Biol Chem 277 14747 14756
115. R Murakami K Ifuku A Takabayashi T Shikanai T Endo F Sato 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
116. N Murata M Miyao T Omata H Matsunami T Kuwabara 1984 Stoichiometry of components in the photosynthetic oxygen evolution system of Photosystem-II particles prepared with triton X-100 from spinach-chloroplasts Biochim Biophys Acta 765 363 369
117. JW Murray J Barber 2006 Identification of a calcium-binding site in the PsbO protein of Photosystem II Biochemistry 45 4128 4130
118. JW Murray J Barber 2007 Structural characteristics of channels and pathways in Photosystem II including the identification of an oxygen channel J Struct Biol 159 228 237
119. Y Nakamura T Kaneko S Sato M Mimuro H Miyashita T Tsuchiya S Sasamoto A Watanabe K Kawashima Y Kishida C Kiyokawa M Kohara M Matsumoto A Matsuno N Nakazaki S Shimpo C Takeuchi M Yamada S Tabata 2003 Complete genome structure of Gloeobacter violaceus PCC 7421, a cyanobacterium that lacks thylakoids DNA Res 10 137 145
120. N Nelson CF Yocum 2006 Structure and function of Photosystems I and II Annu Rev Plant Biol 57 521 565
121. J Nield J Barber 2006 Refinement of the structural model for the Photosystem II supercomplex of higher plants BBA-Bioenergetics 1757 353 361
122. J Nield O Kruse J Ruprecht P da Fonseca C Buchel J Barber 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
123. J Nield EV Orlova EP Morris B Gowen M van Heel J Barber 2000 3D map of the plant Photosystem II supercomplex obtained by cryoelectron microscopy and single particle analysis Nat Struct Biol 7 44 47
124. J Nield M Balsera J De Las Rivas J Barber 2002 Three-dimensional electron cryo-microscopy study of the extrinsic domains of the oxygen-evolving complex of spinach Assignment of the PsbO protein J Biol Chem 277 23972 23972
125. Nixon PJ, Sarcina M, Diner BA (2005) The D1 and D2 core proteins. In: Wydrzynski TS, Satoh K (eds) Photosystem II the light-driven water: Plastoquinone oxidoreductase, vol. 22. Springer, Dordrecht, pp 71-94
126. M Nowaczyk C Berghaus R Stoll M Rogner 2004 Preliminary structural characterisation of the 33 kDa protein (psbo) in solution studied by site-directed mutagenesis and nmr spectroscopy Phys Chem Chem Phys 6 4878 4881
127. 2-extracted PS-II particles FEBS Lett 166 381 384
128. JB Philbrick BA Diner BA Zilinskas 1991 Construction and characterization of cyanobacterial mutants lacking the manganese-stabilizing polypeptide of Photosystem-II J Biol Chem 266 13370 13376
129. H Popelkova MM Im J D'Auria SD Betts N Lydakis-Simantiris CF Yocum 2002 N-terminus of the Photosystem II manganese stabilizing protein: Effects of sequence elongation and truncation Biochemistry 41 2702 2711
130. H Popelkova MM Im CF Yocum 2002 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
131. H Popelkova MM Im CF Yocum 2003 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
132. H Popelkova A Wyman C Yocum 2003 Amino acid sequences and solution structures of manganese stabilizing protein that affect reconstitution of Photosystem II activity Photosynth Res 77 21 34
133. JJ Pueyo M Alfonso C Andres R Picorel 2002 Increased tolerance to thermal inactivation of oxygen evolution in spinach Photosystem II membranes by substitution of the extrinsic 33-kDa protein by its homologue from a thermophilic cyanobacterium BBA-Bioenergetics 1554 29 35
134. 4 cluster in site-directed mutants impaired in the binding of the manganese-stabilizing protein Biochemistry 36 15244 15252
135. R Radmer O Ollinger 1982 Nitrogen and oxygen evolution by hydroxylamine-treated chloroplasts FEBS Lett 144 162 166
136. 2-evolving site determined with water analogs FEBS Lett 152 39 43
137. 2 evolution Biochim Biophys Acta 850 21 32
138. MR Razeghifard D Kuzek RJ Pace 2005 EPR kinetic studies of the S-1 state in spinach thylakoids BBA-Bioenergetics 1708 35 41
139. Renger G, Holzwarth AR (2005) Primary electron transfer. In: Wydrzynski T, Satoh K (eds) Photosystem II the light-driven water: Plastoquinone oxidoreductase, vol 22. Springer, Dordrecht, pp 139-175
140. G Renger T Bittner J Messinger 1994 Structure-function-relationships in photosynthetic water oxidation Biochem Soc T 22 318 322
141. Rippka R, Waterbury J, Cohnen-Bazire G (1974) A cyanobacterium which lacks thylakoids. Arch Microbiol 100:419-436
142. JL Roose Y Kashino HB Pakrasi 2007 The PsbQ protein defines cyanobacterial Photosystem II complexes with highest activity and stability Proc Natl Acad Sci USA 104 2548 2553
143. JL Roose KM Wegener HB Pakrasi 2007 The extrinsic proteins of Photosystem II Photosynth Res 92 369 387
144. Y Sambongi S Uchiyama Y Kobayashi Y Igarashi J Hasegawa 2002 Cytochrome c from a thermophilic bacterium has provided insights into the mechanisms of protein maturation, folding, and stability Eur J Biochem 269 3355 3361
145. A Seidler 1996 The extrinsic polypeptides of Photosystem II BBA-Bioenergetics 1277 35 60
146. A Seidler 1996 Intermolecular and intramolecular interactions of the 33-kDa protein in Photosystem II Eur J Biochem 242 485 490
147. Shen J-R, Kamiya N (2005) 3D crystal structure of the phososystem II core. In: Wydrzynski T, Satoh K (eds) Photosystem II the light-driven water: Plastoquinone oxidoreductase, vol 22. Springer, Dordrecht, pp 425-447
148. T Shutova KD Irrgang V Shubin VV Klimov G Renger 1997 Analysis of pH induced structural changes of the isolated extrinsic 33 kilodalton protein of Photosystem II Biochemistry 36 6350 6358
149. T Shutova KD Irrgang VV Klimov G Renger 2000 Is the manganese stabilizing 33 kDa protein of Photosystem II attaining a 'natively unfolded' or 'molten globule' structure in solution? FEBS Lett 467 137 140
150. T Shutova G Deikus KD Irrgang VV Klimov G Renger 2001 Origin and properties of fluorescence emission from the extrinsic 33 kDa manganese stabilizing protein of higher plant water oxidizing complex BBA-Bioenergetics 1504 371 378
151. T Shutova A Villarejo B Zietz V Klimov T Gillbro G Samuelsson G Renger 2003 Comparative studies on the properties of the extrinsic manganese- stabilizing protein from higher plants and of a synthetic peptide of its c-terminus BBA-Bioenergetics 1604 95 104
152. T Shutova J Nikitina G Deikus B Andersson V Klimov G Samuelsson 2005 Structural dynamics of the manganese-stabilizing protein-effect of ph, calcium, and manganese Biochemistry 44 15182 15192
153. T Shutova VV Klimov B Andersson G Samuelsson 2007 A cluster of carboxylic groups in PsbO protein is involved in proton transfer from the water oxidizing complex of Photosystem II BBA-Bioenergetics 1767 434 440
154. M Sonoyama A Motoki G Okamoto M Hirano H Ishida S Katoh 1996 Secondary structure and thermostability of the Photosystem II manganese-stabilizing protein of the thermophilic cyanobacterium Synechococcus elongatus Biochim Biophys Acta 1297 167 170
155. C Spetea T Hundal F Lohmann B Andersson 1999 GTP bound to chloroplast thylakoid membranes is required for light-induced, multienzyme degradation of the Photosystem II D1 protein Proc Natl Acad Sci USA 96 6547 6552
156. C Spetea T Hundal B Lundin M Heddad I Adamska B Andersson 2004 Multiple evidence for nucleotide metabolism in the chloroplast thylakoid lumen Proc Natl Acad Sci USA 101 1409 1414
157. AS Steunou D Bhaya MM Bateson MC Melendrez DM Ward E Brecht JW Peters M Kuhl AR Grossman 2006 In situ analysis of nitrogen fixation and metabolic switching in unicellular thermophilic cyanobacteria inhabiting hot spring microbial mats Proc Natl Acad Sci USA 103 2398 2403
158. T Suzuki H Ohta I Enami 2005 Cross-reconstitution of the extrinsic proteins and Photosystem II complexes from chlamydomonas reinhardtii and spinacia oleracea Photosynth Res 84 239 244
159. B Svensson DM Tiede DR Nelson BA Barry 2004 Structural studies of the manganese stabilizing subunit in Photosystem II Biophys J 86 1807 1812
160. N Tamura G Cheniae 1985 Effects of Photosystem-II extrinsic proteins on microstructure of the oxygen-evolving complex and its reactivity to water analogs Biochim Biophys Acta 809 245 259
161. S Tanaka K Wada 1988 The status of cysteine residues in the extrinsic 33 kDa protein of spinach Photosystem-II complexes Photosynth Res 17 255 266
162. S Tanaka Y Kawata K Wada K Hamaguchi 1989 Extrinsic 33-kilodalton protein of spinach oxygen-evolving complexes: Kinetic studies of folding and disulfide reduction Biochemistry 28 7188 7193
163. Theg SM, Shi L-X (2005) Protein transport and post translational processing in Photosystem II biosynthesis and homeostasis. In: Wydrzynski T, Satoh K (eds) Photosystem II the light-driven water: Plastoquinone oxidoreductase, vol 22. Springer, Dordrecht, pp 669-682
164. LE Thornton H Ohkawa JL Roose Y Kashino N Keren HB Pakrasi 2004 Homologs of plant PsbP and PsbQ proteins are necessary for regulation of Photosystem II activity in the cyanobacterium synechopystis 6803 Plant Cell 16 2164 2175
165. A Tohri T Suzuki S Okuyama K Kamino A Motoki M Hirano H Ohta JR Shen Y Yamamoto I Enami 2002 Comparison of the structure of the extrinsic 33 kDa protein from different organisms Plant Cell Physiol 43 429 439
166. B van den Burg VGH Eijsink 2002 Selection of mutations for increased protein stability Curr Opin Biotechnol 13 333 337
167. C Vieille GJ Zeikus 2001 Hyperthermophilic enzymes: Sources, uses, and molecular mechanisms for thermostability Microbiol Mol Biol Rev 65 1 43
168. R Wales BJ Newman D Pappin JC Gray 1989 The extrinsic 33 kDa polypeptide 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
169. PH Weinreb WG Zhen AW Poon KA Conway PT Lansbury 1996 Nacp, a protein implicated in alzheimer's disease and learning, is natively unfolded Biochemistry 35 13709 13715
170. AK Williamson JR Liggins W Hillier T Wydrzynski 2007 The importance of protein-protein interactions for optimising oxygen activity in Photosystem II: Reconstitution with a recombinant thioredoxin-manganese stabilising protein Photosynth Res 92 305 314
171. Witt HT (2005) Photosystem II: Structural elements, the first 3D crystal structure and functional implications. In: Wydrzynski T, Satoh K (eds) Photosystem II the light-driven water: Plastoquinone oxidoreductase, vol 22. Springer, Dordrecht, pp 425-447
172. Wydrzynski T, Satoh K (2006) Photosystem II, the light driven water:Plastoquinone oxidoreductase. Springer, Dordrecht
173. T Wydrzynski W Hillier J Messinger 1996 On the functional significance of substrate accessibility in the photosynthetic water oxidation mechanism Physiol Plantarum 96 342 350
174. T Wydrzynski W Hillier B Conlan 2007 Engineering model proteins for Photosystem II function Photosynth Res 94 225 233
175. AJ Wyman CF Yocum 2005 Structure and activity of the Photosystem II manganese-stabilizing protein: Role of the conserved disulfide bond Photosynth Res 85 359 372
176. Yachandra VK (2005) The catalytic manganese cluster: Organisation of the metal ions. In: Wydrzynski TS, Satoh K (eds) Photosystem II the light-driven water: Plastoquinone oxidoreductase, vol. 22. Springer, Dordrecht, pp 235- 260
177. Y Yamamoto 2001 Quality control of Photosystem II Plant Cell Physiol 42 121 128
178. 2-evolving Photosystem-2 preparation by tris treatment FEBS Lett 133 265 268
179. Y Yamamoto Y Ishikawa E Nakatani M Yamada HM Zhang T Wydrzynski 1998 Role of an extrinsic 33 kilodalton protein of Photosystem II in the turnover of the reaction center-binding protein D1 during photoinhibition Biochemistry 37 1565 1574
180. T Yamaoka K Satoh S Katoh 1978 Photosynthetic activities of a thermophilic blue-green-alga Plant Cell Physiol 19 943 954
181. 4Ca cluster Science 314 821 825
182. XP Yi M McChargue S Laborde LK Frankel TM Bricker 2005 The manganese-stabilizing protein is required for Photosystem II assembly/stability and photoautotrophy in higher plants J Biol Chem 280 16170 16174
183. F Zhang JP Gao J Weng CY Tan KC Ruan CH Xu D Jiang 2005 Structural and functional differentiation of three groups of tyrosine residues by acetylation of n-acetylimidazole in manganese stabilizing protein Biochemistry 44 719 725
184. IZ Zubrzycki LK Frankel PS Russo TM Bricker 1998 Hydrodynamic studies on the manganese-stabilizing protein of Photosystem II Biochemistry 37 13553 13558