Structures and functions of the extrinsic proteins of photosystem II from different species

Photosynthesis Research

Volumn 98, Issue 1-3, 2008, Pages 349-363

  Enami, Isao ^a   Okumura, Akinori ^b   Nagao, Ryo ^a   Suzuki, Takehiro ^c   Iwai, Masako ^a   Shen, Jian Ren ^d  

^a TOKYO UNIVERSITY OF SCIENCE   (Japan)

^b NIHON UNIVERSITY   (Japan)

^c Japan Science and Technology Agency   (Japan)

^d OKAYAMA UNIVERSITY   (Japan)

Author keywords

A novel extrinsic protein; Extrinsic proteins; Oxygen evolving complex; Photosystem II; PsbO; PsbP; PsbQ; PsbQ ; PsbU; PsbV

Indexed keywords

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

ALGA; AMINO ACID SEQUENCE; CHEMISTRY; COMPARATIVE STUDY; CYANOBACTERIUM; METABOLISM; MOLECULAR GENETICS; PHOTOSYNTHESIS; PHOTOSYSTEM II; PLANT; PROTEIN CONFORMATION; REVIEW; SPECIES DIFFERENCE;

ALGAE; AMINO ACID SEQUENCE; CYANOBACTERIA; MOLECULAR SEQUENCE DATA; PHOTOSYNTHESIS; PHOTOSYSTEM II PROTEIN COMPLEX; PLANTS; PROTEIN CONFORMATION; SPECIES SPECIFICITY;

BACILLARIOPHYTA; CHLOROPHYTA; CYANOBACTERIA; EMBRYOPHYTA; EUGLENA; RHODOPHYTA;

EID: 57849142823     PISSN: 01668595     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11120-008-9343-9     Document Type: Review

References (108)

1. S Alizadeh R Nechushtai J Barber P Nixon 1994 Nucleotide sequence of the psbE, psbF and trnM genes from the chloroplast genome of Chlamydomonas reinhardtii Biochim Biophys Acta 1188 439 442 10.1016/0005-2728(94)90067-1
2. EV Armbrust JA Berges C Bowler BR Green D Martinez NH Putnam 2004 The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism Science 306 79 86 10.1126/science.1101156
3. I Balint J Bhattacharya A Perelman D Schatz Y Moskovitz N Keren 2006 Inactivation of the extrinsic subunit of photosystem II, PsbU, in Synechococcus PCC 7942 results in elevated resistance to oxidative stress FEBS Lett 580 2117 2122 10.1016/j.febslet.2006.03.020
4. M Bernier R Carpentier 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 10.1016/0014-5793(95)00101-E
5. DA Berthold GT Babcock CF Yocum 1981 A highly resolved, oxygen-evolving photosystem II preparation from spinach thylakoid membranes: EPR and electron-transport properties FEBS Lett 134 231 234 10.1016/0014-5793(81)80608-4
6. SD Betts JR Ross E Pichersky CF Yocum 1997 Mutation Val235Ala weakens binding of the 33-kDa manganese stabilizing protein of Photosystem II to one of two sites Biochemistry 36 4047 4053 10.1021/bi962413b
7. 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 high rates of oxygen evolution activity Biochemistry 37 14230 14236 10.1021/bi981305h
8. Bricker TM, Burnap RL (2007) The extrinsic proteins of photosystem II. In: Wydrzynski TJ, Satoh K (eds) Photosystem II: the light-driven water:plastoquinone oxidoreductase. Springer, Dordrecht, pp 95-120
9. TM Bricker LK Frankel 1987 Use of a monoclonal antibody in structural investigations of the 49-kDa polypeptide of photosystem II Arch Biochem Biophys 256 295 301 10.1016/0003-9861(87)90449-8
10. TM Bricker LK Frankel 2003 Carboxylate groups on the manganese- stabilizing protein are required for efficient binding of the 24 kDa extrinsic protein to photosystem II Biochemistry 42 2056 2061 10.1021/bi020652v
11. TM Bricker WR Odom CB Queirolo 1988 Close association of the 33 kDa extrinsic protein with the apoprotein of CPa1 in photosystem II FEBS Lett 231 111 117 10.1016/0014-5793(88)80713-0
12. 550 binding to Photosystem II Biochim Biophys Acta 1556 92 96 10.1016/S0005-2728(02)00367-5
13. 2 evolution Biochemistry 30 440 446 10.1021/bi00216a020
14. 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 proteins to the Photosystem II reaction center Biochemistry 33 13712 13718 10.1021/bi00250a023
15. J De Las Rivas J Barber 2004 Analysis of the structure of the PsbO protein and its implications Photosynth Res 81 329 343 10.1023/B:PRES. 0000036889.44048.e4
16. C de Vitry J Olive D Drapier M Recouvreur FA Wollman 1989 Posttranslational events leading to the assembly of photosystem II protein complex: a study using photosynthesis mutants from Chlamydomonas reinhardtii J Cell Biol 109 991 1006 10.1083/jcb.109.3.991
17. Debus RJ (2007) The catalytic manganese cluster: protein ligation. In: Wydrzynski TJ, Satoh K (eds) Photosystem II: the light-driven water:plastoquinone oxidoreductase. Springer, Dordrecht, pp 261-284
18. JJ Eaton-Rye N Murata 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 10.1016/S0005-2728(89)80075-1
19. JJ Eaton-Rye JA Shand WS Nicoll 2003 pH-dependent photoautotrophic growth of specific photosystem II mutants lacking lumenal extrinsic polypeptides in Synechocystis PCC 6803 FEBS Lett 543 148 153 10.1016/S0014-5793(03)00432-0
20. I Enami K Satoh S Katoh 1987 Crosslinking between the 33 kDa extrinsic protein and the 47 kDa chlorophyll-carrying protein of the PSII reaction center core complex FEBS Lett 226 161 165 10.1016/0014-5793(87)80571-9
21. I Enami K Kamino JR Shen K Satoh S Katoh 1989 Isolation and characterization of photosystem II complexes which lack light-harvesting chlorophyll a/b proteins but retain three extrinsic proteins related to oxygen evolution from spinach Biochim Biophys Acta 977 33 39 10.1016/S0005-2728(89) 80006-4
22. I Enami T Miyaoka Y Mochizuki JR Shen K Satoh S Katoh 1989 Nearest neighbor relationships among constituent proteins of oxygen-evolving Photosystem II membranes: binding and function of the extrinsic proteins Biochim Biophys Acta 973 35 40 10.1016/S0005-2728(89)80399-8
23. I Enami Y Mochizuki S Takahashi T Kakuno T Horio K Satoh 1990 Evidence from crosslinking for 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
24. I Enami M Kaneko N Kitamura H Koike K Sonoike Y Inoue 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
25. I Enami S Ohta S Mitsuhashi S Takahashi M Ikeuchi S Katoh 1992 Evidence from crosslinking for a close association of the extrinsic 33 kDa protein with the 9.4 kDa subunit of cytochrome b559 and the 4.8 kDa product of psbI gene in oxygen-evolving photosystem II complexes from spinach Plant Cell Physiol 33 291 297
26. I Enami M Kitamura T Tomo Y Isokawa H Ohta S Katoh 1994 Is the primary cause of thermal inactivation of oxygen evolution in spinach PSII membranes release of the extrinsic 33 kDa protein or of Mn? Biochim Biophys Acta 1186 52 58 10.1016/0005-2728(94)90134-1
27. 2+ Biochim Biophys Acta 1185 75 80 10.1016/0005-2728(94)90195-3
28. I Enami H Murayama H Ohta M Kamo K Nakazato JR Shen 1995 Isolation and characterization of a Photosystem II complex from the red alga Cyanidium caldarium: association of cytochrome c-550 and a 12 kDa protein with the complex Biochim Biophys Acta 1232 208 216 10.1016/0005-2728(95)00122-0
29. I Enami A Tohri M Kamo H Ohta JR Shen 1997 Identification of domains on the 43 kDa chlorophyll-carrying protein (CP43) that are shielded from tryptic attack by binding of the extrinsic 33 kDa protein with photosystem II complex Biochim Biophys Acta 1320 17 26 10.1016/S0005-2728(97)00005-4
30. I Enami M Kamo H Ohta S Takahashi T Miura M Kusayanagi 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 10.1074/jbc.273.8.4629
31. 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 10.1021/bi9724624
32. 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 alga and higher plant Plant Cell Physiol 41 1354 1364 10.1093/pcp/pcd069
33. I Enami M Iwai A Akiyama T Suzuki A Okumura T Katoh 2003 Comparison of binding and functional properties of two extrinsic components, Cyt c550 and a 12 kDa protein, in cyanobacterial PSII with those in red algal PSII Plant Cell Physiol 44 820 827 10.1093/pcp/pcg106
34. I Enami T Suzuki O Tada Y Nakada K Nakamura A Tohri 2005 Distribution of the extrinsic proteins as a potential marker for the evolution of photosynthetic oxygen-evolving photosystem II FEBS J 272 5020 5030 10.1111/j.1742-4658.2005. 04912.x
35. KN Ferreira TM Iverson K Maghlaoui J Barber S Iwata 2004 Architecture of the photosynthetic oxygen-evolving center Science 303 1831 1838 10.1126/science.1093087
36. Frankel LK, Bricker TM (1990) Mapping of NHS-biotinylation sites and the epitope of the monoclonal antibody FAC2 on the apoprotein of CPa-1. In: Baltschffsky M (ed) Current research in photosynthesis, vol I. Kluwer Academic Publishers, Dordrecht, pp 639-642
37. LK Frankel TM Bricker 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 Biochemstry 31 11059 11063 10.1021/bi00160a015
38. LK Frankel TM Bricker 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 10.1021/bi00022a024
39. LK Frankel JA Cruz TM Bricker 1999 Carboxylate groups on the manganese-stabilizing protein are required for its efficient binding to photosystem II Biochemistry 38 14275 14278 10.1021/bi991366v
40. C Frazão FJ Enguita R Coelho GM Sheldrick JA Navarro M Hervás 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 10.1007/s007750100208
41. HM Gleiter E Haag JR Shen JJ Eaton-Rye Y Inoue WF Vermaas 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 10.1021/bi00206a008
42. KC Han JR Shen M Ikeuchi Y Inoue 1994 Chemical crosslinking studies of extrinsic proteins in cyanobacterial photosystem II FEBS Lett 355 121 124 10.1016/0014-5793(94)01182-6
43. H Hayashi Y Fujimura PS Mohanty N Murata 1993 The role of CP47 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 10.1007/BF00018073
44. RG Hermann J Alt B Schiller WR Widger WA Cramer 1984 Nucleotide sequence of the gene for apocytochrome b-559 on the spinach plastid chromosome: implications for the structure of the membrane protein FEBS Lett 176 239 244 10.1016/0014-5793(84)80949-7
45. M Ikeuchi Y Inoue 1988 A new photosystem II reaction center component (4.8 kDa protein) encoded by chloroplast genome FEBS Lett 241 99 104 10.1016/0014-5793(88)81039-1
46. N Inoue-Kashino Y Kashino K Satoh I Terashima HB Pakrasi 2005 PsbU provides a stable architecture for the oxygen-evolving system in cyanobacterial photosystem II Biochemistry 44 12214 12228 10.1021/bi047539k
47. S Ishihara A Takabayashi K Ido T Endo K Ifuku F Sato 2007 Distinct functions for the two PsbP-like proteins PPL1 and PPL2 in the chloroplast thylakoid lumen of Arabidopsis Plant Physiol 145 668 679 10.1104/pp. 107.105866
48. Y Ishikawa Y Yamamoto M Otsubo SM Theg N Tamura 2002 Chemical modification of amine groups on PSII protein(s) retards photoassembly of the photosynthetic water-oxidizing complex Biochemstry 41 1972 1980 10.1021/bi0102499
49. Y Isogai Y Yamamoto M Nishimura 1985 Association of the 33 kDa polypeptide with the 43 kDa component in Photosystem II particles FEBS Lett 187 240 244 10.1016/0014-5793(85)81250-3
50. N Kamiya JR Shen 2003 Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-Å resolution Proc Natl Acad Sci USA 100 98 103 10.1073/pnas.0135651100
51. Y Kashino WM Lauber JA Carroll Q Wang J Whitmarsh K Satoh 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 10.1021/bi026012+
52. Y Kashino T Takahashi N Inoue-Kashino A Ban Y Ikeda K Satoh 2007 Ycf12 is a core subunit in the photosystem II complex Biochim Biophys Acta 1767 1269 1275 10.1016/j.bbabio.2007.08.008
53. CA Kerfeld MR Sawaya H Bottin KT Tran M Sugiura D Cascio 2003 Structural and EPR characterization of the soluble form of Cytochrome c-550 and of the psbV2 gene product from the cyanobacterium Thermosynechococcus elongatus Plant Cell Physiol 44 697 706 10.1093/pcp/pcg084
54. 2 evolution Biochim Biophys Acta 807 64 73 10.1016/0005-2728(85)90053-2
55. T Kuwabara N Murata 1982 Inactivation of photosynthetic oxygen evolution and concomitant release of three polypeptides in the photosystem II particles of spinach chloroplasts Plant Cell Physiol 23 533 539
56. 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 10.1021/bi9522615
57. 550 in Synechocystis sp. PCC6803 Biochemistry 40 10350 10359 10.1021/bi0100135
58. B Loll J Kern W Saenger A Zouni J Biesiadka 2005 Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II Nature 438 1040 1044 10.1038/nature04224
59. N Lydakis-Simantiris SD Betts CF Yocum 1999 Leucine245 is a critical residue for folding and function of the manganese-stabilizing protein of Photosystem II Biochemistry 38 15528 15535 10.1021/bi991599m
60. 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 10.1021/bi981847z
61. SP Mayfield M Schirmer-Rahire G Frank H Zuber JD Rochaix 1989 Analysis of the genes of the OEE1 and OEE3 proteins of the photosystem II complex from Chlamydomonas reinhardtii Plant Mol Biol 12 683 693 10.1007/BF00044159
62. R Mei JP Green RT Sayre WD Frasch 1989 Manganese-binding proteins of the oxygen-evolving complex Biochemstry 28 5560 5567 10.1021/bi00439a033
63. 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
64. T Miura JR Shen S Takahashi M Kamo E Nakamura H Ohta 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 10.1074/jbc.272.10.6128
65. M Miyao N Murata 1989 The mode of binding of three extrinsic proteins of 33 kDa, 23 kDa and 18 kDa in photosystem II complex of spinach Biochim Biophys Acta 977 315 321 10.1016/S0005-2728(89)80086-6
66. A Motoki T Shimazu M Hirano S Katoh 1998 Two regions of the Mn-stabilizing protein from Synechococcus elongatus that are involved in binding to photosystem II complexes Biochim Biophys Acta 1365 492 502 10.1016/S0005-2728(98)00102-9
67. 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 10.1074/jbc.M100766200
68. F Müh T Renger A Zouni 2008 Crystal structure of cyanobacterial photosystem II at 3.0 Å resolution: a closer look at the antenna system and the small membrane-intrinsic subunits Plant Physiol Biochem 46 238 264 10.1016/j.plaphy.2008.01.003
69. 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 chloroplast Biochim Biophys Acta 765 363 369 10.1016/0005-2728(84)90177-4
70. R Nagao A Ishii O Tada T Suzuki N Dohmae A Okumura 2007 Isolation and characterization of oxygen-evolving thylakoid membranes and Photosystem II particles from a marine diatom Chaetoceros gracilis Biochim Biophys Acta 1767 1353 1362 10.1016/j.bbabio.2007.10.007
71. Y Nishiyama H Hayashi T Watanabe N Murata 1994 Photosynthetic oxygen evolution is stabilized by cytochrome c550 against heat inactivation in Synechococcus sp PCC 7002 Plant Physiol 105 1313 1319 10.1104/pp. 105.4.1313
72. Y Nishiyama DA Los N Murata 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 10.1104/pp. 120.1.301
73. WR Odom TM Bricker 1992 Interaction of CPa-1 with the manganese-stabilizing protein of Photosystem II: Identification of domains crosslinked by 1-ethyl-3-(3-dimethylaminopropyl)-carbodiimide Biochemistry 31 5616 5620 10.1021/bi00139a027
74. Ohta H, Yoshida N, Sano M, Hirano M, Nakazato K, Enami I (1995) Evidence for electrostatic interaction of the loop A on CP47 with the extrinsic 33 kDa protein. In: Mathis P (ed) Photosynthesis: from light to biosphere, vol II. Kluwer Academic Publishers, Dordrecht, pp 361-364
75. H Ohta T Suzuki M Ueno A Okumura S Yoshihara JR Shen 2003 Extrinsic proteins of photosystem II: an intermediate member of PsbQ protein family in red algal PS II Eur J Biochem 270 4156 4163 10.1046/j.1432-1033.2003.03810.x
76. A Okumura H Ohta Y Inoue I Enami 2001 Identification of functional domains of the extrinsic 12 kDa protein in red algal PSII by limited proteolysis and directed mutagenesis Plant Cell Physiol 42 1331 1337 10.1093/pcp/pce170
77. A Okumura M Sano T Suzuki H Tanaka R Nagao K Nakazato 2007 Aromatic structure of tyrosine-92 in the extrinsic PsbU protein of red algal photosystem II is important for its functioning FEBS Lett 581 5255 5258
78. 2-washed Photosystem II particles depleted of 33, 24, and 16 kDa polypeptides FEBS Lett 168 281 286 10.1016/0014-5793(84)80263-X
79. MP Oudot-Le Secq J Grimwood H Shapiro EV Armbrust C Bowler BR Green 2007 Chloroplast genomes of the diatoms Phaeodactylum tricornutum and Thalassiosira pseudonana: comparison with other plastid genomes of the red lineage Mol Genet Genomics 277 427 439 10.1007/s00438-006-0199-4
80. 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 10.1021/bi020228u
81. H Popelkova A Wyman CF Yocum 2003 Amino acid sequences and solution structures of manganese stabilizing protein that affect reconstitution of photosystem II activity Photosynth Res 77 21 34 10.1023/A:1024970926655
82. 384, 385G leads to a defect associated with the oxygen-evolving complex Biochemistry 31 11482 11488 10.1021/bi00161a029
83. 444R Biochemistry 35 4046 4053 10.1021/bi952661s
84. 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 10.1073/pnas.0609337104
85. JL Roose KM Wegener HB Pakrasi 2007 The extrinsic proteins of photosystem II Photosynth Res 92 369 387 10.1007/s11120-006-9117-1
86. 6 from the cyanobacterium Arthrospira maxima Biochemistry 40 9215 9225 10.1021/bi002679p
87. A Seidler 1994 Introduction of a histidine tail at the N-terminus of a secretory protein expressed in E. coli Protein Eng 7 1277 1280 10.1093/protein/7.10.1277
88. A Seidler 1996 The extrinsic polypeptides of photosystem II Biochim Biophys Acta 1277 35 60 10.1016/S0005-2728(96)00102-8
89. JR Shen Y Inoue 1993 Binding and functional properties of two new extrinsic components, cytochrome c-550 and a 12 kDa protein, in cyanobacterial photosystem II Biochemistry 32 1825 1832 10.1021/bi00058a017
90. JR Shen Y Inoue 1993 Cellular localization of cytochrome c-550. Its specific association with cyanobacterial photosystem II J Biol Chem 268 20408 20413
91. JR Shen M Ikeuchi Y Inoue 1992 Stoichiometric association of extrinsic cytochrome c550 and 12 kDa protein with a highly purified oxygen-evolving photosystem II core complex from Synechococcus vulcanus FEBS Lett 301 145 149 10.1016/0014-5793(92)81235-E
92. JR Shen RL Burnap Y Inoue 1995 An independent role of cytochrome c-550 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 10.1021/bi00039a023
93. JR Shen W Vermaas Y Inoue 1995 The role of cytochrome c-550 as studied through reverse genetics and mutant characterization in Synechocystis sp. PCC 6803 J Biol Chem 270 6901 6907 10.1074/jbc.270.12.6901
94. JR Shen M Ikeuchi Y Inoue 1997 Analysis of the psbU gene encoding the 12 kDa extrinsic protein of photosystem II and studies on its role by deletion mutagenesis in Synechocystis sp. PCC 6803 J Biol Chem 272 17821 17826 10.1074/jbc.272.28.17821
95. JR Shen M Qian Y Inoue RL Burnap 1998 Functional characterization of Synechocystis sp. PCC 6803 ΔpsbU and ΔpsbV mutants reveals important roles of cytochrome c-550 in cyanobacterial PSII Biochemistry 37 1551 1558 10.1021/bi971676i
96. Shen JR, Henmi T, Kamiya N (2008) Structure and function of photosystem II. In: Fromme F (ed) Photosynthetic protein complexes, a structural approach. Wiley-VCH, Weinheim
97. Y Shigemori J Inagaki H Mori M Nishimura S Takahashi Y Yamamoto 1994 The presequence of the precursor to the nucleus-encoded 30 kDa protein of photosystem II in Euglena gracilis Z induces two hydrophobic domains Plant Mol Biol 24 209 215 10.1007/BF00040587
98. TC Summerfield JA Shand FK Bentley JJ Eaton-Rye 2005 PsbQ (Sll1638) in Synechocystis sp. PCC 6803 is required for photosystem II activity in specific mutants and in nutrient-limiting conditions Biochemistry 44 805 815 10.1021/bi048394k
99. T Suzuki J Minagawa T Tomo K Sonoike H Ohta I Enami 2003 Binding and functional properties of the extrinsic proteins in oxygen-evolving photosystem II particle from a green alga, Chlamydomonas reinhardtii having his-tagged CP47 Plant Cell Physiol 44 76 84 10.1093/pcp/pcg010
100. T Suzuki O Tada M Makimura A Tohri H Ohta Y Yamamoto 2004 Isolation and characterization of oxygen-evolving photosystem II complexes retaining the PsbO, P and Q proteins from Euglena gracilis Plant Cell Physiol 45 1168 1175 10.1093/pcp/pch131
101. 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 10.1007/s11120-004-7760-y
102. 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 Synechocystis 6803 Plant Cell 16 2164 2175 10.1105/tpc.104.023515
103. A Tohri T Suzuki S Okuyama K Kamino A Motoki M Hirano 2002 Comparison of the structure of the extrinsic 33 kDa protein from different organisms Plant Cell Physiol 43 429 439 10.1093/pcp/pcf053
104. A Tohri N Dohmae T Suzuki H Ohta Y Inoue I Enami 2004 Identification of domains on the extrinsic 23 kDa protein possibly involved in electrostatic interaction with the extrinsic 33 kDa protein in spinach photosystem II Eur J Biochem 271 962 971 10.1111/j.1432-1033.2004.03998.x
105. A Tyagi J Hermans J Steppuhn C Jansson F Vater RG Herrmann 1987 Nucleotide sequence of cDNA clones encoding the complete "33 kDa" precursor protein associated with the photosynthetic oxygen-evolving complex from spinach Mol Gen Genet 207 288 293 10.1007/BF00331591
106. J Veerman FK Bentley JJ Eaton-Rye CW Mullineaux S Vasil'ev D Bruce 2005 The PsbU subunit of photosystem II stabilizes energy transfer and primary photochemistry in the phycobilisome-photosystem II assembly of Synechocystis sp PCC 6803 Biochemistry 44 16939 16948 10.1021/bi051137a
107. Whitmarsh J, Pakrasi HB (1996) Form and function of cytochrome b559. In: Ort DR, Yocum CF (eds) Photosynthesis: the light reactions. Kluwer Academic Publishers, Dordrecht, pp 249-264
108. 2-evolving photosystem-2 preparation by Tris treatment FEBS Lett 133 265 268 10.1016/0014-5793(81)80520-0