The lipoproteins of cyanobacterial photosystem II

Journal of Photochemistry and Photobiology B: Biology

Volumn 104, Issue 1-2, 2011, Pages 191-203

  Fagerlund, Robert D ^a   Eaton Rye, Julian J ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

Cyanobacteria; CyanoP; CyanoQ; Lipoproteins; Photosystem II; Psb27

Indexed keywords

ALGAL PROTEIN; CALCIUM; CC 9605; CHLORIDE; CYANOQ PROTEIN; CYSTEINE; GENE PRODUCT; HYDROXYLAMINE; IRON; LIPOPROTEIN; PLASTOQUINONE; POLYPEPTIDE; PROTEIN PSB 27; PSBO PROTEIN; PSBV PROTEIN; TRYPSIN; UNCLASSIFIED DRUG; WH 8102; WH 8109; ZINC ION;

ARABIDOPSIS; ARTHROSPIRA MAXIMA; CLADISTICS; CYANOBACTERIUM; DNA BINDING MOTIF; ENZYME METABOLISM; ESCHERICHIA COLI; GENE DELETION; GLOEOBACTER VIOLACEUS; HYDROPHILICITY; HYDROPHOBICITY; MASS SPECTROMETRY; MOLECULAR DOCKING; MOLECULAR INTERACTION; NONHUMAN; NUCLEOTIDE SEQUENCE; OXYGEN EVOLUTION; PHOTOSYSTEM II; PHYLOGENY; PRIORITY JOURNAL; PROCHLOROCOCCUS; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; REVIEW; SPINACH; SYNECHOCOCCUS; SYNECHOCOCCUS ELONGATUS; SYNECHOCYSTIS; THYLAKOID; THYLAKOID MEMBRANE; TOBACCO; UNINDEXED SEQUENCE; WILD TYPE;

BACTERIAL PROTEINS; CYANOBACTERIA; LIPOPROTEINS; PHOTOSYSTEM II PROTEIN COMPLEX; PROTEIN SUBUNITS; THYLAKOIDS;

CHLOROPHYTA; CYANOBACTERIA; EMBRYOPHYTA; PROCHLOROCOCCUS; SYNECHOCYSTIS SP. PCC 6803;

EID: 79958010013     PISSN: 10111344     EISSN: 18732682     Source Type: Journal    
DOI: 10.1016/j.jphotobiol.2011.01.022     Document Type: Review

References (89)

1. G. Renger, and T. Renger Photosystem II: the machinery of photosynthetic water splitting Photosyth. Res. 98 2008 53 80 (Pubitemid 50289510)
2. A. Guskov, A. Gabdulkhakov, M. Broser, C. Glöckner, J. Hellmich, J. Kern, J. Frank, F. Müh, W. Saenger, and A. Zouni Recent progress in the crystallographic studies of photosystem II ChemPhysChem 11 2010 1160 1171
3. P.J. Nixon, F. Michoux, J. Yu, M. Boehm, and J. Komenda Recent advances in understanding the assembly and repair of photosystem II Ann. Bot. 106 2010 1 16
4. Y. Kashino, W.M. Lauber, J.A. Carroll, Q. Wang, J. Whitmarsh, K. Satoh, and H.B. Pakrasi Proteomic analysis of a highly active photosystem II preparation from the cyanobacterium Synechocystis sp. PCC 6803 reveals the presence of novel polypeptides Biochemistry 41 2002 8004 8012 (Pubitemid 34655167)
5. J. Kern, and G. Renger Photosystem II: structure and mechanism of the water:plastoquinone oxidoreductase Photosynth. Res. 94 2007 183 202 (Pubitemid 350229101)
6. N. Kamiya, and J.-R. Shen Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7 resolution Proc. Natl. Acad. Sci. USA 100 2003 98 103 (Pubitemid 36078036)
7. K.N. Ferreira, T.M. Iverson, K. Maghlaoui, J. Barber, and S. Iwata Architecture of the photosynthetic oxygen-evolving center Science 303 2004 1831 1838 (Pubitemid 38374869)
8. B. Loll, J. Kern, W. Saenger, A. Zouni, and J. Biesiadka Towards complete cofactor arrangement in the 3.0 resolution structure of photosystem II Nature 438 2005 1040 1044 (Pubitemid 43093979)
9. A. Guskov, J. Kern, A. Gabdulkhakov, M. Broser, A. Zouni, and W. Saenger Cyanobacterial photosystem II at 2.9- resolution and the role of quinones, lipids, channels and chloride Nat. Struct. Mol. Biol. 16 2009 334 342
10. J. Nield, E.V. Orlova, E.P. Morris, B. Gowen, M. van Heel, and J. Barber 3D map of the plant photosystem II supercomplex obtained by cryoelectron microscopy and single particle analysis Nat. Struct. Biol. 7 2000 44 47 (Pubitemid 30043247)
11. J. Nield, and J. Barber Refinement of the structural model of the photosystem II supercomplex of higher plants Biochim. Biophys. Acta 1757 2006 353 361 (Pubitemid 43993853)
12. I. Enami, A. Okumura, R. Nagao, T. Suzuki, M. Iwai, and J.-R. Shen Structures and functions of the extrinsic proteins of photosystem II from different species Photosynth. Res. 98 2008 349 363 (Pubitemid 50247998)
13. R. Nagao, T. Suzuki, A. Okumura, A. Niikura, M. Iwai, N. Dohmae, T. Tomo, J.-R. Shen, M. Ikeuchi, and I. Enami Topological analysis of the extrinsic PsbO, PsbP and PsbQ proteins in a green algal PSII complex by cross-linking with a water-soluble carbodiimide Plant Cell Physiol. 51 2010 718 727
14. J.L. Roose, K.M. Wegener, and H.B. Pakrasi The extrinsic proteins of photosystem II Photosynth. Res. 92 2007 369 387 (Pubitemid 47246537)
15. J. De Las Rivas, M. Balsera, and J. Barber Evolution of oxygenic photosynthesis: genome-wide analysis of the OEC extrinsic proteins Trends Plant Sci. 9 2004 18 25 (Pubitemid 38157642)
16. L.E. Thornton, H. Ohkawa, J.L. Roose, Y. Kashino, N. Keren, and H.B. Pakrasi Homologs of plant PsbP and PsbQ proteins are necessary for regulation of photosystem II activity in the cyanobacterium Synechocystis 6803 Plant Cell 16 2004 2164 2175 (Pubitemid 39059735)
17. K.U. Cormann, J.-A. Bangert, M. Ikeuchi, M. Rögner, R. Stoll, and M.M. Nowaczyk Structure of Psb27 in solution: implications for transient binding to photosystem II during biogenesis and repair Biochemistry 48 2009 8768 8770
18. P.D. Mabbitt, G.J.P. Rautureau, C.L. Day, S.M. Wilbanks, J.J. Eaton-Rye, and M.G. Hinds Solution structure of Psb27 from cyanobacterial photosystem II Biochemistry 48 2009 8771 8773
19. S.A. Jackson, R.D. Fagerlund, S.M. Wilbanks, and J.J. Eaton-Rye Crystal Structure of PsbQ from Synechocystis sp. PCC 6803 at 1.8 : Implications for binding and function in cyanobacterial photosystem II Biochemistry 49 2010 2765 2767
20. F. Michoux, K. Takasaka, M. Boehm, P.J. Nixon, and J.W. Murray Structure of CyanoP at 2.8 : implications for the evolution and function of the PsbP subunit of photosystem II Biochemistry 49 2010 7411 7413
21. A.S. Juncker, H. Willenbrock, G. von Heijne, S. Brunak, H. Nielsen, and A. Krogh Prediction of lipoprotein signal peptides in Gram-negative bacteria Protein Sci. 12 2003 1652 1662 (Pubitemid 36910046)
22. J.D. Bendtsen, H. Nielsen, G. von Heijne, and S. Brunak Improved prediction of signal peptides: signalP 3.0 J. Mol. Biol. 340 2004 783 795 (Pubitemid 38829638)
23. T. Ujihara, I. Sakurai, N. Mizusawa, and H. Wada A method for analyzing lipid-modified proteins with mass spectrometry Anal. Biochem. 374 2008 429 431
24. T. Yamashita, and W.L. Butler Photooxidtion by photosystem II of tris-washed chloroplasts Plant Physiol. 44 1969 1342 1346
25. Y. Kashino, N. Inoue-Kashino, J.L. Roose, and H.B. Pakrasi Absence of the PsbQ protein results in destabilization of the PsbV protein and decreased oxygen evolution activity in cyanobacterial photosystem II J. Biol. Chem. 281 2006 20834 20841 (Pubitemid 44121125)
26. T.C. Summerfield, J.A. Shand, F.K. Bentley, and J.J. Eaton-Rye PsbQ (Sll1638) in Synechocystis sp. PCC 6803 is required for photosystem II activity in specific mutants and in nutrient-limiting conditions Biochemistry 44 2005 805 815 (Pubitemid 40105513)
27. J.J. Eaton-Rye, J.A. Shand, and W.S. Nicoll pH-dependent photoautotrophic growth of specific photosystem II mutants lacking lumenal extrinsic polypeptides in Synechocystis PCC 6803 FEBS Lett. 543 2003 148 153 (Pubitemid 36577245)
28. J.J. Eaton-Rye Requirements for different combinations of the extrinsic proteins in specific cyanobacterial photosystem II mutants Photosynth. Res. 84 2005 275 281 (Pubitemid 41110658)
29. T.C. Summerfield, J.J. Eaton-Rye, and L.A. Sherman Global gene expression of a ΔPsbO:ΔPsbU mutant and a spontaneous revertant in the cyanobacterium Synechocystis sp. strain PCC 6803 Photosynth. Res. 94 2007 265 274 (Pubitemid 50001828)
30. J.J. Eaton-Rye, and W.F.J. Vermaas Oligonucleotide-directed mutagenesis of psbB, the gene encoding CP47, employing a deletion strain of the cyanobacterium Synechocystis sp. PCC 6803 Plant Mol. Biol. 17 1991 1165 1177
31. T.R. Morgan, J.A. Shand, S.M. Clarke, and J.J. Eaton-Rye 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 1998 14437 14449 (Pubitemid 28489050)
32. J.L. Roose, Y. Kashino, and H.B. Pakrasi The PsbQ protein defines cyanobacterial photosystem II complexes with highest activity and stability Proc. Natl. Acad. Sci. USA 104 2007 2548 2553 (Pubitemid 46391433)
33. J.-R. Shen, W. Vermaas, and Y. Inoue The role of cytochrome c-550 as studied through reverse genetics and mutant characterization in Synechocystis sp. PCC 6803 J. Biol. Chem. 270 1995 6901 6907
34. J.-R. Shen, M. Qian, Y. Inoue, and R.L. Burnap Functional characterization of Synechocystis sp. PCC 6803 ΔpsbU and ΔpsbV mutants reveals important roles of cytochrome c-550 in cyanobacterial oxygen evolution Biochemistry 37 1998 1551 1558 (Pubitemid 28093670)
35. 550 of photosystem II in Synechocystis sp. PCC6803 Biochemistry 43 2004 14161 14170 (Pubitemid 39482766)
36. T.M. Bricker, J. Morvant, N. Masri, H.M. Sutton, and L.K. Frankel Isolation of a highly active photosystem II preparation from Synechocystis 6803 using a histidine-tagged mutant of CP 47 Biochimica. Biophys. Acta 1409 1998 50 57 (Pubitemid 28511112)
37. S. Guindon, and O. Gascuel A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood System. Biol. 52 2003 696 704 (Pubitemid 37365050)
38. J.P. Huelsenbeck, and F. Ronquist MRBAYES: Bayesian inference of phylogenetic trees Bioinformatics 17 2001 754 755 (Pubitemid 32851390)
39. F. Ronquist, and J.P. Huelsenbeck MrBayes 3: Bayesian phylogenetic inference under mixed models Bioinformatics 19 2003 1572 1574 (Pubitemid 37038874)
40. K. Ifuku, S. Ishihara, and F. Sato Molecular functions of oxygen-evolving complex family proteins in photosynthetic electron flow J. Integr. Plant Biol. 52 2010 723 734
41. S. Yabuta, K. Ifuku, A. Takabayashi, S. Ishihara, K. Ido, N. Ishikawa, T. Endo, and F. Sato Three PsbQ-like proteins are required for the function of the chloroplast NAD(P)H dehydrogenase complex in Arabidopsis Plant Cell Physiol. 51 2010 866 876
42. V. Calderone, M. Trabucco, A. Vujicic, R. Battistutta, and G.M. Giacometti Crystal structure of the PsbQ protein of photosystem II from higher plants EMBO Rep. 4 2003 900 905 (Pubitemid 37304408)
43. M. Balsera, J.B. Arellano, J.L. Revuelta, J. De Las Rivas, and J.A. Hermoso The 1.49 resolution crystal structure of PsbQ from photosystem II of Spinacia oleracea reveals a PPII structure in the N-terminal region J. Mol. Biol. 350 2005 1051 1060 (Pubitemid 40943461)
44. T. Kuwabara, T. Murata, M. Miyao, and N. Murata Partial degradation of the 18-kDa protein of the photosynthetic oxygen-evolving complex: a study of a binding site Biochim. Biophys. Acta 850 1986 146 155
45. J. Dundas, Z. Ouyang, J. Tseng, A. Binkowski, Y. Turpaz, and J. Liang CASTp: computed atlas of surface topography of proteins with structural and topographical mapping of functionally annotated residues Nucl. Acids Res. 34 2006 W116 W118
46. D. Kozakov, D.R. Hall, D. Beglov, R. Brenke, S.R. Comeau, Y. Shen, K. Li, J. Zheng, P. Vakili, I.C. Paschalidis, and S. Vajda Achieving reliability and high accuracy in automated protein docking: Cluspro, PIPER, SDU, and stability analysis in CAPRI rounds 13-19 Proteins 78 2010 3124 3130
47. E. Krissinel, and K. Henrick Inference of macromolecular assemblies from crystalline state J. Mol. Biol. 372 2007 774 797 (Pubitemid 47321791)
48. H.M. Gleiter, E. Haag, J.-R. Shen, J.J. Eaton-Rye, Y. Inoue, W.F.J. Vermaas, and G. Renger Functional characterization of mutant strains of the cyanobacterium Synechocystis sp. PCC 6803 lacking short domains within the large, lumen-exposed loop of the chlorophyll protein CP47 in photosystem II Biochemistry 33 1994 12063 12071 (Pubitemid 24328021)
49. M. Qian, S.F. Al-Khaldi, C. Putnam-Evans, T.M. Bricker, and R.L. Burnap Photoassembly of the photosystem II (Mn)4 cluster in site-directed mutants impaired in the binding of the manganese-stabilizing protein Biochemistry 36 1997 15244 15252 (Pubitemid 27527989)
50. J.-R. Shen, R.L. Burnap, and Y. Inoue 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 1995 12661 12668
51. S. Ishihara, A. Takabayashi, K. Ido, T. Endo, K. Ifuku, and F. Sato Distinct functions for the two PsbP-like proteins PPL1 and PPL2 in the chloroplast thylakoid lumen of Arabidopsis Plant Physiol. 145 2007 668 679 (Pubitemid 350127601)
52. Y. Ishikawa, W.P. Schroder, and C. Funk Functional analysis of the PsbP-like protein (sll1418) in Synechocystis sp. PCC 6803 Photosynth. Res. 84 2005 257 262 (Pubitemid 41110656)
53. T.C. Summerfield, R.T. Winter, and J.J. Eaton-Rye Investigation of a requirement for the PsbP-like protein in Synechocystis sp. PCC 6803 Photosynth. Res. 84 2005 263 268 (Pubitemid 41114772)
54. J.-R. Shen, and Y. Inoue Binding and functional properties of two new extrinsic components, cytochrome c-550 and a 12-kDa protein In cyanobacterial photosystem II, Biochemistry 32 1993 1825 1832 (Pubitemid 23066457)
55. D. Sveshnikov, C. Funk, and W.P. Schröder The PsbP-like protein (sll1418) of Synechocystis sp. PCC 6803 stabilises the donor side of Photosystem II Photosynth. Res. 93 2007 101 109 (Pubitemid 47310289)
56. P. Joliot Modulated light source use with the oxygen electrode Meth. Enzymol. 24 1972 123 134
57. N. Sato Phylogenomic and structural modeling analyses of the PsbP superfamily reveal multiple small segment additions in the evolution of photosystem II-associated PsbP protein in green plants Mol. Phylogenet. Evol. 56 2010 176 186
58. K. Ifuku, T. Nakatsu, H. Kato, and F. Sato Crystal structure of the PsbP protein of photosystem II from Nicotiana tabacum EMBO Rep. 5 2004 362 367 (Pubitemid 38618277)
59. J. Kohoutová, I. Kutá Smatanová, J. Brynda, M. Lapkouski, J.L. Revuelta, J.B. Arellano, and R. Ettrich Crystallization and preliminary crystallographic characterization of the extrinsic PsbP protein of photosystem II from Spinacia oleracea Acta Cryst. F65 2009 111 115
60. K. Ifuku, and F. Sato Importance of the N-terminal sequence of the extrinsic 23 kDa polypeptide in photosystem II in ion retention in oxygen evolution Biochim. Biophys. Acta 1546 2001 196 204 (Pubitemid 32217816)
61. 2+ retention in photosystem II Plant Cell Physiol. 43 2002 1244 1249 (Pubitemid 35337220)
62. N. Bondarava, S. Un, and A. Krieger-Liszkay Manganese binding to the 23 kDa extrinsic protein of photosystem II Biochim. Biophys. Acta 1776 2007 583 588 (Pubitemid 46863352)
63. K.G. Tina, R. Bhadra, and N. Srinivasan PIC: protein interactions calculator Nucl. Acids Res. 35 2007 W473 W476
64. 559 of photosystem II Biochim. Biophys. Acta 1367 1998 63 87 (Pubitemid 28451585)
65. M. Ikeuchi, Y. Inoue, and W. Vermaas P. Mathis, Photosynthesis: From Light to Biosphere 1995 Kluwer Academic Publishers Dordrecht 297 300
66. M.M. Nowaczyk, R. Hebeler, E. Schlodder, H.E. Meyer, B. Warscheid, and M. Rögner Psb27, a cyanobacterial lipoprotein, is involved in the repair cycle of photosystem II Plant Cell 18 2006 3121 3131 (Pubitemid 46013280)
67. J.L. Roose, and H.B. Pakrasi Evidence that D1 processing is required for manganese binding and extrinsic protein assembly into photosystem II J. Biol. Chem. 279 2004 45417 45422 (Pubitemid 39491525)
68. K. Satoh, and Y. Yamamoto The carboxyl-terminal processing of precursor D1 protein of the photosystem II reaction center Photosynth. Res. 94 2007 203 215 (Pubitemid 350229097)
69. F. Mamedov, M.M. Nowaczyk, A. Thapper, M. Rögner, and S. Styring Functional characterization of monomeric photosystem II core preparations from Thermosynechococcus elongatus with or without the Psb27 protein Biochemistry 46 2007 5542 5551 (Pubitemid 46729194)
70. W.F.J. Vermass, A.W. Rutherford, and Ö. Hansson Site-directed mutagenesis in photosystem II of the cyanobacterium Synechocystis sp. PCC 6803: donor D is a tyrosine residue in the D2 protein Proc. Natl. Acad. Sci. USA 85 1988 8477 8481
71. A.W. Rutherford, A. Boussac, and P. Faller The stable tyrosyl radical in photosystem II: why D? Biochim. Biophys. Acta 1655 2004 222 230 (Pubitemid 38526183)
72. J.L. Roose, and H.B. Pakrasi The Psb27 protein facilitates manganese cluster assembly in photosystem II J. Biol. Chem. 283 2008 4044 4050
73. F.K. Bentley, H. Luo, P. Dilbeck, R.L. Burnap, and J.J. Eaton-Rye Effects of inactivating psbM and psbT on photodamage and assembly of photosystem II in Synechocystis sp. PCC 6803 Biochemistry 47 2008 11637 11646
74. G.M. Cheniae, and I.F. Martin Effects of hydroxylamine on photosystem II. I. Factors affecting the decay of oxygen evolution Plant Physiol. 47 1971 568 575
75. 2 evolution I. Biochemical and kinetic aspects, Biochim. Biophys. Acta 253 1971 167 181
76. 2 evolution Plant Physiol. 50 1972 87 94
77. 2O oxidation complex in Synechocystis sp. PCC6803 Biochemistry 35 1996 874 882
78. H. Chen, D. Zhang, J. Guo, H. Wu, M. Jin, Q. Lu, C. Lu, and L. Zhang A Psb27 homologue in Arabidopsis thaliana is required for efficient repair of photodamaged photosystem II Plant Mol. Biol. 61 2006 567 575 (Pubitemid 44172764)
79. 559 subunit from transplastomic tobacco plants Biochim. Biophys. Acta 1777 2008 1501 1509
80. L. Wei, J. Guo, M. Ouyang, X. Sun, J. Ma, W. Chi, C. Lu, and L. Zhang LPA19, a Psb27 homolog in Arabidopsis thaliana, facilitates D1 protein precursor processing during PSII biogenesis J. Biol. Chem. 285 2010 21391 21398
81. J.B. Peltier, O. Emanuelsson, D.E. Kalume, J. Ytterberg, G. Friso, A. Rudella, D.A. Liberles, L. Soderberg, P. Roepstorff, G. von Heijne, and K.J. van Wijk Central functions of the lumenal and peripheral thylakoid proteome of Arabidopsis determined by experimentation and genome-wide prediction Plant Cell 14 2002 211 236 (Pubitemid 34140408)
82. D.W. Ritchie Evaluation of protein docking predictions using Hex 3.1 in CAPRI rounds 1 and 2 Proteins 52 2003 98 106 (Pubitemid 36648857)
83. D. Schneidman-Duhovny, Y. Inbar, R. Nussinov, and H.J. Wolfson PatchDock and SymmDock: servers for rigid and symmetric docking Nucl. Acids Res. 33 2005 W363 W367
84. M.F. Lensink, and S.J. Wodak Docking and scoring protein interactions: CAPRI 2009 Proteins 78 2010 3073 3084
85. T.M. Bricker, and L.K. Frankel The structure and function of the 33 kDa extrinsic protein of photosystem II: a critical assessment Photosynth. Res. 56 1998 157 173 (Pubitemid 28381938)
86. E.J. Boekema, J.F.L. van Breemen, H. van Roon, and J.P. Dekker Conformational changes in photosystem II supercomplexes upon removal of extrinsic subunits Biochemistry 39 2000 12907 12915
87. H. Popelkova, A. Commet, and C.F. Yocum Asp157 is required for the function of PsbO, the photosystem II manganese-stabilizing protein Biochemistry 48 2009 11920 11928
88. M.A. Larkin, G. Blackshields, N.P. Brown, R. Chenna, P.A. McGettigan, H. McWilliam, F. Valentin, I.M. Wallace, A. Wilm, R. Lopez, J.D. Thompson, T.J. Gibson, and D.G. Higgins Clustal W and Clustal X version 2.0 Bioinformatics 23 2007 2947 2948 (Pubitemid 350162903)
89. W.L. DeLano The PyMOL Molecular Graphics System 2002 DeLano Scientific Palo Alto, CA, USA