Abstract
Photosystem II (PSII) is the water-splitting enzyme complex of photosynthesis and consists of a large number of protein subunits. Most of these proteins have been structurally and functionally characterized, although there are differences between PSII of plants, algae and cyanobacteria. Here we catalogue all known PSII proteins giving a brief description, where possible of their genetic origin, physical properties, structural relationships and functions. We have also included details of auxiliary proteins known at present to be involved in the in vivo assembly, maintenance and turnover of PSII and which transiently bind to the reaction centre core complex. Finally, we briefly give details of the proteins which form the outer light-harvesting systems of PSII in different types of organisms.
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Abbreviations
- AC:
-
Allophycocyanin
- Chl:
-
Chlorophyll
- Cyt:
-
Cytochrome
- FCP:
-
Fucoxantin-binding complex
- LHC:
-
Light-harvesting complex
- LMM:
-
Low molecular mass
- OEC:
-
Oxygen-evolving complex
- PBS:
-
Phycobilisomes
- PC:
-
Phycocyanin
- PE:
-
Phycoerytrin
- Pheo:
-
Pheophytin
- PQ:
-
Plastoquinone
- PQH2 :
-
Plastoquinol
- PS:
-
Photosystem
- RC:
-
Reaction centre
- RNAi:
-
RNA interference
References
Anbudurai PR, Pakrasi HB (1993) Mutational analysis of the PsbL protein of photosystem II in the cyanobacterium Synechocystis sp. PCC 6803. Z Naturforsch C 48:267–274
Anderson LB, Maderia M, Ouellette AJ, Putnam-Evans C, Higgins L, Krick T, MacCoss MJ, Lim H, Yates JR, Barry BA (2002) Posttranslational modifications in the CP43 subunit of photosystem II. Proc Natl Acad Sci USA 99:14676–14681
Aspinall-O’Dea M, Wentworth M, Pascal A, Robert B, Ruban A, Horton P (2002) In vitro reconstitution of the activated zeaxanthin state associated with energy dissipation in plants. Proc Natl Acad Sci USA 99:16331–16335
Ballottari M, Girardon J, Dall’osto L, Bassi R (2012) Evolution and functional properties of photosystem II light harvesting complexes in eukaryotes. Biochim Biophys Acta 1817:143–157
Balsera M, Arellano JB, Revuelta JL, De Las Rivas J, Hermoso JA (2005) The 1.49 Å 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
Barbato R, Friso G, Rigoni F, Dalla Vecchia F, Giacometti GM (1992) Structural changes and lateral redistribution of photosystem II during donor side photoinhibition of thylakoids. J Cell Biol 119:325–335
Barber J (2006) Photosystem II: an enzyme of global significance. Biochem Soc Trans 34:619–631
Barber J, De Las Rivas J (1993) A functional model for the role of cytochrome b559 in the protection against donor and acceptor side photoinhibition. Proc Natl Acad Sci USA 90:10942–10946
Barera S, Pagliano C, Pape T, Saracco G, Barber J (2012) Characterization of PSII-LHCII supercomplexes isolated from pea thylakoid membrane by one-step treatment with α- and β-dodecyl-d-maltoside. Phil Trans R Soc B 367:3389–3399
Bentley FK, Luo H, Dilbeck P, Burnap RL, Eaton-Rye JJ (2008) Effects of inactivating psbM and psbT on photodamage and assembly of photosystem II in Synechocystis sp. PCC 6803. Biochemistry 47:11637–11646
Bergantino E, Segalla A, Brunetta A, Teardo E, Rigoni F, Giacometti GM, Szabò I (2003) Light- and pH-dependent structural changes in the PsbS subunit of photosystem II. Proc Natl Acad Sci USA 100:15265–15270
Bibby TS, Nield J, Chen M, Larkum AW, Barber J (2003) Structure of a photosystem II supercomplex isolated from Prochloron didemni retaining its chlorophyll a/b light-harvesting system. Proc Natl Acad Sci USA 100:9050–9054
Bishop CL, Purton S, Nugent JH (2003) Molecular analysis of the Chlamydomonas nuclear gene encoding PsbW and demonstration that PsbW is a subunit of photosystem II, but not photosystem I. Plant Mol Biol 52:285–289
Bishop CL, Ulas S, Baena-Gonzalez E, Aro EM, Purton S, Nugent JH, Mäenpää P (2007) The PsbZ subunit of photosystem II in Synechocystis sp. PCC 6803 modulates electron flow through the photosynthetic electron transfer chain. Photosynth Res 93:139–147
Bondarava N, Beyer P, Krieger-Liszkay A (2005) Function of the 23 kDa extrinsic protein of photosystem II as a manganese binding protein and its role in photoactivation. Biochim Biophys Acta 1708:63–70
Bonente G, Passarini F, Cazzaniga S, Mancone C, Buia MC, Tripodi M, Bassi R, Caffarri S (2008) The occurrence of the psbS gene product in Chlamydomonas reinhardtii and in other photosynthetic organisms and its correlation with energy quenching. Photochem Photobiol 84:1359–1370
Bricker TM, Roose JL, Fagerlund RD, Frankel LK, Eaton-Rye JJ (2012) The extrinsic proteins of photosystem II. Biochim Biophys Acta 1817:121–142
Burrows PA, Sazanov LA, Svab Z, Maliga P, Nixon PJ (1998) Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disrupted plastid ndh genes. EMBO J 17:868–876
Calderone V, Trabucco M, Vujicic A, Battistutta R, Giacometti GM, Andreucci F, Barbato R, Zanotti G (2003) Crystal structure of the PsbQ protein of photosystem II from higher plants. EMBO Rep 4:900–905
Chen M, Bibby TS, Nield J, Larkum AW, Barber J (2005) Structure of a large photosystem II supercomplex from Acaryochloris marina. FEBS Lett 579:1306–1310
Chen H, Zhang D, Guo J, Wu H, Jin M, Lu Q, Lu C, Zhang L (2006) A Psb27 homologue in Arabidopsis thaliana is required for efficient repair of photodamaged photosystem II. Plant Mol Biol 61:567–575
Chi W, Ma J, Zhang L (2012) Regulatory factors for the assembly of thylakoid membrane protein complexes. Philos Trans R Soc Lond B Biol Sci 367:3420–3429
Cormann KU, Bangert JA, Ikeuchi M, Rögner M, Stoll R, Nowaczyk MM (2009) Structure of Psb27 in solution: implications for transient binding to photosystem II during biogenesis and repair. Biochemistry 48:8768–8770
Cramer WA, Whitmarsh J (1977) Photosynthetic cytochromes. Annu Plant Physiol 28:133–172
De Las Rivas J, Barber J (2004) Analysis of the structure of the PsbO protein and its implications. Photosynth Res 81:329–343
Dedner N, Meyer HE, Ashton C, Wildner GF (1988) N-terminal sequence analysis of the 8 kDa protein in Chlamydomonas reinhardtii. Localization of the phosphothreonine. FEBS Lett 236:77–82
Dekker JP, Boekema EJ (2005) Supramolecular organization of thylakoid membrane proteins in green plants. Biochim Biophys Acta 1706:12–39
Dobáková M, Tichy M, Komenda J (2007) Role of the PsbI protein in photosystem II assembly and repair in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol 145:1681–1691
Dobáková M, Sobotka R, Tichý M, Komenda J (2009) Psb28 protein is involved in the biogenesis of the photosystem II inner antenna CP47 (PsbB) in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol 149:1076–1086
Dominici P, Caffarri S, Armenante F, Ceoldo S, Crimi M, Bassi R (2002) Biochemical properties of the PsbS subunit of photosystem II either purified from chloroplast or recombinant. J Biol Chem 277:22750–22758
Eaton-Rye JJ, Vermaas WF (1991) Oligonucleotide-directed mutagenesis of psbB, the gene encoding CP47, employing a deletion mutant strain of the cyanobacterium Synechocystis sp. PCC 6803. Plant Mol Biol 17:1165–1177
Enami I, Okumura A, Nagao R, Suzuki T, Iwai M, Shen JR (2008) Structures and functions of the extrinsic proteins of photosystem II from different species. Photosynth Res 98:349–363
Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303:1831–1838
Froehlich JE, Wilkerson CG, Ray WK, McAndrew RS, Osteryoung KW, Gage DA, Phinney BS (2003) Proteomic study of the Arabidopsis thaliana chloroplastic envelope membrane utilizing alternatives to traditional two-dimensional electrophoresis. J Proteome Res 2:413–425
Funk CC (2000) Functional analysis of the PsbX protein by deletion of the corresponding gene in Synechocystis sp. PCC 6803. Plant Mol Biol 44:815–827
Funk C, Schröder WP, Napiwotzki A, Tjus SE, Renger G, Andersson B (1995) The PSII-S protein of higher plants: a new type of pigment-binding protein. Biochemistry 34:11133–11141
García-Cerdán JG, Kovács L, Tóth T, Kereïche S, Aseeva E, Boekema EJ, Mamedov F, Funk C, Schröder WP (2011) The PsbW protein stabilizes the supramolecular organization of photosystem II in higher plants. Plant J 65:368–381
Gau AE, Thole HH, Sokolenko A, Altschmied L, Herrmann RG, Pistorius EK (1998) PsbY, a novel manganese-binding, low-molecular-mass protein associated with photosystem II. Mol Gen Genet 260:56–68
Ghanotakis DF, Topper JN, Yocum CF (1984) 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
Giorgi LB, Nixon PJ, Merry SA, Joseph DM, De Rivas Las J, Barber J, Porter G, Klug DR (1996) Comparison of primary charge separation in the photosystem II reaction center complex isolated from wild-type and D1–130 mutants of the cyanobacterium Synechocystis PCC 6803. J Biol Chem 271:2093–2101
Grossman AR, Schaefer MR, Chiang GG, Collier JL (1993) The phycobilisome, a light-harvesting complex responsive to environmental conditions. Microbiol Rev 57:725–749
Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A, Saenger W (2009) Cyanobacterial photosystem II at 2.9 Å resolution and the role of quinones, lipids, channels and chloride. Nat Struct Mol Biol 16:334–342
Hager M, Hermann M, Biehler K, Krieger-Liszkay A, Bock R (2002) Lack of the small plastid-encoded PsbJ polypeptide results in a defective water-splitting apparatus of photosystem II, reduced photosystem I levels, and hypersensitivity to light. J Biol Chem 277:14031–14039
Hagman A, Shi LX, Rintamäki E, Andersson B, Schröder WP (1997) The nuclear-encoded PsbW protein subunit of photosystem II undergoes light-induced proteolysis. Biochemistry 36:12666–12671
Hankamer B, Nield J, Zheleva D, Boekema E, Jansson S, Barber J (1997) Isolation and biochemical characterisation of monomeric and dimeric photosystem II complexes from spinach and their relevance to the organisation of photosystem II in vivo. Eur J Biochem 243:422–429
Hanley J, Deligiannakis Y, Pascal A, Faller P, Rutherford AW (1999) Carotenoid oxidation in photosystem II. Biochemistry 38:8189–8195
Hess WR, Rocap G, Ting CS, Larimer F, Stilwagen S, Lamerdin J, Chisholm SW (2001) The photosynthetic apparatus of Prochlorococcus: insights through comparative genomics. Photosynth Res 70:53–71
Hoshida H, Sugiyama R, Nakano Y, Shiina T, Toyoshima Y (1997) Electron paramagnetic resonance and mutational analyses revealed the involvement of photosystem II-L subunit in the oxidation step of Tyr-Z by P680+ to form the Tyr-Z+P680Pheo− state in photosystem II. Biochemistry 36:12053–12061
Huang J, Taylor JP, Chen JG, Uhrig JF, Schnell DJ, Nakagawa T, Korth KL, Jones AM (2006) The plastid protein THYLAKOID FORMATION1 and the plasma membrane G-protein GPA1 interact in a novel sugar-signaling mechanism in Arabidopsis. Plant Cell 18:1226–1238
Ido K, Ifuku K, Yamamoto Y, Ishihara S, Murakami A, Takabe K, Miyake C, Sato F (2009) Knockdown of the PsbP protein does not prevent assembly of the dimeric PSII core complex but impairs accumulation of photosystem II supercomplexes in tobacco. Biochim Biophys Acta 1787:873–881
Ifuku K, Sato F (2001) Importance of the N-terminal sequence of the extrinsic 23 kDa polypeptide in photosystem II in ion-retention in oxygen-evolution. Biochim Biophys Acta 1546:196–204
Ifuku K, Nakatsu T, Kato H, Sato F (2004) Crystal structure of the PsbP protein of photosystem II from Nicotiana tabacum. EMBO Rep 5:362–367
Ifuku K, Ishihara S, Sato F (2010) Molecular functions of oxygen-evolving complex family proteins in photosynthetic electron flow. J Integr Plant Biol 52:723–734
Ifuku K, Ido K, Sato F (2011) Molecular functions of PsbP and PsbQ proteins in the photosystem II supercomplex. J Photochem Photobiol B 104:158–164
Ikeuchi M, Koike H, Inoue Y (1989a) N-terminal sequencing of low-molecular-mass components in cyanobacterial photosystem II core complex. Two components correspond to unidentified open reading frames of plant chloroplast DNA. FEBS Lett 253:178–182
Ikeuchi M, Takio K, Inoue Y (1989b) N-terminal sequencing of photosystem II low molecular mass proteins. 5 and 4.1 kDa components of the O2 evolving complex from higher plants. FEBS Lett 242:263–269
Ikeuchi M, Eggers B, Shen GZ, Webber A, Yu JJ, Hirano A, Inoue Y, Vermaas W (1991) Cloning of the psbK gene from Synechocystis sp. PCC 6803 and characterization of photosystem II in mutants lacking PSII-K. J Biol Chem 266:11111–11115
Inoue-Kashino N, Kashino Y, Satoh K, Terashima I, Pakrasi HB (2005) PsbU provides a stable architecture for the oxygen-evolving system in cyanobacterial photosystem II. Biochemistry 44:12214–12228
Inoue-Kashino N, Kashino Y, Takahashi Y (2011) Psb30 is a photosystem II reaction center subunit and is required for optimal growth in high light in Chlamydomonas reinhardtii. J Photochem Photobiol B 104:220–228
Ishihara S, Yamamoto Y, Ifuku K, Sato F (2005) Functional analysis of four members of the PsbP family in photosystem II in Nicotiana tabacum using differential RNA interference. Plant Cell Physiol 46:1885–1893
Iwai M, Katoh H, Katayama M, Ikeuchi M (2004) PSII-Tc protein plays an important role in dimerization of photosystem II. Plant Cell Physiol 45:1809–1816
Iwai M, Suzuki T, Kamiyama A, Sakurai I, Dohmae N, Inoue Y, Ikeuchi M (2010) The PsbK subunit is required for the stable assembly and stability of other small subunits in the PSII complex in the thermophilic cyanobacterium Thermosynechococcus elongatus BP-1. Plant Cell Physiol 51:554–560
Jansen MAK, Greenberg BM, Edelman M, Mattoo AK, Gaba V (1996) Accelerated degradation of the D2 protein of photosystem II under ultraviolet radiation. Photochem Photobiol 63:814–817
Kashino Y, Koike H, Yoshio M, Egashira H, Ikeuchi M, Pakrasi HB, Satoh K (2002a) Low-molecular-mass polypeptide components of a photosystem II preparation from the thermophilic cyanobacterium Thermosynechococcus vulcanus. Plant Cell Physiol 43:1366–1373
Kashino Y, Lauber WM, Carroll JA, Wang Q, Whitmarsh J, Satoh K, Pakrasi HB (2002b) 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
Kato Y, Sugiura M, Oda A, Watanabe T (2009) Spectroelectrochemical determination of the redox potential of pheophytin a, the primary electron acceptor in photosystem II. Proc Natl Acad Sci USA 106:17365–17370
Katoh HH, Ikeuchi MM (2001) Targeted disruption of psbX and biochemical characterization of photosystem II complex in the thermophilic cyanobacterium Synechococcus elongatus. Plant Cell Physiol 42:179–188
Kawakami K, Iwai M, Ikeuchi M, Kamiya N, Shen JR (2007) Location of PsbY in oxygen-evolving photosystem II revealed by mutagenesis and X-ray crystallography. FEBS Lett 581:4983–4987
Kawakami K, Umena Y, Iwai M, Kawabata Y, Ikeuchi M, Kamiya N, Shen JR (2011) Roles of PsbI and PsbM in photosystem II dimer formation and stability studied by deletion mutagenesis and X-ray crystallography. Biochim Biophys Acta 1807:319–325
Kereïche S, Kiss AZ, Kouril R, Boekema EJ, Horton P (2010) The PsbS protein controls the macro-organisation of photosystem II complexes in the grana membranes of higher plant chloroplasts. FEBS Lett 584:759–764
Keren N, Ohkawa H, Welsh EA, Liberton M, Pakrasi HB (2005) Psb29, a conserved 22-kDa protein, functions in the biogenesis of Photosystem II complexes in Synechocystis and Arabidopsis. Plant Cell 17:2768–2781
Kim S, Sandusky P, Bowlby NR, Aebersold R, Green BR, Vlahaskis S, Yocum CF, Pichersky E (1992) Characterization of a spinach psbS cDNA encoding the 22 kDa protein of photosystem II. FEBS Lett 314:67–71
Kiss AZ, Ruban AV, Horton P (2008) The PsbS protein controls the organization of the photosystem II antenna in higher plant thylakoid membranes. J Biol Chem 283:3972–3978
Kitamura K, Ozawa S, Shiina T, Toyoshima Y (1994) l-protein, encoded by psbL, restores normal functioning of the primary quinone acceptor, QA, in isolated D1/D2/CP47/Cytb-559/I photosystem II reaction center core complex. FEBS Lett 354:113–116
Knaff DB, Arnon DI (1969) Spectral evidence for a photoreactive component of the oxygen-evolving system in photosynthesis. Proc Natl Acad Sci USA 63:963–969
Komenda J, Barber J (1995) Comparison of psbO and psbH deletion mutants of Synechocystis PCC 6803 indicates that degradation of D1 protein is regulated by the QB site and dependent on protein synthesis. Biochemistry 34:9625–9631
Komenda J, Lupínková L, Kopecký J (2002) Absence of the psbH gene product destabilizes photosystem II complex and bicarbonate binding on its acceptor side in Synechocystis PCC 6803. FEBS J 269:610–619
Komenda J, Tichý M, Eichacker LA (2005) The PsbH protein is associated with the inner antenna CP47 and facilitates D1 processing and incorporation into PSII in the cyanobacterium Synechocystis PCC 6803. Plant Cell Physiol 46:1477–1483
Komenda J, Sobotka R, Nixon PJ (2012a) Assembling and maintaining the photosystem II complex in chloroplasts and cyanobacteria. Curr Opin Plant Biol 15:245–251
Komenda J, Knoppová J, Kopečná J, Sobotka R, Halada P, Yu J, Nickelsen J, Boehm M, Nixon PJ (2012b) The Psb27 assembly factor binds to the CP43 complex of photosystem II in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol 158:476–486
Kruk J, Strzalka K (2001) Redox changes of cytochrome b559 in the presence of plastoquinones. J Biol Chem 276:86–91
Lautner A, Klein R, Ljungberg U, Reiländer H, Bartling D, Andersson B, Reinke H, Beyreuther K, Herrmann RG (1988) Nucleotide sequence of cDNA clones encoding the complete precursor for the “10-kDa” polypeptide of photosystem II from spinach. J Biol Chem 263:10077–10081
Li XP, Björkman O, Shih C, Grossman AR, Rosenquist M, Jansson S, Niyogi KK (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403:391–395
Liu H, Frankel LK, Bricker TM (2009) Characterization and complementation of a psbR mutant in Arabidopsis thaliana. Arch Biochem Biophys 489:34–40
Liu H, Huang RY, Chen J, Gross ML, Pakrasi HB (2011) Psb27, a transiently associated protein, binds to the chlorophyll binding protein CP43 in photosystem II assembly intermediates. Proc Natl Acad Sci USA 108:18536–18541
Ljungberg U, Akerlund HE, Andersson B (1986) Isolation and characterization of the 10-kDa and 22-kDa polypeptides of higher plant photosystem 2. Eur J Biochem 158:477–482
Loll B, Kern J, Saenger W, Zouni A, Biesiadka J (2005) Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature 438:1040–1044
Lorković ZJ, Schröder WP, Pakrasi HB, Irrgang KD, Herrmann RG, Oelmüller R (1995) Molecular characterization of PsbW, a nuclear-encoded component of the photosystem II reaction center complex in spinach. Proc Natl Acad Sci USA 92:8930–8934
Lundin B, Hansson M, Schoefs B, Vener AV, Spetea C (2007) The Arabidopsis PsbO2 protein regulates dephosphorylation and turnover of the photosystem II reaction centre D1 protein. Plant J 49:528–539
Lundin B, Nurmi M, Rojas-Stuetz M, Aro EM, Adamska I, Spetea C (2008) Towards understanding the functional difference between the two PsbO isoforms in Arabidopsis thaliana-insights from phenotypic analyses of psbo knockout mutants. Photosynth Res 98:405–414
Luo H, Eaton-Rye JJ (2008) Directed mutagenesis of the transmembrane domain of the PsbL subunit of photosystem II in Synechocystis sp. PCC 6803. Photosynth Res 98:337–347
Mabbitt PD, Rautureau GJ, Day CL, Wilbanks SM, Eaton-Rye JJ, Hinds MG (2009) Solution structure of Psb27 from cyanobacterial photosystem II. Biochemistry 48:8771–8773
MacColl R (1998) Cyanobacterial phycobilisomes. J Struct Biol 124:311–334
Mamedov F, Nowaczyk MM, Thapper A, Rögner M, Styring S (2007) Functional characterization of monomeric photosystem II core preparations from Thermosynechococcus elongatus with or without the Psb27 protein. Biochemistry 46:5542–5551
Mant A, Robinson C (1998) An Arabidopsis cDNA encodes an apparent polyprotein of two non-identical thylakoid membrane proteins that are associated with photosystem II and homologous to algal ycf32 open reading frames. FEBS Lett 423:183–188
Mayes SR, Cook KM, Self SJ, Zhang Z, 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
Mayes SR, Dubbs JM, Vass I, Hideg E, Nagy L, Barber J (1993) Further characterization of the psbH locus of Synechocystis sp. PCC 6803: Inactivation of psbH impairs QA to QB electron transport in photosystem 2. Biochemistry 32:1454–1465
Mayfield SP, Bennoun P, Rochaix JD (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
Meades GD Jr, McLachlan A, Sallans L, Limbach PA, Frankel LK, Bricker TM (2005) Association of the 17-kDa extrinsic protein with photosystem II in higher plants. Biochemistry 44:15216–15221
Meetam M, Keren N, Ohad I, Pakrasi HB (1999) The PsbY protein is not essential for oxygenic photosynthesis in the cyanobacterium Synechocystis sp. PCC 68031. Plant Physiol 121:1267–1272
Michel HP, Bennett J (1987) Identification of the phosphorylation site of an 8.3 kDa protein from photosystem II of spinach. FEBS Lett 212:103–108
Michel HP, Hunt DF, Shabanowitz J, Bennett J (1988) Tandem mass spectrometry reveals that three photosystem II proteins of spinach chloroplasts contain N-acetyl-O-phosphothreonine at their NH2 termini. J Biol Chem 263:1123–1130
Michoux F, Takasaka K, Boehm M, Komenda J, Nixon PJ, Murray JW (2012) Crystal structure of the Psb27 assembly factor at 1.6 Å: implications for binding to Photosystem II. Photosynth Res 110:169–175
Miyao M, Murata N (1984) Calcium ions can be substituted for the 24-kDa polypetide in photosynthetic oxygen evolution. FEBS Lett 168:119–120
Monod C, Takahashi Y, Goldschmidt-Clermont M, Rochaix JD (1994) The chloroplast ycf8 open reading frame encodes a photosystem II polypeptide which maintains photosynthetic activity under adverse growth conditions. EMBO J 13:2747–2754
Morais F, Barber J, Nixon PJ (1998) The chloroplast encoded alpha subunit of cytochrome b559 is required for assembly of the PSII complex in both the light and dark in Chlamydomonas reinhardtii. J Biol Chem 273:29315–29320
Morais F, Kühn K, Stewart DH, Barber J, Brudvig GW, Nixon PJ (2001) Photosynthetic water oxidation in cytochrome b559 mutants containing a disrupted heme-binding pocket. J Biol Chem 276:31986–31993
Mullineaux CW (2008) Phycobilisome-reaction centre interaction in cyanobacteria. Photosynth Res 95:175–182
Mulo P, Sirpiö S, Suorsa M, Aro EM (2008) Auxiliary proteins involved in the assembly and sustenance of photosystem II. Photosynth Res 98:489–501
Murakami R, Ifuku K, Takabayashi A, Shikanai T, Endo T, Sato F (2002) Characterization of an Arabidopsis thaliana mutant with impaired psbO, one of genes encoding 33-kDa protein of oxygen-evolving complex, which shows retarded growth. FEBS Lett 523:138–142
Murakami R, Ifuku K, Takabayashi A, Shikanai T, Endo T, Sato F (2005) Functional dissection of two Arabidopsis PsbO proteins: PsbO1 and PsbO2. FEBS J 272:2165–2175
Murray JW, Barber J (2007) Structural characteristics of channels and pathways in photosystem II including the identification of an oxygen channel. J Struct Biol 159:228–237
Murray JW, Maghlaoui K, Barber J (2007) The structure of allophycocyanin from Thermosynechococcus elongatus at 3.5 Å resolution. Acta Crystallogr Sect F 63:998–1002
Murray JW, Maghlaoui K, Kargul J, Ishida N, Lai TL, Rutherford AW, Sugiura M, Boussac A, Barber J (2008) X-ray crystallography identifies two chloride binding sites in the oxygen evolving centre of photosystem II. Energy Environ Sci 1:161–166
Nagao R, Ishii A, Tada O, Suzuki T, Dohmae N, Okumura A, Iwai M, Takahashi T, Kashino Y, Enami I (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
Nagao R, Tomo T, Noguchi E, Nakajima S, Suzuki T, Okumura A, Kashino Y, Mimuro M, Ikeuchi M, Enami I (2010a) Purification and characterization of a stable oxygen-evolving Photosystem II complex from a marine centric diatom, Chaetoceros gracilis. Biochim Biophys Acta 1797:160–166
Nagao R, Moriguchi A, Tomo T, Niikura A, Nakajima S, Suzuki T, Okumura A, Iwai M, Shen JR, Ikeuchi M, Enami I (2010b) Binding and functional properties of five extrinsic proteins in oxygen-evolving photosystem II from a marine centric diatom, Chaetoceros gracilis. J Biol Chem 285:29191–29199
Nagatsuka T, Fukuhara S, Akabari K, Toyoshima Y (1991) Disintegration and reconstitution of photosystem II reaction center core complex. II. Possible involvement of low-molecular-mass proteins in the functioning of QA in the PSII reaction center. Biochim Biophys Acta 1057:223–231
Nanba O, Satoh K (1987) Isolation of a photosystem II reaction center consisting of D1 and D2 polypeptides and cytochrome b559. Proc Natl Acad Sci USA 84:109–112
Neilson JA, Durnford DG (2010) Structural and functional diversification of the light-harvesting complexes in photosynthetic eukaryotes. Photosynth Res 106:57–71
Nixon PJ, Gounaris K, Coomber SA, Hunter CN, Dyer TA, Barber J (1989) psbG is not a photosystem two gene but may be an ndh gene. J Biol Chem 264:14129–14135
Nixon PJ, Michoux F, Yu J, Boehm M, Komenda J (2010) Recent advances in understanding the assembly and repair of photosystem II. Ann Bot 106:1–16
Nowaczyk MM, Hebeler R, Schlodder E, Meyer HE, Warscheid B, Rögner M (2006) Psb27, a cyanobacterial lipoprotein, is involved in the repair cycle of photosystem II. Plant Cell 18:3121–3131
Nowaczyk MM, Krause K, Mieseler M, Sczibilanski A, Ikeuchi M, Rögner M (2012) Deletion of psbJ leads to accumulation of Psb27-Psb28 photosystem II complexes in Thermosynechococcus elongatus. Biochim Biophys Acta 1817:1339–1345
Ohad I, Dal Bosco C, Herrmann RG, Meurer J (2004) Photosystem II proteins PsbL and PsbJ regulate electron flow to the plastoquinone pool. Biochemistry 43:2297–2308
Ohnishi N, Takahashi Y (2001) PsbT polypeptide is required for efficient repair of photodamaged photosystem II reaction center. J Biol Chem 276:33798–33804
Ohnishi N, Takahashi Y (2008) Chloroplast-encoded PsbT is required for efficient biogenesis of photosystem II complex in the green alga Chlamydomonas reinhardtii. Photosynth Res 98:315–322
Ohta H, Suzuki T, Ueno M, Okumura A, Yoshihara S, Shen JR, Enami I (2003) Extrinsic proteins of photosystem II: an intermediate member of PsbQ protein family in red algal PSII. Eur J Biochem 270:4156–4163
Okumura A, Nagao R, Suzuki T, Yamagoe S, Iwai M, Nakazato K, Enami I (2008) A novel protein in photosystem II of a diatom Chaetoceros gracilis is one of the extrinsic proteins located on lumenal side and directly associates with PSII core components. Biochim Biophys Acta 1777:1545–1551
Oudot-Le Secq MP, Grimwood J, Shapiro H, Armbrust EV, Bowler C, Green BR (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
Pagliano C, La Rocca N, Andreucci F, Deák Z, Vass I, Rascio N, Barbato R (2009) The extreme halophyte Salicornia veneta is depleted of the extrinsic PsbQ and PsbP proteins of the oxygen-evolving complex without loss of functional activity. Ann Bot 103:505–515
Pagliano C, Chimirri F, Saracco G, Marsano F, Barber J (2011) One-step isolation and biochemical characterization of a highly active plant PSII monomeric core. Photosynth Res 108:33–46
Pakrasi HB, Nyhus KJ, Granok H (1990) Targeted deletion mutagenesis of the beta subunit of cytochrome b559 protein destabilizes the reaction center of photosystem II. Naturforsch 45:423–429
Pakrasi HB, De Ciechi P, Whitmarsh J (1991) Site directed mutagenesis of the heme axial ligands of cytochrome b559 affects the stability of the photosystem II complex. EMBO J 10:1619–1627
Partensky F, Hess WR, Vaulot D (1999) Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol Mol Biol Rev 63:106–127
Peltier JB, Friso G, Kalume DE, Roepstorff P, Nilsson F, Adamska I, van Wijk KJ (2000) Proteomics of the chloroplast: systematic identification and targeting analysis of lumenal and peripheral thylakoid proteins. Plant Cell 12:319–341
Peltier JB, Ytterberg AJ, Sun Q, van Wijk KJ (2004) New functions of the thylakoid membrane proteome of Arabidopsis thaliana revealed by a simple, fast, and versatile fractionation strategy. J Biol Chem 279:49367–49383
Peltier JB, Cai Y, Sun Q, Zabrouskov V, Giacomelli L, Rudella A, Ytterberg AJ, Rutschow H, van Wijk KJ (2006) The oligomeric stromal proteome of Arabidopsis thaliana chloroplasts. Mol Cell Proteomics 5:114–133
Pérez-Bueno ML, Rahoutei J, Sajnani C, García-Luque I, Barón M (2004) Proteomic analysis of the oxygen-evolving complex of photosystem II under biotec stress: Studies on Nicotiana benthamiana infected with tobamoviruses. Proteomics 4:418–425
Pérez-Bueno ML, Barón M, García-Luque I (2011) PsbO, PsbP, and PsbQ of photosystem II are encoded by gene families in Nicotiana benthamiana. Structure and functionality of their isoforms. Photosynthetica 49:573–580
Philbrick JB, Diner BA, Zilinskas BA (1991) Construction and characterization of cyanobacterial mutants lacking the manganese-stabilizing polypeptide of photosystem II. J Biol Chem 266:13370–13376
Pursiheimo S, Rintamäki E, Baena-Gonzales E, Aro EM (1998) Thylakoid protein phosphorylation in evolutionally divergent species with oxygenic photosynthesis. FEBS Lett 423:178–182
Putnam-Evans C, Bricker TM (1994) Site-directed mutagenesis of the CP47 protein of photosystem II: alteration of the basic residue 448R to 448G prevents the assembly of functional photosystem II centers under chloride-limiting conditions. Biochemistry 33:10770–10776
Regel RE, Ivleva NB, Zer H, Meurer J, Shestakov SV, Herrmann RG, Pakrasi HB, Ohad I (2001) Deregulation of electron flow within photosystem II in the absence of the PsbJ protein. J Biol Chem 276:41473–41478
Rinalducci S, Larsen MR, Mohammed S, Zolla L (2006) Novel protein phosphorylation site identification in spinach stroma membranes by titanium dioxide microcolumns and tandem mass spectrometry. J Proteome Res 5:973–982
Roose JL, Pakrasi HB (2008) The Psb27 protein facilitates manganese cluster assembly in photosystem II. J Biol Chem 283:4044–4050
Roose JL, Wegener KM, Pakrasi HB (2007a) The extrinsic proteins of photosystem II. Photosynth Res 92:369–387
Roose JL, Kashino Y, Pakrasi HB (2007b) The PsbQ protein defines cyanobacterial photosystem II complexes with highest activity and stability. Proc Natl Acad Sci USA 104:2548–2553
Sakata S, Mizusawa N, Kubota-Kawai H, Sakurai I, Wada H (2013) Psb28 is involved in recovery of photosystem II at high temperature in Synechocystis sp. PCC 6803. Biochim Biophys Acta 1827:50–59
Sakurai I, Mizusawa N, Ohashi S, Kobayashi M, Wada H (2007) Effects of the lack of phosphatidylglycerol on the donor side of photosystem II. Plant Physiol 144:1336–1346
Schubert M, Petersson UA, Haas BJ, Funk C, Schröder WP, Kieselbach T (2002) Proteome map of the chloroplast lumen of Arabidopsis thaliana. J Biol Chem 277:8354–8365
Schwenkert S, Umate P, Dal Bosco C, Volz S, Mlçochová L, Zoryan M, Eichacker LA, Ohad I, Herrmann RG, Meurer J (2006) PsbI affects the stability, function, and phosphorylation patterns of photosystem II assemblies in tobacco. J Biol Chem 281:34227–34238
Seidler A (1996) The extrinsic polypeptides of photosystem II. Biochim Biophys Acta 1277:35–60
Sharma J, Panico M, Barber J, Morris HR (1997) Characterization of the low molecular weight photosystem II reaction center subunits and their light-induced modifications by mass spectrometry. J Biol Chem 272:3935–3943
Shen JR, Burnap RL, Inoue Y (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
Shi LX, Schröder WP (1997) Compositional and topological studies of the PsbW protein in spinach thylakoid membrane. Photosynth Res 53:45–53
Shi LX, Schröder W (2004) The low molecular mass subunits of the photosynthetic supracomplex, photosystem II. Biochim Biophys Acta 1608:75–96
Shi LX, Kim SJ, Marchant A, Robinson C, Schröder WP (1999) Characterisation of the PsbX protein from photosystem II and light regulation of its gene expression in higher plants. Plant Mol Biol 40:737–744
Shi LX, Hall M, Funk C, Schröder W (2012) Photosystem II, a growing complex: updates on newly discovered components and low molecular mass proteins. Biochim Biophys Acta 1817:13–25
Sirpiö S, Allahverdiyeva Y, Suorsa M, Paakkarinen V, Vainonen J, Battchikova N, Aro EM (2007) TLP18.3, a novel thylakoid lumen protein regulating photosystem II repair cycle. Biochem J 406:415–425
Stewart DH, Brudvig GW (1998) Cytochrome b559 of photosystem II. Biochim Biophys Acta 1367:63–87
Sugiura M, Harada S, Manabe T, Hayashi H, Kashino Y, Boussac A (2010) Psb30 contributes to structurally stabilise the photosystem II complex in the thermophilic cyanobacterium Thermosynechococcus elongatus. Biochim Biophys Acta 1797:1546–1554
Summer EJ, Schmid VH, Bruns BU, Schmidt GW (1997) Requirement for the H phosphoprotein in photosystem II of Chlamydomonas reinhardtii. Plant Physiol 113:1359–1368
Suorsa M, Regel RE, Paakkarinen V, Battchikova N, Herrmann RG, Aro EM (2004) Protein assembly of photosystem II and accumulation of subcomplexes in the absence of low molecular mass subunits PsbL and PsbJ. Eur J Biochem 271:96–107
Suorsa M, Sirpiö S, Allahverdiyeva Y, Paakkarinen V, Mamedov F, Styring S, Aro EM (2006) PsbR, a missing link in the assembly of the oxygen-evolving complex of plant photosystem II. J Biol Chem 281:145–150
Suzuki T, Minagawa J, Tomo T, Sonoike K, Ohta H, Enami I (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
Swiatek M, Kuras R, Sokolenko A, Higgs D, Olive J, Cinque G, Müller B, Eichacker LA, Stern DB, Bassi R, Herrmann RG, Wollman FA (2001) The chloroplast gene ycf9 encodes a photosystem II (PSII) core subunit, PsbZ, that participates in PSII supramolecular architecture. Plant Cell 13:1347–1367
Swiatek M, Regel RE, Meurer J, Wanner G, Pakrasi HB, Ohad I, Herrmann RG (2003) Effects of selective inactivation of individual genes for low-molecular-mass subunits on the assembly of photosystem II, as revealed by chloroplast transformation: the psbEFLJ operon in Nicotiana tabacum. Mol Gen Genomics 268:699–710
Tae GS, Cramer WA (1992) Truncation of the carboxy-terminal domain of the psbE gene product in Synechocystis sp. PCC 6803: requirements for photosystem II assembly and function. Biochemistry 31:4066–4074
Takahashi Y, Matsumoto H, Goldschmidt-Clermont M, Rochaix JD (1994) Directed disruption of the Chlamydomonas chloroplast psbK gene destabilizes the photosystem II reaction center complex. Plant Mol Biol 24:779–788
Takasaka K, Iwai M, Umena Y, Kawakami K, Ohmori Y, Ikeuchi M, Takahashi Y, Kamiya N, Shen JR (2010) Structural and functional studies on Ycf12 (Psb30) and PsbZ-deletion mutants from a thermophilic cyanobacterium. Biochim Biophys Acta 1797:278–284
Takishita K, Uchida A (1999) Molecular cloning and nucleotide sequence analysis of psbA from dinoflagellates: origin of the dinoflagellate plastid. Phycol Res 43:207–216
Teardo E, de Laureto PP, Bergantino E, Dalla Vecchia F, Rigoni F, Szabò I, Giacometti GM (2007) Evidences for interaction of PsbS with photosynthetic complexes in maize thylakoids. Biochim Biophys Acta 1767:703–711
Thangaraj B, Ryan CM, Souda P, Krause K, Faull KF, Weber AP, Fromme P, Whitelegge JP (2010) Data-directed top-down Fourier-transform mass spectrometry of a large integral membrane protein complex: photosystem II from Galdieria sulphuraria. Proteomics 10:3644–3656
Thornton LE, Ohkawa H, Roose JL, Kashino Y, Keren N, Pakrasi HB (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
Trotta A, Redondo-Gómez S, Pagliano C, Clemente ME, Rascio N, Rocca NL, Antonacci A, Andreucci F, Barbato R (2012) Chloroplast ultrastructure and thylakoid polypeptide composition are affected by different salt concentrations in the halophytic plant Arthrocnemum macrostachyum. J Plant Physiol 169:111–116
Turkina MV, Kargul J, Blanco-Rivero A, Villarejo A, Barber J, Vener AV (2006) Environmentally modulated phosphoproteome of photosynthetic membranes in the green alga Chlamydomonas reinhardtii. Mol Cell Proteomics 5:1412–1425
Umate P, Schwenkert S, Karbat I, Dal Bosco C, Mlcòchová L, Volz S, Zer H, Herrmann RG, Ohad I, Meurer J (2007) Deletion of PsbM in tobacco alters the QB site properties and the electron flow within photosystem II. J Biol Chem 282:9758–9767
Umate P, Fellerer C, Schwenkert S, Zoryan M, Eichacker LA, Sadanandam A, Ohad I, Herrmann RG, Meurer J (2008) Impact of PsbTc on forward and back electron flow, assembly, and phosphorylation patterns of photosystem II in tobacco. Plant Physiol 148:1342–1353
Umena Y, Kawakami K, Shen JR, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473:55–60
Veerman J, Bentley FK, Eaton-Rye JJ, Mullineaux CW, Vasil’ev S, Bruce D (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
Vener AV, Harms A, Sussman MR, Vierstra RD (2001) Mass spectrometric resolution of reversible protein phosphorylation in photosynthetic membranes of Arabidopsis thaliana. J Biol Chem 276:6959–6966
Wang Q, Sullivan RW, Kight A, Henry RL, Huang J, Jones AM, Korth KL (2004) Deletion of the chloroplast-localized thylakoid formation1 gene product in Arabidopsis leads to deficient thylakoid formation and variegated leaves. Plant Physiol 136:3594–3604
Wegener KM, Bennewitz S, Oelmüller R, Pakrasi HB (2011) The Psb32 protein aids in repairing photodamaged photosystem II in the cyanobacterium Synechocystis 6803. Mol Plant 4:1052–1061
Wei L, Guo J, Ouyang M, Sun X, Ma J, Chi W, Lu C, Zhang L (2010) LPA19, a Psb27 homolog in Arabidopsis thaliana, facilitates D1 protein precursor processing during PSII biogenesis. J Biol Chem 285:21391–21398
Wu J, Putnam-Evans C, Bricker TM (1996) Site-directed mutagenesis of the CP47 protein of photosystem II: 167 W in the lumenally exposed loop C is required for photosystem II assembly and stability. Plant Mol Biol 32:537–542
Wu HY, Liu MS, Lin TP, Cheng YS (2011) Structural and functional assays of AtTLP18.3 identify its novel acid phosphatase activity in thylakoid lumen. Plant Physiol 157:1015–1025
Yang Y, Ramelot TA, Cort JR, Wang D, Ciccosanti C, Hamilton K, Nair R, Rost B, Acton TB, Xiao R, Everett JK, Montelione GT, Kennedy MA (2011) Solution NMR structure of photosystem II reaction center protein Psb28 from Synechocystis sp. strain PCC 6803. Proteins 79:340–344
Yi X, McChargue M, Laborde S, Frankel LK, Bricker TM (2005) The manganese-stabilizing protein is required for photosystem II assembly/stability and photoautotrophy in higher plants. J Biol Chem 280:16170–16174
Yi X, Hargett SR, Frankel LK, Bricker TM (2006) The PsbQ protein is required in Arabidopsis for photosystem II assembly/stability and photoautotrophy under low light conditions. J Biol Chem 281:26260–26267
Yi X, Hargett SR, Frankel LK, Bricker TM (2009) The PsbP protein, but not the PsbQ protein, is required for normal thylakoid architecture in Arabidopsis thaliana. FEBS Lett 583:2142–2147
Zhang ZH, Mayes SR, Vass I, Nagy L, Barber J (1993) Characterization of the psbK locus of Synechocystis sp. PCC 6803 in terms of photosystem II function. Photosynth Res 38:369–377
Zhang L, Wei Q, Wu W, Cheng Y, Hu G, Hu F, Sun Y, Zhu Y, Sakamoto W, Huang J (2009) Activation of the heterotrimeric G protein alpha-subunit GPA1 suppresses the ftsh-mediated inhibition of chloroplast development in Arabidopsis. Plant J 58:1041–1053
Acknowledgments
JB thanks the Biological and Biotechnological Science Research Council (BBSRC) and the Engineering and Physical Science Research Council (EPSRC) for financial support. This work was also supported by the European Commission (ArtipHyction project (303435) FCH-JU-2011-1; Eco2CO2 project (309701) FP7-NMP2012). We thank Prof. Peter Nixon (Imperial College London) for useful suggestions during the preparation of this manuscript.
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Pagliano, C., Saracco, G. & Barber, J. Structural, functional and auxiliary proteins of photosystem II. Photosynth Res 116, 167–188 (2013). https://doi.org/10.1007/s11120-013-9803-8
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DOI: https://doi.org/10.1007/s11120-013-9803-8