Skip to main content
SpringerLink
Log in

Expression, assembly and auxiliary functions of photosystem II oxygen-evolving proteins in higher plants

  • Research Article
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

The oxygen-evolving complex (OEC) of higher plant photosystem II (PSII) consists of an inorganic Mn4Ca cluster and three nuclear-encoded proteins, PsbO, PsbP and PsbQ. In this review, we focus on the assembly of these OEC proteins, and especially on the role of the small intrinsic PSII proteins and recently found “novel” PSII proteins in the assembly process. The numerous auxiliary functions suggested during the past few years for the OEC proteins will likewise be discussed. For example, besides being a manganese-stabilizing protein, PsbO has been found to bind calcium and GTP and possess a carbonic anhydrase activity. In addition, specific roles have been suggested for the two isoforms of the PsbO protein in Arabidopsis thaliana. PsbP and PsbQ seem to play an additional role in the formation of PSII supercomplexes and in grana stacking, besides their originally recognized role in providing a proper calcium and chloride ion concentration for water splitting.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

Abbreviations

LHCII:

Light harvesting complex of photosystem II

LMM:

Low molecular mass

OEC:

Oxygen-evolving complex

PSII:

Photosystem II

PSI:

Photosystem I

References

  • Anbudurai PR, Mor TS, Ohad I, Shestakov SV, Pakrasi HB (1994) The ctpA gene encodes the C-terminal processing protease for the D1 protein of the photosystem II reaction center. Proc Natl Acad Sci USA 91:8082–8086

    Article  CAS  PubMed  Google Scholar 

  • Anderson JM, Aro E-M (1994) Grana stacking and protection of photosystem II in thylakoid membranes of higher plant leaves under sustained high irradiance: a hypothesis. Photosynth Res 41:315–326

    Article  CAS  Google Scholar 

  • Anderson JM, Chow WS (2002) Structural and functional dynamics of plant photosystem II. Philos Trans R Soc Lond B 357:1421–1430

    Article  CAS  Google Scholar 

  • Aro E-M, Virgin I, Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143:113–134

    Article  CAS  PubMed  Google Scholar 

  • Aro E-M, Suorsa M, Rokka A, Allahverdiyeva Y, Paakkarinen V, Saleem A, Battchikova N, Rintamäki E (2005) Dynamics of photosystem II: a proteomic approach to thylakoid protein complexes. J Exp Bot 56:347–356

    Article  CAS  PubMed  Google Scholar 

  • Baena-Gonzales E, Aro E-M (2002) Biogenesis, assembly and turnover of photosystem II units. Philos Trans R Soc Lond B 357:1451–1459

    Article  Google Scholar 

  • Ban A, Satoh K, Kashino Y (2006) PsbY is crucial for the stable binding of extrinsic protein in photosystem II. Plant Cell Phys 47(Suppl):162

    Google Scholar 

  • Barber J, Ferreira K, Maghlaoui K, Iwata S (2004) Structural model of the oxygen-evolving centre of photosystem II with mechanistic implication. Phys Chem Chem Phys 6:4737–4742

    Article  CAS  Google Scholar 

  • Bernier M, Carpentier R (1995) The action of mercury on the binding of the extrinsic polypeptides asscoaited with the water oxidazing complex of photosystem II. FEBS Lett 360:251–254

    Article  CAS  PubMed  Google Scholar 

  • Betts SD, Ross JR, Pichersky E, Yocum CF (1997) Mutation Val235Ala weakens binding of the 33-kDa manganese stabilizing protein of photosystem II to one of two sites. Biochemistry 36:4047–4053

    Article  CAS  PubMed  Google Scholar 

  • Boekema EJ, van Breemen JFL, van Roon H, Dekker JP (2000) Conformational changes in photosystem II supercomplexes upon removal of extrinsic subunits. Biochemistry 39:12907–12915

    Article  CAS  PubMed  Google Scholar 

  • Bondareva 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

    Article  Google Scholar 

  • Bricker TM, Frankel LK (2002) The structure and function of CP47 and CP43 in photosystem II. Photosynth Res 72:131–146

    Article  CAS  PubMed  Google Scholar 

  • Bricker TM, Frankel LK (2003) Carboxylate groups of the manganese-stabilizing protein are required for efficient binding of the 24 kDa extrinsic protein to Photosystem II. Biochemistry 42:2056–2061

    Article  CAS  PubMed  Google Scholar 

  • Buchanan B, Luan S (2005) Redox regulation in the chloroplast lumen: a new frontier in photosynthesis research. J Exp Bot 56:1439–1447

    Article  CAS  PubMed  Google Scholar 

  • Büchel C, Barber J, Ananyev G, Eshagi S, Watt R, Dismukes C (1999) Photoassembly of the manganese cluster and oxygen evolution from monomeric and dimeric CP47 reaction center photosystem II complexes. Proc Natl Acad Sci USA 96:14288–14293

    Article  PubMed  Google Scholar 

  • Chen H, Zhang D, Guo J, Wu H, Jin M, Lu Q, Lu C, Zhang LX (2006) A Psb27 homologue in Arabidopsis thaliana is required for efficient repair of photodamaged photosystem II. Plant Mol Biol 61:567–575

    Article  CAS  PubMed  Google Scholar 

  • Chu HA, Hillier W, Debus RJ (2004) Evidence that the C-terminus of the D1 polypeptide of photosystem II is ligated to the manganese ion that undergoes oxidation during the S-1 to S-2 transition: an isotope-edited FTIR study. Biochemistry 43:3152–3166

    Article  CAS  PubMed  Google Scholar 

  • Danielsson R, Suorsa M, Paakkarinen V, Albertsson P-Å, Styring S, Aro E-M, Mamedov F (2006) Dimeric and monomeric organization of Photosystem II: distribution of five distinct complexes in the different domains of the thylakoid membrane. J Biol Chem 281:14241–14249

    Article  CAS  PubMed  Google Scholar 

  • De Las Rivas J, Barber J (2004) Analysis of the structure of the PsbO protein and its implications. Photosynth Res 81:329–343

    Article  PubMed  Google Scholar 

  • De Las Rivas J, Roman A (2005) Structure and evolution of the extrinsic proteins that stabilize the oxygen-evolving engine. Photochem Photobiol Sci 4:1003–1010

    Article  PubMed  Google Scholar 

  • De Las Rivas J, Balsera M, Barber J (2004) Evolution of oxygenic photosynthesis: genome-wide analyss of the OEC extrinsic proteins. Trends Plant Sci 9:18–25

    Article  PubMed  Google Scholar 

  • Dekker JP, Boekema EJ (2005) Supramolecular organization of thylakoid membrane proteins in green plants. Biochim Biophys Acta 1706:12–39

    Article  CAS  PubMed  Google Scholar 

  • Diner BA (2001) Amino acid residues involved in the co-ordination and assembly of the manganese cluster of photosystem II. Proton-coupled electron transport of the redox-active tyrosines and its relationship to water oxidation. Biochim Biophys Acta 1503:147–163

    Article  CAS  PubMed  Google Scholar 

  • Eaton-Rye JJ (2005) Requirements for different combinations of the extrinsic proteins in specific cyanobacterial photosystem II mutants. Photosynt Res 84:275–281

    Article  CAS  Google Scholar 

  • Enami I, Suzuki T, Tada O, Nakada Y, Nakamura K, Tohri A, Ohta H, Inoue I, Shen JR (2005) Distribution of the extrinsic proteins as potential marker for the evolution of photosynthetic oxygen-evolving photosystem II. FEBS J 272:5020–5030

    Article  CAS  PubMed  Google Scholar 

  • Ettinger WF, Theg SM (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

    Article  CAS  PubMed  Google Scholar 

  • Ferreira KN, Iverson T, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving complex. Science 303:1831–1838

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Goulas E, Schubert M, Kieselbach T, Kleczkowski LA, Gardeström P, Schröder WP, Hurry V (2006) The chloroplast lumen and stromal proteomes of Arabidopsis thaliana show differential sensitivity to short- and long-term exposure to low temperature. Plant J 47:720–734

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Hashimoto A, Akasaka T, Yamamoto Y (1993) Characteristics of the assembly of the 33 kDa oxygen-evolving complex proteins in the etioplasts and the developing chloroplasts of barley seedlings. Biochim Biophys Acta 1183:397–407

    Article  CAS  Google Scholar 

  • Hashimoto A, Yamamoto Y, Theg SM (1996) Unassembled subunits of the photosynthetic oxygen-evolving complex present in the thylakoid lumen are long-lived and assembly-competent. FEBS Lett 391:29–34

    Article  CAS  PubMed  Google Scholar 

  • Hashimoto A, Ettinger WF, Yamamoto Y, Theg SM (1997) Assembly of newly imported oxygen-evolving complex subunits in isolated chloroplasts: sites of assembly and mechanism of binding. Plant Cell 9:441–452

    Article  CAS  PubMed  Google Scholar 

  • Heredia P, De Las Rivas J (2003) Calcium-dependent conformational change and thermal stability of the isolated PsbO protein detected by FTIR spectroscopy. Biochemistry 42:11831–11838

    Article  CAS  PubMed  Google Scholar 

  • Hua S, Dube SK, Barnett NM, Kung S-D (1992) Photosystem II 23 kDa polypeptide of oxygen-evolving complex is encoded by a multigene family in tobacco. Plant Mol Biol 18:997–999

    Article  CAS  PubMed  Google Scholar 

  • Ifuku K, Yamamoto Y, Ono T, Ishihara S, Sato F (2005) PsbP protein, but not PsbQ protein, is essential for the regulation and stabilization of photosystem II in higher plants. Plant Physiol 139:1175–1184

    Article  CAS  PubMed  Google Scholar 

  • Ishihara S, Yamamoto Y, Ifuko 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

    Article  CAS  PubMed  Google Scholar 

  • Kamiya N, Shen J-R (2003) Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-Å resolution. Proc Natl Acad Sci USA 100:98–103

    Article  CAS  PubMed  Google Scholar 

  • Kashino Y, Lauber WM, Carrol JA, Wang Q, Whitmarsh J, Satoh K, Pakrasi HB (2002) Proteomic analysis of highly active photosystem II preparation from the cyanobacterium Synechocystis sp. PCC 6803 reveals the presence of novel polypeptides. Biochemistry 41:8004–8012

    Article  CAS  PubMed  Google Scholar 

  • Keren N, Ohkawa H, Welsh EA, Liberton M, Pakrasi HB (2005) Psb29, a conserved 22-kD protein, functions in the biogenesis of photosystem II complexes in Synechocystis and Arabidopsis. Plant Cell 17:2768–2781

    Article  CAS  PubMed  Google Scholar 

  • Kieselbach T, Schröder WP (2003) The proteome of the chloroplast lumen of higher plants. Photosynth Res 78:249–264

    Article  CAS  PubMed  Google Scholar 

  • Kieselbach T, Bystedt M, Hynds P, Robinson C, Schröder WP (2000) A peroxidise homologue and novel plastocyanin located by proteomics to the Arabidopsis chloroplasts thylakoid lumen. FEBS Lett 480:271–276

    Article  CAS  PubMed  Google Scholar 

  • Kimura Y, Mizusawa N, Yamanari T, Ishii A, Ono T (2005a) Structural changes of D1 C-terminal alpha-carboxylate during S-state cycling in photosynthetic oxygen evolution. J Biol Chem 280:2078–2083

    Article  CAS  Google Scholar 

  • Kimura Y, Mizusawa N, Ishii A, Nakazawa S, Ono T (2005b) Changes in structural and functional properties of oxygen evolving complex induced by replacement of D1-glutamate 189 with glutamine in photosystem II – ligation of glutamate 189 carboxylate to the manganese cluster. J Biol Chem 280:37895–37900

    Article  CAS  Google Scholar 

  • Klimov VV, Baranov SV (2001) Bicarbonate requirement for the water-oxidizing complex of Photosystem II. Biochim Biophys Acta 1503:187–196

    Article  CAS  PubMed  Google Scholar 

  • Knoepfle N, Bricker TM, Putnam-Evans C (1999) Site-directed mutaganesis of basic arginine residues 305 and 342 in the CP43 protein of photosystem II affects oxygen-evolving activity in Synechocystis 6803. Biochemistry 38:1582–1588

    Article  CAS  PubMed  Google Scholar 

  • Kruk J, Burda K, Jemiola-Rzeminska M, Strzalka K (2003) The 33 kDa protein of photosystem II is a low-affinity calcium- and lanthanide-binding protein. Biochemistry 42:14862–14867

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Lu YK, Theg SM, Stemler AJ (2005) Carbonic anhydrase activity of the photosystem II OEC33 protein from pea. Plant Cell Physiol 46:1944–1953

    Article  CAS  PubMed  Google Scholar 

  • Lundin B, Hansson M, Schoefs B, Vener A, Spetea C (2007a) Arabidopsis PsbO2 protein regulates dephosphorylation and turnover of the photosystem II reaction centre D1 protein. Plant J 49:528–539

    Article  CAS  Google Scholar 

  • Lundin B, Thuswaldner S, Shutova T, Eshaghi S, Samuelsson G, Barber J, Andersson B, Spetea C (2007b) Subsequent events to GTP binding by the plant PsbO protein: structural changes, GTP hydrolysis and dissociation from the photosystem II complex. BBA-Bioenergetics (2006). DOI: 10.1016/j.bbabio.2006.10.009

  • Mayfield S, Bennoum P, Rochaix JD (1987) Expression of the nuclear encoded OEE1 proteins is required for oxygen evolution and stability of photosystem II particles in Chlamydomonas reinhardtii. EMBO J 6:313–318

    CAS  PubMed  Google Scholar 

  • Meetam M, Keren N, Ohad I, Pakrasi HB (1999) The PsbY protein is not essential for oxygenic photosynthesis in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol 121:1267–1272

    Article  CAS  PubMed  Google Scholar 

  • Meierhoff K, Westhoff P (1993) Differential biogenesis of photosystem II in mesophyll and bundle-sheath cells of monocotyledonous NADP-malic enzyme-type C4 plants – the nonstoichiometric abundance of the subunits of photosystem II in the bundle-sheath chloroplasts and the transcriptional activity of the plastome-encoded genes. Planta 191:23–33

    Article  CAS  Google Scholar 

  • Mizusawa N, Yamanari T, Kimura Y, Ishii A, Nakazawa S, Ono T (2004) Changes in the functional and structural properties of the Mn cluster induced by replacing the side group of the C-terminus of the D1 protein of photosystem II. Biochemistry 43:14644–14652

    Article  CAS  PubMed  Google Scholar 

  • Miyao M, Murata N (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

    Article  CAS  Google Scholar 

  • Miyao M, Murata N (1989) The mode of binding of three extrinsic proteins of 33 kDa, 23 kDa and 18 kDa in the photosystem II complex of spinach. Biochim Biophys Acta 977:315–321

    Article  CAS  Google Scholar 

  • Murakami S, Packer L (1970) Protonation and chloroplast membrane structure. J Cell Biol 47:332–351

    Article  CAS  Google Scholar 

  • Murakami R, Ifuku K, Takabayashi A, Shikanai T, Endo T, Sato F (2002) Characterization of an Arabidopsis thaliana mutant with impaired psbO, one of the two genes encoding extrinsic 33-kDa proteins in photosystem II. FEBS Lett 523:138–142

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Murray JW, Barber J (2006) Identification of a calcium-binding site in the PsbO protein of photosystem II. Biochemistry 45:4128–4130

    Article  CAS  PubMed  Google Scholar 

  • Neufeld S, Zinchenko V, Stephan DP, Bader KP, Pistorius EK (2004) On the functional significance of the polypeptide PsbY for photosynthetic water oxidation in the cyanobacterium Synechocystis sp. strain PCC 6803. Mol Gen Genomics 271:458–467

    Article  CAS  Google Scholar 

  • Nield J, Orlova E, Morris E, Gowen B, van Heel M, Barber J (2000a) 3D map of the plant photosystem II supercomplex obtained by cryoelectron microscopy and single particle analysis. Nat Struct Biol 1:44–47

    Google Scholar 

  • Nield J, Kruse O, Ruprecht J, de Fonseca P, Buchel C, Barber J (2000b) 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

    CAS  Google Scholar 

  • Nield J, Balsera M, De Las Rivas J, Barber J (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 277:15006–15012

    Article  CAS  PubMed  Google Scholar 

  • Nowaczyk M, Hebeler R, Schlodder E, Meyer H, Warscheid B, Rögner M (2006) Psb27, a cyanobacterial lipoprotein, is involved in the repair cycle of photosystem II. Plant Cell 18:3121–3131

    Article  CAS  PubMed  Google Scholar 

  • Perez-Bueno ML, Rahoutei J, Sajnani C, Garcia-Luque I, Baron 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

    Article  CAS  PubMed  Google Scholar 

  • Popelkova H, Im MM, Yocum CF (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

    Article  CAS  PubMed  Google Scholar 

  • Rahoutei J, Garcia-Luque I, Baron M (2000) Inhibition of photosynthesis by viral infection: effect on PSII structure and function. Physiol Plant 110:286–292

    Article  CAS  Google Scholar 

  • Roose JL Pakrasi HB (2004) Evidence that D1 processing is required for manganese binding and extrinsic protein assembly into photosystem II. J Biol Chem 279:45417–45422

    Article  Google Scholar 

  • Rokka A, Suorsa M, Saleem A, Battchikova N, Aro E-M (2005) Synthesis and assembly of thylakoid protein complexes: multiple assembly steps of photosystem II. Biochem J 388:159–168

    Article  CAS  PubMed  Google Scholar 

  • Rosenberg C, Christian J, Bricker TM, Putnam-Evans C (1999) Site-directed mutagenesis of glutamate residues in the large extrinsic loop of the photosystem II protein CP43 affects oxygen-evolving activity and PSII assembly. Biochemistry 38:15994–16000

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Seidler A (1996) The extrinsic polypeptides of photosystem II. Biochim Biophys Acta 1277:35–60

    Article  PubMed  Google Scholar 

  • Shen J-R, Inoue Y (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

    Article  CAS  PubMed  Google Scholar 

  • Shi L-X, Schröder WP (2004) The low molecular mass subunits of the photosynthetic supracomplex photosystem II. Biochim Biophys Acta 1608:75–96

    Article  CAS  PubMed  Google Scholar 

  • Shutova T, Irrgang K-D, Shubin V, Klimov VV, Renger G (1997) Analysis of pH-induced structural changes of the isolated extrinsic 33 kilodalton protein of photosystem II. Biochemistry 36:6350–6358

    Article  CAS  PubMed  Google Scholar 

  • Shutova T, Nikitina J, Deikus G, Andersson B, Klimov V, Samuelsson G (2005) Structural dynamics of the manganese-stabilizing protein – effect of pH, calcium, and manganese. Biochemistry 44:15182–15192

    Article  CAS  PubMed  Google Scholar 

  • Spetea C, Hundal T, Lohmann F, Andersson B (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

    Article  CAS  PubMed  Google Scholar 

  • Spetea C, Hundal T, Lundin B, Heddad M, Adamska I, Andersson B (2004) Multiple evidence for nucleotide metabolism in the chloroplast thylakoid lumen. Proc Natl Acad Sci USA 101:1409–1414

    Article  CAS  PubMed  Google Scholar 

  • Sugimoto I, Takahashi Y (2003) Evidence that the PsbK polypeptide is associated with the photosystem II core antenna complex CP43. J Biol Chem 278:45004–45010

    Article  CAS  PubMed  Google Scholar 

  • Summerfield TC, Shand JA, Bentley FK, Eaton-Rye JJ (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

    Article  CAS  PubMed  Google Scholar 

  • Suorsa M, Regel R, Paakkarinen V, Battchikova N, Herrmann RG, Aro E-M (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

    Article  CAS  PubMed  Google Scholar 

  • Suorsa M, Sirpiö S, Allahverdiyeva Y, Paakkarinen V, Mamedov F, Styring S, Aro E-M (2006) PsbR – a missing link in the assembly of the oxygen-evolving complex of plant photosystem II. J Biol Chem 281:145–150

    Article  CAS  PubMed  Google Scholar 

  • 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 particles from green alga, Chlamydomonas reinhardtii having His-tagged CP47. Plant Cell Physiol 44:76–84

    Article  CAS  PubMed  Google Scholar 

  • Suzuki T, Tada O, Makimura M, Tohri A, Ohta H, Yamamoto Y, Enami I (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

    Article  CAS  PubMed  Google Scholar 

  • Takahashi H, Ehara Y, Hirano H (1991) A protein in the oxygen-evolving complex in the chloroplast is associated with the symptom expression on tobacco leaves infected with cucumber mosaic virus strain. Plant Mol Biol 16:689–698

    Article  CAS  PubMed  Google Scholar 

  • 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 16:2154–2175

    Article  Google Scholar 

  • Tohri A, Suzuki T, Okuyama S, Kamino K, Motoki A, Hirano M, Ohta H, Shen JR, Yamamoto Y, Enami I (2002) Comparison of the structure of the extrinsic 33 kDa protein from different organisms. Plant Cell Physiol 43:429–439

    Article  CAS  PubMed  Google Scholar 

  • Villarejo A, Shutova T, Moskvin O, Forssen M, Klimov VV, Samuelsson G (2002) A photosystem II-associated carbonic anhydrase regulates the efficiency of photosynthetic oxygen evolution. EMBO J 21:1930–1938

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto Y (2001) Quality control of photosystem II. Plant Cell Physiol 42:121–128

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Young A, McChargue NM, Frankel LK, Bricker TM, Putnam-Evans C (2002) Alterations of the oxygen-evolving apparatus induced by a (305)Arg→Ser mutation in the CP43 protein of Photosystem II from Synechocystis sp. PCC 6803 under chloride-limiting conditions. Biochemistry 41:15747–15853

    Article  CAS  PubMed  Google Scholar 

  • Yu H, Yu X, Britt RD (2006) The 33 kDa protein can be removed without affecting the association of the 23 and 17 kDa proteins with the lumenal side of PS II of spinach. Biochemistry 45:3404–3011

    Article  CAS  PubMed  Google Scholar 

  • Xu Q, Bricker T (1992) Structural organization of protein on the oxidizing side of photosystem II. J Biol Chem 267:25816–25821

    CAS  PubMed  Google Scholar 

  • Zhang LX, Paakkarinen V, van Wijk KJ, Aro E-M (1999) Co-translational assembly of the D1 protein into photosystem II. J Biol Chem 274:16062–16067

    Article  CAS  PubMed  Google Scholar 

  • Zouni A, Witt H-T, Kern J, Fromme P, Krauss N, Saenger W, Orth P (2001) Crustal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution. Nature 409:739–743

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgement

We thank the Academy of Finland for funding the research in our laboratory.

Author information

Authors and Affiliations

  1. Department of Biology, Plant Physiology and Molecular Biology, University of Turku, 20014, Turku, Finland

    Marjaana Suorsa & Eva-Mari Aro

Authors
  1. Marjaana Suorsa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eva-Mari Aro
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Eva-Mari Aro.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Suorsa, M., Aro, EM. Expression, assembly and auxiliary functions of photosystem II oxygen-evolving proteins in higher plants. Photosynth Res 93, 89–100 (2007). https://doi.org/10.1007/s11120-007-9154-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-007-9154-4

Keywords

Search

Navigation