The Psb27 assembly factor binds to the CP43 complex of photosystem II in the cyanobacterium Synechocystis sp. PCC 6803
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
Grantová podpora
BB/F020554/1
Biotechnology and Biological Sciences Research Council - United Kingdom
PubMed
22086423
PubMed Central
PMC3252115
DOI
10.1104/pp.111.184184
PII: pp.111.184184
Knihovny.cz E-zdroje
- MeSH
- bakteriální proteiny genetika metabolismus MeSH
- fotosystém I - proteinový komplex metabolismus MeSH
- fotosystém II - proteinový komplex genetika metabolismus MeSH
- multiproteinové komplexy metabolismus MeSH
- mutace MeSH
- stabilita proteinů MeSH
- Synechocystis metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- bakteriální proteiny MeSH
- fotosystém I - proteinový komplex MeSH
- fotosystém II - proteinový komplex MeSH
- multiproteinové komplexy MeSH
- photosystem II, chlorophyll binding protein, CP-43 MeSH Prohlížeč
We have investigated the location of the Psb27 protein and its role in photosystem (PS) II biogenesis in the cyanobacterium Synechocystis sp. PCC 6803. Native gel electrophoresis revealed that Psb27 was present mainly in monomeric PSII core complexes but also in smaller amounts in dimeric PSII core complexes, in large PSII supercomplexes, and in the unassembled protein fraction. We conclude from analysis of assembly mutants and isolated histidine-tagged PSII subcomplexes that Psb27 associates with the "unassembled" CP43 complex, as well as with larger complexes containing CP43, possibly in the vicinity of the large lumenal loop connecting transmembrane helices 5 and 6 of CP43. A functional role for Psb27 in the biogenesis of CP43 is supported by the decreased accumulation and enhanced fragmentation of unassembled CP43 after inactivation of the psb27 gene in a mutant lacking CP47. Unexpectedly, in strains unable to assemble PSII, a small amount of Psb27 comigrated with monomeric and trimeric PSI complexes upon native gel electrophoresis, and Psb27 could be copurified with histidine-tagged PSI isolated from the wild type. Yeast two-hybrid assays suggested an interaction of Psb27 with the PsaB protein of PSI. Pull-down experiments also supported an interaction between CP43 and PSI. Deletion of psb27 did not have drastic effects on PSII assembly and repair but did compromise short-term acclimation to high light. The tentative interaction of Psb27 and CP43 with PSI raises the possibility that PSI might play a previously unrecognized role in the biogenesis/repair of PSII.
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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 complex. Proc Natl Acad Sci USA 91: 8082–8086 PubMed PMC
Barber J. (2006) Photosystem II: an enzyme of global significance. Biochem Soc Trans 34: 619–631 PubMed
Bibby TS, Nield J, Barber J. (2001) Iron deficiency induces the formation of an antenna ring around trimeric photosystem I in cyanobacteria. Nature 412: 743–745 PubMed
Boehm M, Romero E, Reisinger V, Yu J, Komenda J, Eichacker LA, Dekker JP, Nixon PJ. (2011) Investigating the early stages of photosystem II assembly in Synechocystis sp. PCC 6803: isolation of CP47 and CP43 complexes. J Biol Chem 286: 14812–14819 PubMed PMC
Boekema EJ, Hifney A, Yakushevska AE, Piotrowski M, Keegstra W, Berry S, Michel KP, Pistorius EK, Kruip J. (2001) A giant chlorophyll-protein complex induced by iron deficiency in cyanobacteria. Nature 412: 745–748 PubMed
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 PubMed
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 PubMed
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 PubMed PMC
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 PubMed
Fagerlund RD, Eaton-Rye JJ. (2011) The lipoproteins of cyanobacterial photosystem II. J Photochem Photobiol B 104: 191–203 PubMed
Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S. (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303: 1831–1838 PubMed
Grasse N, Mamedov F, Becker K, Styring S, Rögner M, Nowaczyk MM. (2011) Role of novel dimeric photosystem II (PSII)-Psb27 protein complex in PSII repair. J Biol Chem 286: 29548–29555 PubMed PMC
Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A, Saenger W. (2009) Cyanobacterial photosystem II at 2.9-A resolution and the role of quinones, lipids, channels and chloride. Nat Struct Mol Biol 16: 334–342 PubMed
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 PubMed
Kashino Y, Lauber WM, Carroll JA, Wang Q, Whitmarsh J, Satoh K, Pakrasi HB. (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 PubMed
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 PubMed
Komenda J, Barker M, Kuviková S, de Vries R, Mullineaux CW, Tichý M, Nixon PJ. (2006) The FtsH protease slr0228 is important for quality control of photosystem II in the thylakoid membrane of Synechocystis sp. PCC 6803. J Biol Chem 281: 1145–1151 PubMed
Komenda J, Kuviková S, Granvogl B, Eichacker LA, Diner BA, Nixon PJ. (2007) Cleavage after residue Ala352 in the C-terminal extension is an early step in the maturation of the D1 subunit of photosystem II in Synechocystis PCC 6803. Biochim Biophys Acta 1767: 829–837 PubMed
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. Eur J Biochem 269: 610–619 PubMed
Komenda J, Nickelsen J, Tichý M, Prásil O, Eichacker LA, Nixon PJ. (2008) The cyanobacterial homologue of HCF136/YCF48 is a component of an early photosystem II assembly complex and is important for both the efficient assembly and repair of photosystem II in Synechocystis sp. PCC 6803. J Biol Chem 283: 22390–22399 PubMed
Komenda J, Reisinger V, Müller BC, Dobáková M, Granvogl B, Eichacker LA. (2004) Accumulation of the D2 protein is a key regulatory step for assembly of the photosystem II reaction center complex in Synechocystis PCC 6803. J Biol Chem 279: 48620–48629 PubMed
Kubota H, Sakurai I, Katayama K, Mizusawa N, Ohashi S, Kobayashi M, Zhang P, Aro EM, Wada H. (2010) Purification and characterization of photosystem I complex from Synechocystis sp. PCC 6803 by expressing histidine-tagged subunits. Biochim Biophys Acta 1797: 98–105 PubMed
Liu H, Huang RYC, Chen J, Gross ML, Pakrasi HB. (2011a) Psb27, a transiently associated protein, binds to the chlorophyll-binding protein in photosystem II assembly intermediates. Proc Natl Acad Sci USA http://dx.doi.org/10.1073/pnas.1111597108 PubMed DOI PMC
Liu H, Roose JL, Cameron JC, Pakrasi HB. (2011b) A genetically tagged Psb27 protein allows purification of two consecutive photosystem II (PSII) assembly intermediates in Synechocystis 6803, a cyanobacterium. J Biol Chem 286: 24865–24871 PubMed PMC
Lupínková L, Komenda J. (2004) Oxidative modifications of the photosystem II D1 protein by reactive oxygen species: from isolated protein to cyanobacterial cells. Photochem Photobiol 79: 152–162 PubMed
Mabbitt PD, Rautureau GJP, Day CL, Wilbanks SM, Eaton-Rye JJ, Hinds MG. (2009) Solution structure of Psb27 from cyanobacterial photosystem II. Biochemistry 48: 8771–8773 PubMed
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 PubMed
Marder JB, Goloubinoff P, Edelman M. (1984) Molecular architecture of the rapidly metabolized 32-kilodalton protein of photosystem II. Indications for COOH-terminal processing of a chloroplast membrane polypeptide. J Biol Chem 259: 3900–3908 PubMed
Melkozernov AN, Bibby TS, Lin S, Barber J, Blankenship RE. (2003) Time-resolved absorption and emission show that the CP43′ antenna ring of iron-stressed synechocystis sp. PCC6803 is efficiently coupled to the photosystem I reaction center core. Biochemistry 42: 3893–3903 PubMed
Nixon PJ, Trost JT, Diner BA. (1992) Role of the carboxy terminus of polypeptide D1 in the assembly of a functional water-oxidizing manganese cluster in photosystem II of the cyanobacterium Synechocystis sp. PCC 6803: Assembly requires a free carboxyl group at C-terminal position 344. Biochemistry 31: 10859–10871 PubMed
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 PubMed PMC
Nowaczyk MM, Sander J, Grasse N, Cormann KU, Rexroth D, Bernát G, Rögner M. (2010) Dynamics of the cyanobacterial photosynthetic network: communication and modification of membrane protein complexes. Eur J Cell Biol 89: 974–982 PubMed
Pakrasi HB, Williams JGK, Arntzen CJ. (1988) Targeted mutagenesis of the psbE and psbF genes blocks photosynthetic electron transport: evidence for a functional role of cytochrome b559 in photosystem II. EMBO J 7: 325–332 PubMed PMC
Pasch JC, Nickelsen J, Schünemann D. (2005) The yeast split-ubiquitin system to study chloroplast membrane protein interactions. Appl Microbiol Biotechnol 69: 440–447 PubMed
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 PubMed
Roose JL, Pakrasi HB. (2008) The Psb27 protein facilitates manganese cluster assembly in photosystem II. J Biol Chem 283: 4044–4050 PubMed
Roose JL, Wegener KM, Pakrasi HB. (2007) The extrinsic proteins of photosystem II. Photosynth Res 92: 369–387 PubMed
Schägger H, von Jagow G. (1991) Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal Biochem 199: 223–231 PubMed
Shen G, Boussiba S, Vermaas WFJ. (1993) Synechocystis sp PCC 6803 strains lacking photosystem I and phycobilisome function. Plant Cell 5: 1853–1863 PubMed PMC
Takahashi M, Shiraishi T, Asada K. (1988) COOH-terminal residues of D1 and the 44 kDa CPa-2 at spinach photosystem II core complex. FEBS Lett 240: 6–8 PubMed
Umena Y, Kawakami K, Shen J-R, Kamiya N. (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473: 55–60 PubMed
Vermaas WFJ, Ikeuchi M, Inoue Y. (1988) Protein composition of the photosystem II core complex in genetically engineered mutants of the cyanobacterium Synechocystis sp. PCC 6803. Photosynth Res 17: 97–113 PubMed
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 PubMed PMC
Wellburn AR, Lichtenthaler K. (1984) Formulae and programme to determine total carotenoids and chlorophyll a and b of leaf extracts in different solvents. Sybesma C, , Advances in Photosynthesis Research, Martinus Nijjhoff, Dordrecht, The Netherlands, pp 10–12
Williams JGK. (1988) Construction of specific mutations in PSII photosynthetic reaction center by genetic engineering methods in Synechocystis 6803. Methods Enzymol 167: 766–778
Zhang ZH, Mayes SR, Vass I, Nagy L, Barber J. (1993) Characterization of the psbK locus of Synechocystis PCC 6803 in terms of photosystem II function. Photosynth Res 38: 369–377 PubMed
Zouni A, Witt HT, Kern J, Fromme P, Krauss N, Saenger W, Orth P. (2001) Crystal structure of photosystem II from Synechococcus elongatus at 3.8 A resolution. Nature 409: 739–743 PubMed
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