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A role of the C-terminal extension of the photosystem II D1 protein in sensitivity of the cyanobacterium Synechocystis PCC 6803 to photoinhibition

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Abstract

The D1 protein, a key protein subunit of Photosystem II complex (PSII), is synthesised as a precursor (pD1) with a carboxyl-terminal extension. In the cyanobacterium Synechocystis sp. PCC 6803, this extension consists of 16 amino acid residues and it is cleaved by a specific protease in two putative steps with the final cleavage after the residue Ala344. In order to define the importance of the extension for the functioning of PSII, we constructed and characterized several site-directed mutants of Synechocystis that differ in the length and amino acid sequence of this extension. The mutant lacking the entire C-terminal extension exhibited slightly increased sensitivity to photoinhibition. Analysis of the PSII assembly in the mutant by the blue-native electrophoresis in combination with radioactive labelling revealed an increased level of the unassembled D1 protein in this strain. Replacement of the amino acid residue Asn359 by His or Asp also led to the higher vulnerability to photoinhibition of both mutants. In the Asn359His mutant, this vulnerability was accompanied by an increased level of the PSII core lacking CP43 indicating limitation of the repair cycle in the CP43 reassembly step.

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References

  1. A. K. Mattoo, J. B. Marder and M. Edelman, Dynamics of the photosystem II reaction center Cell 1989 56 241–246

    Article  CAS  Google Scholar 

  2. L. Zhang and E. M. Aro, Synthesis membrane insertion and assembly of the chloroplast-encoded D1 protein into photosystem II FEBS Lett. 2002 512 13–18

    Article  CAS  Google Scholar 

  3. M. Takahashi, T. Shiraishi and K. Asada, COOH-terminal residues of D1 and the 44-kDa CPa-2 at spinach photosystem II core complex FEBS Lett. 1988 240 6–8

    Article  CAS  Google Scholar 

  4. P. N. Nixon, J. T. Trost and B. A. Diner, 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 1992 31 10859–10871

    Article  CAS  Google Scholar 

  5. B. Svensson, I. Vass and S. Styring, Sequence analysis of the D1 and D2 reaction center proteins of Photosystem II Z. Naturforsch., C: Biosci. 1991 46 765–776

    Article  CAS  Google Scholar 

  6. J. T. Trost, D. A. Chisholm, D. B. Jordan and B. A. Diner, The D1 C-terminal Processing Protease of Photosystem II from Scenedesmus obliquus J. Biol. Chem. 1997 272 20348–20356

    Article  CAS  Google Scholar 

  7. F. Taguchi, Y. Yamamoto, N. Inagaki and K. Satoh, Recognition signal for the C-terminal processing protease of D1 precursor protein in the photosystem II reaction center FEBS Lett. 1993 326 227–231

    Article  CAS  Google Scholar 

  8. 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. 2004 279 45417–45422

    Article  CAS  Google Scholar 

  9. K. C. Keiler, P. R. H. Waller and R. T. Bauer, Role of a peptide tagging system in degradation of proteins synthesized from damaged messenger RNA Science 1996 271 990–993

    Article  CAS  Google Scholar 

  10. Y. Yamamoto, N. Inagaki and K. Satoh, Overexpression and characterization of carboxyl-terminal processing protease for precursor D1 protein - Regulation of enzyme-substrate interaction by molecular environments J. Biol. Chem. 2001 276 7518–7525

    Article  CAS  Google Scholar 

  11. N. Inagaki, Y. Yamamoto and K. Satoh, A sequential two-step proteolytic process in the carboxyl-terminal truncation of precursor D1 protein in Synechocystis sp. PCC 6803 FEBS Lett. 2001 509 197–201

    Article  CAS  Google Scholar 

  12. N. B. Ivleva, S. V. Shestakov and H. B. Pakrasi, The Carboxyl-Terminal Extension of the Precursor D1 Protein of Photosystem II Is Required for Optimal Photosynthetic Performance of the Cyanobacterium Synechocystis sp. PCC 6803 Plant Physiol. 2000 124 1403–1411

    Article  CAS  Google Scholar 

  13. O. Prášil, N. Adir and I. Ohad, in Topics in Photosynthesis, ed. J. Barber, Elsevier Science Publ. Amsterdam, 1992, pp. 295-348

  14. J. Barber, Photosystem two Biochim. Biophys. Acta 1998 1365 269–277

    Article  CAS  Google Scholar 

  15. J. G. K. Williams, Construction of specific mutations in PSII photosynthetic reaction center by genetic engineering methods in Synechocystis 6803 Methods Enzymol. 1988 167 766–778

    Article  CAS  Google Scholar 

  16. H. B. Pakrasi, J. G. K. Williams and C. J. Arntzen, Targeted mutagenesis of the psbE and psbF blocks photosynthetic electron transport: evidence for a functional role of cytochrome b-559 in photosystem II EMBO J. 1988 7 325–332

    Article  CAS  Google Scholar 

  17. S. H. Ke and E. L. Madison, Rapid and efficient site-directed mutagenesis by single-tube ‘megaprimer’ PCR method Nucleic Acids Res. 1997 25 3371–3372

    Article  CAS  Google Scholar 

  18. M. Tichý, L. Lup’inková, C. Sicora, I. Vass, S. Kuviková, O. Prášil and J. Komenda, Synechocystis 6803 mutants expressing distinct forms of the Photosystem II D1 protein from Synechococcus 7942: Relationship between the psbA coding region and sensitivity to visible and UV-B radiation Biochim. Biophys. Acta 2003 1605 55–66

    Article  Google Scholar 

  19. J. Komenda, L. Lup’inková, J. Kopecký Absence of the psbH gene product destabilizes photosystem II complex and bicarbonate binding on its acceptor side in Synechocystis PCC 6803 Eur. J. Biochem. 2002 269 610–619

    Article  CAS  Google Scholar 

  20. H. Schagger, G. Von Jagow Blue native electrophoresis for isolation of membrane-protein complexes in enzymatically active form Anal. Biochem. 1991 199 223–231

    Article  CAS  Google Scholar 

  21. J. Komenda, V. Reisinger, B. Ch. Müller, M. Dobáková, B. Granvogl and L. A. Eichacker, 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. 2004 279 48620–48629

    Article  CAS  Google Scholar 

  22. A. R. Wellburn and K. Lichtenthaler, in Advances In Photosynthesis Research, vol. 2, ed. C. Sybesma, Martinus Nijjhoff, Dordrecht, 1984, pp. 10-12

  23. S. S. Golden, J. Brusslan and R. Haselkorn, Expression of a family of psbA genes encoding a photosystem II polypeptide in the cyanobacterium Anacystis nidulans R2 EMBO J. 1986 5 2789–2798

    Article  CAS  Google Scholar 

  24. J. Komenda, Role of two forms of the D1 protein in the recovery from photoinhibition of Photosystem II in the cyanobacterium Synechococcus PCC 7942 Biochim. Biophys. Acta 2000 1457 243–252

    Article  CAS  Google Scholar 

  25. B. Klinkert, F. Ossenbühl, M. Sikorski, S. Berry, L. Eichacker and J. Nickelsen, PratA, a periplasmic tetratricopeptide repeat protein involved in biogenesis of Photosystem II in Synechocystis sp. PCC 6803 J. Biol. Chem. 2004 279 44639–44644

    Article  CAS  Google Scholar 

  26. K. N. Ferreira, T. M. Iverson, K. Maghlaoui, J. Barber and S. Iwata, Architecture of the photosynthetic oxygen-evolving center Science 2004 303 1831–1838

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Institute of Microbiology, Academy of Sciences, Opatovický mlýn, 37981, Třeboň, Czech Republic

    Stanislava Kuviková, Martin Tichý & Josef Komenda

  2. Institute of Physical Biology, University of South Bohemia, Zámek 136, 37333, Nové Hrady, Czech Republic

    Stanislava Kuviková, Martin Tichý & Josef Komenda

Authors
  1. Stanislava Kuviková
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  2. Martin Tichý
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  3. Josef Komenda
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Correspondence to Josef Komenda.

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Dedicated to Professor James Barber on the occasion of his 65th birthday.

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Kuviková, S., Tichý, M. & Komenda, J. A role of the C-terminal extension of the photosystem II D1 protein in sensitivity of the cyanobacterium Synechocystis PCC 6803 to photoinhibition. Photochem Photobiol Sci 4, 1044–1048 (2005). https://doi.org/10.1039/b506059a

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