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J. Biol. Chem., Vol. 281, Issue 2, 1145-1151, January 13, 2006

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The FtsH Protease slr0228 Is Important for Quality Control of Photosystem II in the Thylakoid Membrane of Synechocystis sp. PCC 6803^*

Josef Komenda¶1, Myles Barker, Stanislava Kuviková¶, Remco de Vries, Conrad W. Mullineaux||, Martin Tich¶, and Peter J. Nixon

From the ^¶Institute of Microbiology, Academy of Sciences, Opatovick mln, 37981 Tebo, Czech Republic, Institute of Physical Biology, University of South Bohemia, Zámek 136, 37333 Nové Hrady, Czech Republic,Wolfson Biochemistry Building, Division of Biology, Faculty of Life Sciences, Imperial College London, South Kensington Campus, London SW7 2AZ, United Kingdom, and ^||School of Biological Sciences, Queen Mary, University of London, Mile End Road, London E1 4NS, United Kingdom

The cyanobacterium Synechocystis sp. PCC 6803 contains four members of the FtsH protease family. One of these, FtsH (slr0228), has been implicated recently in the repair of photodamaged photosystem II (PSII) complexes. We have demonstrated here, using a combination of blue native PAGE, radiolabeling, and immunoblotting, that FtsH (slr0228) is required for selective replacement of the D1 reaction center subunit in both wild type PSII complexes and in PSII subcomplexes lacking the PSII chlorophyll a-binding subunit CP43. To test whether FtsH (slr0228) has a more general role in protein quality control in vivo, we have studied the synthesis and degradation of PSII subunits in wild type and in defined insertion and missense mutants incapable of proper assembly of the PSII holoenzyme. We discovered that, when the gene encoding FtsH (slr0228) was disrupted in these strains, the overall level of assembly intermediates and unassembled PSII proteins markedly increased. Pulse-chase experiments showed that this was due to reduced rates of degradation in vivo. Importantly, analysis of epitope-tagged and green fluorescent protein-tagged strains revealed that slr0228 was present in the thylakoid and not the cytoplasmic membrane. Overall, our results show that FtsH (slr0228) plays an important role in controlling the removal of PSII subunits from the thylakoid membrane and is not restricted to selective D1 turnover.

Received for publication, April 8, 2005 , and in revised form, November 11, 2005.

^* This work was supported by the Grant Agency of the Czech Republic (Project 203/04/0800) (to J. K.), by the Ministry of Education, Youth, and Sports of the Czech Republic (Project MSM6007665808) (to M. T.), by the Czech Academy of Sciences (Institutional Research Concept AV0Z50200510) (to J. K. and M. T.), by the Biotechnology and Biological Sciences Research Council (to P. J. N.), and the Wellcome Trust (to C. W. M.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

¹ To whom correspondence should be addressed: Institute of Microbiology, Opatovicky mlyn, 37981 Trebon, Czech Republic. Tel.: 420-384721101; Fax: 420-384721246; E-mail: komenda{at}alga.cz.

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