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J. Biol. Chem., Vol. 283, Issue 33, 22390-22399, August 15, 2008

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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^*

Josef Komenda¹, Jörg Nickelsen^¶, Martin Tich, Ondej Práil, Lutz A. Eichacker^||, and Peter J. Nixon^**

From the Institute of Microbiology, Academy of Sciences, Opatovick mln, 37981 Tebo, Czech Republic, the Institute of Physical Biology, University of South Bohemia, Zámek 136, 37333 Nové Hrady, Czech Republic, the ^¶Institute of Plant Molecular Biology, Ludwig-Maximilian University Munich, Menzinger Str. 67, 80368 Munich, Germany, the ^||Botanical Institute, Ludwig-Maximilian University Munich, Menzinger Str. 67, 80368 Munich, Germany, and the ^**Wolfson Biochemistry Building, Division of Biology, Faculty of Natural Sciences, Imperial College London, S. Kensington Campus, London SW7 2AZ, United Kingdom

The role of the slr2034 (ycf48) gene product in the assembly and repair of photosystem II (PSII) has been studied in the cyanobacterium Synechocystis PCC 6803. YCF48 (HCF136) is involved in the assembly of Arabidopsis thaliana PSII reaction center (RC) complexes but its mode of action is unclear. We show here that YCF48 is a component of two cyanobacterial PSII RC-like complexes in vivo and is absent in larger PSII core complexes. Interruption of ycf48 slowed the formation of PSII complexes in wild type, as judged from pulse-labeling experiments, and caused a decrease in the final level of PSII core complexes in wild type and a marked reduction in the levels of PSII assembly complexes in strains lacking either CP43 or CP47. Absence of YCF48 also led to a dramatic decrease in the levels of the COOH-terminal precursor (pD1) and the partially processed form, iD1, in a variety of PSII mutants and only low levels of unassembled mature D1 were observed. Yeast two-hybrid analyses using the split ubiquitin system showed an interaction of YCF48 with unassembled pD1 and, to a lesser extent, unassembled iD1, but not with unassembled mature D1 or D2. Overall our results indicate a role for YCF48 in the stabilization of newly synthesized pD1 and in its subsequent binding to a D2-cytochrome b₅₅₉ pre-complex, also identified in this study. Besides a role in assembly, we show for the first time that YCF48 also functions in the selective replacement of photodamaged D1 during PSII repair.

Received for publication, March 10, 2008 , and in revised form, June 10, 2008.

^* The work was supported by the Grant Agency of the Czech Republic Project number 206/06/0322 (to J. K.), Ministry of Education, Youth and Sports of the Czech Republic Project number MSM6007665808 (to M. T.), Czech Academy of Sciences Grants AV0Z50200510 (to O. P.) and IAA400200801 (to J. K.), and the Biotechnology and Biological Sciences Research Council (to P. J. N.). 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.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Table S1 and Figs. S1–S7.

¹ To whom correspondence should be addressed: Institute of Microbiology, Opatovicky mlyn, 37981 Trebon, Czech Republic. Tel.: 420-384340431; Fax: 420-384340415; E-mail: komenda{at}alga.cz.

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