Pitt, a novel tetratricopeptide repeat protein involved in light-dependent chlorophyll biosynthesis and thylakoid membrane biogenesis in Synechocystis sp. PCC 6803.

Biogenesis of photosynthetic pigment/protein complexes is a highly regulated process that requires various assisting factors. Here, we report on the molecular analysis of the Pitt gene (slr1644) from the cyanobacterium Synechocystis sp. PCC 6803 (Synechocystis 6803) that encodes a membrane-bound tetratricopeptide repeat (TPR) protein of formerly unknown function. Targeted inactivation of Pitt affected photosynthetic performance and light-dependent chlorophyll synthesis. Yeast two-hybrid analyses and native PAGE strongly suggest a complex formation between Pitt and the light-dependent protochlorophyllide oxidoreductase (POR). Consistently, POR levels are approximately threefold reduced in the pitt insertion mutant. The membrane sublocalization of Pitt was found to be dependent on the presence of the periplasmic photosystem II (PSII) biogenesis factor PratA, supporting the idea that Pitt is involved in the early steps of photosynthetic pigment/protein complex formation.

[1]  J. Nickelsen,et al.  Interaction of the Periplasmic PratA Factor and the PsbA (D1) Protein during Biogenesis of Photosystem II in Synechocystis sp. PCC 6803* , 2009, Journal of Biological Chemistry.

[2]  M. Alexandre,et al.  Conformational changes in an ultrafast light-driven enzyme determine catalytic activity , 2008, Nature.

[3]  C. Laloi,et al.  No single way to understand singlet oxygen signalling in plants , 2008, EMBO reports.

[4]  Jean-Michel Claverie,et al.  Phylogeny.fr: robust phylogenetic analysis for the non-specialist , 2008, Nucleic Acids Res..

[5]  O. Belyaeva,et al.  Photoactive pigment—enzyme complexes of chlorophyll precursor in plant leaves , 2007, Biochemistry (Moscow).

[6]  Yasukazu Nakamura,et al.  A Large-scale Protein–protein Interaction Analysis in Synechocystis sp. PCC6803 , 2007, DNA research : an international journal for rapid publication of reports on genes and genomes.

[7]  D. Bryant,et al.  Chlorophyll biosynthesis in bacteria: the origins of structural and functional diversity. , 2007, Annual review of microbiology.

[8]  A. Wilde,et al.  Late Assembly Steps and Dynamics of the Cyanobacterial Photosystem I* , 2007, Journal of Biological Chemistry.

[9]  José G García-Cerdán,et al.  REP27, a Tetratricopeptide Repeat Nuclear-Encoded and Chloroplast-Localized Protein, Functions in D1/32-kD Reaction Center Protein Turnover and Photosystem II Repair from Photodamage1[OA] , 2007, Plant Physiology.

[10]  R. Oelmüller,et al.  The Evolutionarily Conserved Tetratrico Peptide Repeat Protein Pale Yellow Green7 Is Required for Photosystem I Accumulation in Arabidopsis and Copurifies with the Complex1 , 2006, Plant Physiology.

[11]  Q. Lu,et al.  LOW PSII ACCUMULATION1 Is Involved in Efficient Assembly of Photosystem II in Arabidopsis thaliana[W] , 2006, The Plant Cell Online.

[12]  C. Hunter,et al.  Making light work of enzyme catalysis: protochlorophyllide oxidoreductase. , 2005, Trends in biochemical sciences.

[13]  A. P. Sane,et al.  The nuclear gene HCF107 encodes a membrane-associated R-TPR (RNA tetratricopeptide repeat)-containing protein involved in expression of the plastidial psbH gene in Arabidopsis. , 2005, The Plant journal : for cell and molecular biology.

[14]  N. Keren,et al.  Photochemical Competence of Assembled Photosystem II Core Complex in Cyanobacterial Plasma Membrane* , 2005, Journal of Biological Chemistry.

[15]  A. Ben-Shem,et al.  The complex architecture of oxygenic photosynthesis , 2004, Nature Reviews Molecular Cell Biology.

[16]  J. Nickelsen,et al.  PratA, a Periplasmic Tetratricopeptide Repeat Protein Involved in Biogenesis of Photosystem II in Synechocystis sp. PCC 6803* , 2004, Journal of Biological Chemistry.

[17]  Lynne Regan,et al.  TPR proteins: the versatile helix. , 2003, Trends in biochemical sciences.

[18]  H. Aronsson,et al.  POR - import and membrane association of a key element in chloroplast development. , 2003, Physiologia plantarum.

[19]  K. Apel,et al.  Interaction of FLU, a negative regulator of tetrapyrrole biosynthesis, with the glutamyl‐tRNA reductase requires the tetratricopeptide repeat domain of FLU , 2002, FEBS letters.

[20]  Y. Kanesaki,et al.  Salt Stress Inhibits the Repair of Photodamaged Photosystem II by Suppressing the Transcription and Translation of psbAGenes in Synechocystis 1 , 2002, Plant Physiology.

[21]  K. Apel,et al.  FLU: A negative regulator of chlorophyll biosynthesis in Arabidopsis thaliana , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[22]  A. Wilde,et al.  Characterization of the cyanobacterial ycf37: mutation decreases the photosystem I content. , 2001, The Biochemical journal.

[23]  J. Rochaix,et al.  Characterization of Mbb1, a nucleus-encoded tetratricopeptide-like repeat protein required for expression of the chloroplast psbB/psbT/psbH gene cluster in Chlamydomonas reinhardtii. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[24]  J. Nickelsen,et al.  The Nac2 gene of Chlamydomonas encodes a chloroplast TPR‐like protein involved in psbD mRNA stability , 2000, The EMBO journal.

[25]  W. Rüdiger,et al.  Pigment-free NADPH:protochlorophyllide oxidoreductase from Avena sativa L. Purification and substrate specificity. , 1999, European journal of biochemistry.

[26]  D. Brune,et al.  CHLOROPHYLL A SYNTHESIS UPON INTERRUPTION AND DELETION OF POR CODING FOR THE LIGHT-DEPENDENT NADPH:PROTOCHLOROPHYLLIDE OXIDOREDUCTASE IN A PHOTOSYSTEM -I-LESS/CHLL- STRAIN OF SYNECHOCYSTIS SP. PCC 6803 , 1998 .

[27]  T. Hase,et al.  Cloning of the gene encoding a protochlorophyllide reductase: the physiological significance of the co-existence of light-dependent and -independent protochlorophyllide reduction systems in the cyanobacterium Plectonema boryanum. , 1998, Plant & cell physiology.

[28]  J. Rochaix,et al.  The chloroplast ycf3 and ycf4 open reading frames of Chlamydomonas reinhardtii are required for the accumulation of the photosystem I complex , 1997, The EMBO journal.

[29]  R. Bock,et al.  Targeted Inactivation of a Tobacco Intron–containing Open Reading Frame Reveals a Novel Chloroplast-encoded Photosystem I–related Gene , 1997, The Journal of cell biology.

[30]  L. Mcintosh,et al.  Targeted genetic inactivation of the photosystem I reaction center in the cyanobacterium Synechocystis sp. PCC 6803. , 1991, The EMBO journal.

[31]  R. Moran Formulae for determination of chlorophyllous pigments extracted with n,n-dimethylformamide. , 1982, Plant physiology.

[32]  A. Wilde,et al.  Analysis of photosynthetic complexes from a cyanobacterial ycf37 mutant. , 2006, Biochimica et biophysica acta.

[33]  T. Masuda,et al.  Novel Insights into the Enzymology, Regulation and Physiological Functions of Light-dependent Protochlorophyllide Oxidoreductase in Angiosperms , 2004, Photosynthesis Research.

[34]  V. Melnik,et al.  Vectors for the complementation analysis of cyanobacterial mutants , 1999 .