HCF243 Encodes a Chloroplast-Localized Protein Involved in the D1 Protein Stability of the Arabidopsis Photosystem II Complex1[W][OA]

Numerous auxiliary nuclear factors have been identified to be involved in the dynamics of the photosystem II (PSII) complex. In this study, we characterized the high chlorophyll fluorescence243 (hcf243) mutant of Arabidopsis (Arabidopsis thaliana), which shows higher chlorophyll fluorescence and is severely deficient in the accumulation of PSII supercomplexes compared with the wild type. The amount of core subunits was greatly decreased, while the outer antenna subunits and other subunits were hardly affected in hcf243. In vivo protein-labeling experiments indicated that the synthesis rate of both D1 and D2 proteins decreased severely in hcf243, whereas no change was found in the rate of other plastid-encoded proteins. Furthermore, the degradation rate of the PSII core subunit D1 protein is higher in hcf243 than in the wild type, and the assembly of PSII is retarded significantly in the hcf243 mutant. HCF243, a nuclear gene, encodes a chloroplast protein that interacts with the D1 protein. HCF243 homologs were identified in angiosperms with one or two copies but were not found in lower plants and prokaryotes. These results suggest that HCF243, which arose after the origin of the higher plants, may act as a cofactor to maintain the stability of D1 protein and to promote the subsequent assembly of the PSII complex.

[1]  Yasusi Yamamoto,et al.  Quality control of Photosystem II: where and how does the degradation of the D1 protein by FtsH proteases start under light stress?--Facts and hypotheses. , 2011, Journal of photochemistry and photobiology. B, Biology.

[2]  J. Nickelsen,et al.  The Arabidopsis Thylakoid Protein PAM68 Is Required for Efficient D1 Biogenesis and Photosystem II Assembly[W] , 2010, Plant Cell.

[3]  Joel Dudley,et al.  MEGA: A biologist-centric software for evolutionary analysis of DNA and protein sequences , 2008, Briefings Bioinform..

[4]  A. Melis,et al.  Photoinhibition and Recovery in Oxygenic Photosynthesis: Mechanism of a Photosystem II Damage and Repair Cycle , 2008 .

[5]  M. Nei,et al.  MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. , 2007, Molecular biology and evolution.

[6]  Q. Lu,et al.  Retracted: LPA2 Is Required for Efficient Assembly of Photosystem II in Arabidopsis thaliana , 2007, Plant Cell.

[7]  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.

[8]  J. Meurer,et al.  The Synechocystis sp PCC 6803 Oxa1 Homolog Is Essential for Membrane Integration of Reaction Center Precursor Protein pD1[W] , 2006, The Plant Cell Online.

[9]  Nathan Nelson,et al.  Structure and function of photosystems I and II. , 2006, Annual review of plant biology.

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

[11]  Peer Bork,et al.  SMART 5: domains in the context of genomes and networks , 2005, Nucleic Acids Res..

[12]  E. Welsh,et al.  Psb29, a Conserved 22-kD Protein, Functions in the Biogenesis of Photosystem II Complexes in Synechocystis and Arabidopsisw⃞ , 2005, The Plant Cell Online.

[13]  Zhuzhu Zhang,et al.  Decreased stability of photosystem I in dgd1 mutant of Arabidopsis thaliana , 2005, FEBS letters.

[14]  M. Suorsa,et al.  Synthesis and assembly of thylakoid protein complexes: multiple assembly steps of photosystem II. , 2005, The Biochemical journal.

[15]  T. Tzfira,et al.  Involvement of targeted proteolysis in plant genetic transformation by Agrobacterium , 2004, Nature.

[16]  J. Barber,et al.  Structure of photosystem II and molecular architecture of the oxygen-evolving centre. , 2004, Current opinion in structural biology.

[17]  R. Herrmann,et al.  Protein assembly of photosystem II and accumulation of subcomplexes in the absence of low molecular mass subunits PsbL and PsbJ. , 2003, European journal of biochemistry.

[18]  P. Westhoff,et al.  Isolation of high-chlorophyll-fluorescence mutants ofArabidopsis thaliana and their characterisation by spectroscopy, immunoblotting and Northern hybridisation , 2004, Planta.

[19]  Z. Zhang,et al.  Blue native gel electrophoresis analysis of chloroplast pigment protein complexes (SCI) , 2003 .

[20]  Dario Leister,et al.  Chloroplast research in the genomic age. , 2003, Trends in genetics : TIG.

[21]  Peter Westhoff,et al.  The HCF136 protein is essential for assembly of the photosystem II reaction center in Arabidopsis thaliana , 2002, FEBS letters.

[22]  F. Wollman,et al.  Translational regulations as specific traits of chloroplast gene expression , 2002, FEBS letters.

[23]  A. Clarke,et al.  Cutting edge of chloroplast proteolysis. , 2002, Trends in plant science.

[24]  S. Yalovsky,et al.  A Cell-Specific, Prenylation-Independent Mechanism Regulates Targeting of Type II RACs Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.005561. , 2002, The Plant Cell Online.

[25]  R. Bock,et al.  Lack of the Small Plastid-encoded PsbJ Polypeptide Results in a Defective Water-splitting Apparatus of Photosystem II, Reduced Photosystem I Levels, and Hypersensitivity to Light* , 2002, The Journal of Biological Chemistry.

[26]  Chang‐Deng Hu,et al.  Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular fluorescence complementation. , 2002, Molecular cell.

[27]  J. Rochaix.  Assembly,function, and dynamics of the photosynthetic machinery in Chlamydomonas reinhardtii. , 2001, Plant physiology.

[28]  P. Westhoff,et al.  HCF164 encodes a thioredoxin-like protein involved in the biogenesis of the cytochrome b(6)f complex in Arabidopsis. , 2001, The Plant cell.

[29]  K. Cline,et al.  Thylakoid ΔpH-dependent precursor proteins bind to a cpTatC–Hcf106 complex before Tha4-dependent transport , 2001, The Journal of cell biology.

[30]  K. V. van Wijk,et al.  Biogenesis of the Chloroplast-Encoded D1 Protein: Regulation of Translation Elongation, Insertion, and Assembly into Photosystem II , 2000, Plant Cell.

[31]  A. Barkan,et al.  Participation of nuclear genes in chloroplast gene expression. , 2000, Biochimie.

[32]  O. Vallon,et al.  Synthesis, assembly and degradation of thylakoid membrane proteins. , 2000, Biochimie.

[33]  R. Dixon,et al.  Activation tagging in Arabidopsis. , 2000, Plant physiology.

[34]  L. Eichacker,et al.  Assembly of the D1 Precursor in Monomeric Photosystem II Reaction Center Precomplexes Precedes Chlorophyll a–Triggered Accumulation of Reaction Center II in Barley Etioplasts , 1999, Plant Cell.

[35]  K. V. van Wijk,et al.  Co-translational Assembly of the D1 Protein into Photosystem II* , 1999, The Journal of Biological Chemistry.

[36]  F. Wollman,et al.  The biogenesis and assembly of photosynthetic proteins in thylakoid membranes1 , 1999, Biochimica et biophysica acta.

[37]  S. Clough,et al.  Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. , 1998, The Plant journal : for cell and molecular biology.

[38]  P. Westhoff,et al.  A nuclear‐encoded protein of prokaryotic origin is essential for the stability of photosystem II in Arabidopsis thaliana , 1998, The EMBO journal.

[39]  M. Goldschmidt-Clermont.  Coordination of nuclear and chloroplast gene expression in plant cells. , 1998, International review of cytology.

[40]  E. Aro,et al.  Proteolytic activities and proteases of plant chloroplasts , 1997 .

[41]  K. V. van Wijk,et al.  Synthesis and assembly of the D1 protein into photosystem II: processing of the C-terminus and identification of the initial assembly partners and complexes during photosystem II repair. , 1997, Biochemistry.

[42]  D. Ghanotakis,et al.  Introduction to Oxygen Evolution and the Oxygen-Evolving Complex , 1996 .

[43]  N. Mitsukawa,et al.  Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR. , 1995, The Plant journal : for cell and molecular biology.

[44]  H. Schägger,et al.  Analysis of molecular masses and oligomeric states of protein complexes by blue native electrophoresis and isolation of membrane protein complexes by two-dimensional native electrophoresis. , 1994, Analytical biochemistry.

[45]  D. Miles.  The role of high chlorophyll fluorescence photosynthesis mutants in the analysis of chloroplast thylakoid membrane assembly and function , 1994 .

[46]  J. Anderson,et al.  Turnover of the photosystem II D1 protein in higher plants under photoinhibitory and nonphotoinhibitory irradiance. , 1993, The Journal of biological chemistry.

[47]  E. Aro,et al.  Photoinhibition of Photosystem II. Inactivation, protein damage and turnover. , 1993, Biochimica et biophysica acta.

[48]  W. Vermaas,et al.  Synthesis and turnover of photosystem II reaction center polypeptides in cyanobacterial D2 mutants. , 1993, The Journal of biological chemistry.

[49]  N. Adir,et al.  Dynamics of photosystem II: mechanism of photoinhibition and recovery processes , 1992 .

[50]  N. Adir,et al.  Light-dependent D1 protein synthesis and translocation is regulated by reaction center II. Reaction center II serves as an acceptor for the D1 precursor. , 1990, The Journal of biological chemistry.

[51]  W. Vermaas,et al.  Transcript Levels and Synthesis of Photosystem II Components in Cyanobacterial Mutants with Inactivated Photosystem II Genes. , 1990, The Plant cell.

[52]  D. Drapier,et al.  Posttranslational events leading to the assembly of photosystem II protein complex: a study using photosynthesis mutants from Chlamydomonas reinhardtii , 1989, The Journal of cell biology.

[53]  A. Barkan,et al.  Proteins encoded by a complex chloroplast transcription unit are each translated from both monocistronic and polycistronic mRNAs. , 1988, The EMBO journal.

[54]  O. Nanba,et al.  Isolation of a photosystem II reaction center consisting of D-1 and D-2 polypeptides and cytochrome b-559. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[55]  G. Schmidt,et al.  Biogenesis of photosystem II complexes: transcriptional, translational, and posttranslational regulation , 1986, The Journal of cell biology.

[56]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[57]  U. K. Laemmli,et al.  Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4 , 1970, Nature.