Conserved domain structure of pentatricopeptide repeat proteins involved in chloroplast RNA editing

The pentatricopeptide repeat (PPR) proteins form one of the largest families in higher plants and are believed to be involved in the posttranscriptional processes of gene expression in plant organelles. It has been shown by using a genetic approach focusing on NAD(P)H dehydrogenase (NDH) activity that a PPR protein CRR4 is essential for a specific RNA editing event in chloroplasts. Here, we discovered Arabidopsis crr21 mutants that are specifically impaired in the RNA editing of the site 2 of ndhD (ndhD-2), which encodes a subunit of the NDH complex. The CRR21 gene encodes a member of the PPR protein family. The RNA editing of ndhD-2 converts the Ser-128 of NdhD to leucine. In crr21, the activity of the NDH complex is specifically impaired, suggesting that the Ser128Leu change has important consequences for the function of the NDH complex. Both CRR21 and CRR4 belong to the E+ subgroup in the PLS subfamily that is characterized by the presence of a conserved C-terminal region (the E/E+ domain). This E/E+ domain is highly conserved and exchangeable between CRR21 and CRR4, although it is not essential for the RNA binding. Our results suggest that the E/E+ domain has a common function in RNA editing rather than of recognizing specific RNA sequences.

[1]  M. Tillich,et al.  Editing of plastid RNA in Arabidopsis thaliana ecotypes. , 2005, The Plant journal : for cell and molecular biology.

[2]  P. Westhoff,et al.  RNA-binding properties of HCF152, an Arabidopsis PPR protein involved in the processing of chloroplast RNA. , 2003, European journal of biochemistry.

[3]  S. Bentolila,et al.  A pentatricopeptide repeat-containing gene restores fertility to cytoplasmic male-sterile plants , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[4]  K. Toriyama,et al.  A pentatricopeptide repeat‐containing gene that promotes the processing of aberrant atp6 RNA of cytoplasmic male‐sterile rice , 2003, FEBS letters.

[5]  M. Williams,et al.  Incomplete editing of rps12 transcripts results in the synthesis of polymorphic polypeptides in plant mitochondria. , 1996, The Plant cell.

[6]  Frédérique Bitton,et al.  Genome-Wide Analysis of Arabidopsis Pentatricopeptide Repeat Proteins Reveals Their Essential Role in Organelle Biogenesis , 2004, The Plant Cell Online.

[7]  R. Bock.  Sense from nonsense: how the genetic information of chloroplasts is altered by RNA editing. , 2000, Biochimie.

[8]  M. Sugiura,et al.  Involvement of a site‐specific trans‐acting factor and a common RNA‐binding protein in the editing of chloroplast mRNAs: development of a chloroplast in vitro RNA editing system , 2001, The EMBO journal.

[9]  G. Schuster,et al.  HCF152, an Arabidopsis RNA Binding Pentatricopeptide Repeat Protein Involved in the Processing of Chloroplast psbB-psbT-psbH-petB-petD RNAs Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010397. , 2003, The Plant Cell Online.

[10]  Koichi Yoshinaga,et al.  RNA editing in hornwort chloroplasts makes more than half the genes functional. , 2003, Nucleic acids research.

[11]  H. Koop,et al.  Mutagenesis of the genes encoding subunits A, C, H, I, J and K of the plastid NAD(P)H-plastoquinone-oxidoreductase in tobacco by polyethylene glycol-mediated plastome transformation , 1998, Molecular and General Genetics MGG.

[12]  J. Mullet.  Chloroplast Development and Gene Expression , 1988 .

[13]  P. Nixon,et al.  Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disrupted plastid ndh genes , 1998, The EMBO journal.

[14]  Y. Notsu,et al.  The complete sequence of the rice (Oryza sativa L.) mitochondrial genome: frequent DNA sequence acquisition and loss during the evolution of flowering plants , 2002, Molecular Genetics and Genomics.

[15]  B. Sabater,et al.  Post-transcriptional Control of Chloroplast Gene Expression , 2002, The Journal of Biological Chemistry.

[16]  Yasuyuki Yamada,et al.  Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around photosystem I. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[17]  A. Barkan,et al.  Molecular cloning of the maize gene crp1 reveals similarity between regulators of mitochondrial and chloroplast gene expression , 1999, The EMBO journal.

[18]  H. Kössel,et al.  RNA editing in plant mitochondria and chloroplasts , 1996, Plant Molecular Biology.

[19]  Eric Rivals,et al.  Formation of the Arabidopsis Pentatricopeptide Repeat Family1[W] , 2006, Plant Physiology.

[20]  M. Hanson,et al.  A single alteration 20 nt 5' to an editing target inhibits chloroplast RNA editing in vivo. , 2001, Nucleic acids research.

[21]  T. Shikanai,et al.  RNA editing in plant organelles: machinery, physiological function and evolution , 2006, Cellular and Molecular Life Sciences CMLS.

[22]  Kazuo Shinozaki,et al.  A resource of 5,814 dissociation transposon-tagged and sequence-indexed lines of Arabidopsis transposed from start loci on chromosome 5. , 2005, Plant & cell physiology.

[23]  T. Shikanai,et al.  A pentatricopeptide repeat protein is essential for RNA editing in chloroplasts , 2005, Nature.

[24]  M. Sugiura,et al.  Comparative Analysis of RNA Editing Sites in Higher Plant Chloroplasts , 2001, Journal of Molecular Evolution.

[25]  A. Barkan,et al.  A nuclear mutation in maize blocks the processing and translation of several chloroplast mRNAs and provides evidence for the differential translation of alternative mRNA forms. , 1994, The EMBO journal.

[26]  D. Luo,et al.  Cytoplasmic Male Sterility of Rice with Boro II Cytoplasm Is Caused by a Cytotoxic Peptide and Is Restored by Two Related PPR Motif Genes via Distinct Modes of mRNA Silencing[W] , 2006, The Plant Cell Online.

[27]  M. Sugiura,et al.  A simple in vitro RNA editing assay for chloroplast transcripts using fluorescent dideoxynucleotides: distinct types of sequence elements required for editing of ndh transcripts. , 2006, The Plant journal : for cell and molecular biology.

[28]  T. Börner,et al.  Mitochondrial and chloroplast phage-type RNA polymerases in Arabidopsis. , 1997, Science.

[29]  T. Shikanai,et al.  PPR motifs of the nucleus-encoded factor, PGR3, function in the selective and distinct steps of chloroplast gene expression in Arabidopsis. , 2004, The Plant journal : for cell and molecular biology.

[30]  Gilles Peltier,et al.  A nucleus-encoded factor, CRR2, is essential for the expression of chloroplast ndhB in Arabidopsis. , 2003, The Plant journal : for cell and molecular biology.

[31]  Tsuyoshi Endo,et al.  Cyclic electron flow around photosystem I is essential for photosynthesis , 2004, Nature.

[32]  Toshiyuki Shimizu,et al.  A Pentatricopeptide Repeat Protein Is a Site Recognition Factor in Chloroplast RNA Editing*♦ , 2006, Journal of Biological Chemistry.

[33]  Kazuo Shinozaki,et al.  A collection of 11 800 single-copy Ds transposon insertion lines in Arabidopsis. , 2004, The Plant journal : for cell and molecular biology.

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

[35]  H. Handa,et al.  The complete nucleotide sequence and RNA editing content of the mitochondrial genome of rapeseed (Brassica napus L.): comparative analysis of the mitochondrial genomes of rapeseed and Arabidopsis thaliana. , 2003, Nucleic acids research.

[36]  Mitsuyasu Hasebe,et al.  High levels of RNA editing in a vascular plant chloroplast genome: analysis of transcripts from the fern Adiantum capillus-veneris. , 2004, Gene.

[37]  A. Brennicke,et al.  RNA editing in Arabidopsis mitochondria effects 441 C to U changes in ORFs. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[38]  A. Barkan,et al.  RNA Immunoprecipitation and Microarray Analysis Show a Chloroplast Pentatricopeptide Repeat Protein to Be Associated with the 5′ Region of mRNAs Whose Translation It Activatesw⃞ , 2005, The Plant Cell Online.

[39]  P. Maliga,et al.  Lack of conservation of editing sites in mRNAs that encode subunits of the NAD(P)H dehydrogenase complex in plastids and mitochondria of Arabidopsis thaliana , 2001, Current Genetics.

[40]  P. Maliga,et al.  Sequences directing C to U editing of the plastid psbL mRNA are located within a 22 nucleotide segment spanning the editing site. , 1996, The EMBO journal.

[41]  W. Gruissem,et al.  Control of plastid gene expression during development: The limited role of transcriptional regulation , 1987, Cell.