RNA editing in plant organelles: machinery, physiological function and evolution

Abstract.In plants, RNA editing is a process for converting a specific nucleotide of RNA from C to U and less frequently from U to C in mitochondria and plastids. To specify the site of editing, the cis-element adjacent to the editing site functions as a binding site for the trans-acting factor. Genetic approaches using Arabidopsis thaliana have clarified that a member of the protein family with pentatricopeptide repeat (PPR) motifs is essential for RNA editing to generate a translational initiation codon of the chloroplast ndhD gene. The PPR motif is a highly degenerate unit of 35 amino acids and appears as tandem repeats in proteins that are involved in RNA maturation steps in mitochondria and plastids. The Arabidopsis genome encodes approximately 450 members of the PPR family, some of which possibly function as trans-acting factors binding the cis-elements of the RNA editing sites to facilitate access of an unidentified RNA editing enzyme. Based on this breakthrough in the research on plant RNA editing, I would like to discuss the possible steps of co-evolution of RNA editing events and PPR proteins.

[1]  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.

[2]  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.

[3]  P. Maliga,et al.  High-frequency plastid transformation in tobacco by selection for a chimeric aadA gene. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[4]  Maureen R. Hanson,et al.  Cross-Competition in Transgenic Chloroplasts Expressing Single Editing Sites Reveals Shared cis Elements , 2002, Molecular and Cellular Biology.

[5]  C. Chase,et al.  Mitochondrial RNA editing truncates a chimeric open reading frame associated with S male-sterility in maize , 2002, Current Genetics.

[6]  M. Goebl,et al.  The TPR snap helix: a novel protein repeat motif from mitosis to transcription. , 1991, Trends in biochemical sciences.

[7]  J. Wedekind,et al.  Messenger RNA editing in mammals: new members of the APOBEC family seeking roles in the family business. , 2003, Trends in genetics : TIG.

[8]  R. Pease,et al.  A novel form of tissue-specific RNA processing produces apolipoprotein-B48 in intestine , 1987, Cell.

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

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

[11]  Michael W. Gray,et al.  RNA editing in plant mitochondria , 1989, Nature.

[12]  I. Small,et al.  The PPR motif - a TPR-related motif prevalent in plant organellar proteins. , 2000, Trends in biochemical sciences.

[13]  A. Brennicke,et al.  Transcripts of the NADH‐dehydrogenase subunit 3 gene are differentially edited in Oenothera mitochondria. , 1990, The EMBO journal.

[14]  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.

[15]  G. Igloi,et al.  Editing of a chloroplast mRNA by creation of an initiation codon , 1991, Nature.

[16]  Junichi Obokata,et al.  A site-specific factor interacts directly with its cognate RNA editing site in chloroplast transcripts , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[17]  Wei Yu,et al.  Evidence for a Site-specific Cytidine Deamination Reaction Involved in C to U RNA Editing of Plant Mitochondria (*) , 1995, The Journal of Biological Chemistry.

[18]  K. Shinozaki,et al.  Six chloroplast genes (ndhA-F) homologous to human mitochondrial genes encoding components of the respiratory chain NADH dehydrogenase are actively expressed: Determination of the splice sites in ndhA and ndhB pre-mRNAs , 1987, Molecular and General Genetics MGG.

[19]  D. Gestaut,et al.  Arabidopsis emb175 and other ppr knockout mutants reveal essential roles for pentatricopeptide repeat (PPR) proteins in plant embryogenesis , 2005, Planta.

[20]  R. Bock,et al.  Introduction of a heterologous editing site into the tobacco plastid genome: the lack of RNA editing leads to a mutant phenotype. , 1994, The EMBO journal.

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

[22]  G M Manthey,et al.  The product of the nuclear gene PET309 is required for translation of mature mRNA and stability or production of intron‐containing RNAs derived from the mitochondrial COX1 locus of Saccharomyces cerevisiae. , 1995, The EMBO journal.

[23]  L. Cattolico,et al.  Identification of the fertility restoration locus, Rfo, in radish, as a member of the pentatricopeptide‐repeat protein family , 2003 .

[24]  J. Farré,et al.  Gene expression in isolated plant mitochondria: high fidelity of transcription, splicing and editing of a transgene product in electroporated organelles. , 2001, Nucleic acids research.

[25]  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.

[26]  F. Nargang,et al.  The Neurospora crassa cya-5 nuclear gene encodes a protein with a region of homology to the Saccharomyces cerevisiae PET309 protein and is required in a post-transcriptional step for the expression of the mitochondrially encoded COXI protein , 1997, Current Genetics.

[27]  M. Hanson,et al.  Substrate and cofactor requirements for RNA editing of chloroplast transcripts in Arabidopsis in vitro. , 2005, The Plant journal : for cell and molecular biology.

[28]  A. Brennicke,et al.  In Vitro RNA Editing in Pea Mitochondria Requires NTP or dNTP, Suggesting Involvement of an RNA Helicase* , 2003, Journal of Biological Chemistry.

[29]  Jinfa F. Zhang,et al.  The radish Rfo restorer gene of Ogura cytoplasmic male sterility encodes a protein with multiple pentatricopeptide repeats. , 2003, The Plant journal : for cell and molecular biology.

[30]  S. Kawasaki,et al.  Genetic characterization of a pentatricopeptide repeat protein gene, orf687, that restores fertility in the cytoplasmic male-sterile Kosena radish. , 2003, The Plant journal : for cell and molecular biology.

[31]  R. Benne,et al.  Major transcript of the frameshifted coxll gene from trypanosome mitochondria contains four nucleotides that are not encoded in the DNA , 1986, Cell.

[32]  F. Kempken,et al.  Mitochondrial electroporation and in organello RNA editing of chimeric atp6 transcripts , 2005, Molecular Genetics and Genomics.

[33]  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.

[34]  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.

[35]  José M. Gualberto,et al.  RNA editing in wheat mitochondria results in the conservation of protein sequences , 1989, Nature.

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

[37]  Axel Brennicke,et al.  Complex cis-elements determine an RNA editing site in pea mitochondria. , 2004, Nucleic acids research.

[38]  P. Covello,et al.  On the evolution of RNA editing. , 1993, Trends in genetics : TIG.

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

[40]  N. Sherman,et al.  Molecular Cloning of Apobec-1 Complementation Factor, a Novel RNA-Binding Protein Involved in the Editing of Apolipoprotein B mRNA , 2000, Molecular and Cellular Biology.

[41]  A. Barkan,et al.  A chloroplast-localized PPR protein required for plastid ribosome accumulation. , 2003, The Plant journal : for cell and molecular biology.

[42]  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.

[43]  I. Capesius,et al.  Plant Mitochondrial RNA Editing , 1999, Journal of Molecular Evolution.

[44]  A. Inagaki,et al.  Positional cloning of the rice Rf-1 gene, a restorer of BT-type cytoplasmic male sterility that encodes a mitochondria-targeting PPR protein , 2004, Theoretical and Applied Genetics.

[45]  M. Sugiura,et al.  Recognition of RNA Editing Sites Is Directed by Unique Proteins in Chloroplasts: Biochemical Identification of cis-Acting Elements and trans-Acting Factors Involved in RNA Editing in Tobacco and Pea Chloroplasts , 2002, Molecular and Cellular Biology.

[46]  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.

[47]  C. Burant,et al.  Molecular cloning of an apolipoprotein B messenger RNA editing protein. , 1993, Science.

[48]  Hiro Iguchi,et al.  Chloroplast RNA Editing Required for Functional Acetyl-CoA Carboxylase in Plants* , 2001, The Journal of Biological Chemistry.

[49]  Z W Gu,et al.  Apolipoprotein B-48 is the product of a messenger RNA with an organ-specific in-frame stop codon. , 1987, Science.

[50]  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.

[51]  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.

[52]  J. Meurer,et al.  PGR5 Is Involved in Cyclic Electron Flow around Photosystem I and Is Essential for Photoprotection in Arabidopsis , 2002, Cell.

[53]  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.

[54]  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.

[55]  T. Shikanai,et al.  Identification of a novel protein, CRR7, required for the stabilization of the chloroplast NAD(P)H dehydrogenase complex in Arabidopsis. , 2005, The Plant journal : for cell and molecular biology.

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

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

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

[59]  T M Klein,et al.  Chloroplast transformation in Chlamydomonas with high velocity microprojectiles. , 1988, Science.

[60]  M. Hanson,et al.  A single homogeneous form of ATP6 protein accumulates in petunia mitochondria despite the presence of differentially edited atp6 transcripts. , 1994, The Plant cell.

[61]  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.

[62]  H. Carrer,et al.  Site‐specific factor involved in the editing of the psbL mRNA in tobacco plastids. , 1995, The EMBO journal.

[63]  J. Garin,et al.  New Subunits NDH-M, -N, and -O, Encoded by Nuclear Genes, Are Essential for Plastid Ndh Complex Functioning in Higher Plantsw⃞ , 2005, The Plant Cell Online.

[64]  F. Kempken,et al.  Cell type-specific loss of atp6 RNA editing in cytoplasmic male sterile Sorghum bicolor. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[65]  T. Shikanai,et al.  Identification and characterization of Arabidopsis mutants with reduced quenching of chlorophyll fluorescence. , 1999, Plant & cell physiology.

[66]  J. Rochaix Chlamydomonas reinhardtii as the photosynthetic yeast. , 1995, Annual review of genetics.

[67]  Physiological function of a respiratory complex. NAD(P)H dehydrogenase in chloroplasts : Dissection by chloroplast reverse genetics , 2000 .

[68]  J. Grienenberger,et al.  A prokaryotic-type cytidine deaminase from Arabidopsis thaliana gene expression and functional characterization. , 1999, European journal of biochemistry.

[69]  G. Blatch,et al.  The tetratricopeptide repeat: a structural motif mediating protein-protein interactions. , 1999, BioEssays : news and reviews in molecular, cellular and developmental biology.

[70]  M. Hanson,et al.  Plant organelle gene expression: Altered by RNA editing , 1996 .

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

[72]  S. Aubourg,et al.  In Arabidopsis thaliana, 1% of the genome codes for a novel protein family unique to plants , 2000, Plant Molecular Biology.

[73]  K. Shimamoto,et al.  Processing followed by complete editing of an altered mitochondrial atp6 RNA restores fertility of cytoplasmic male sterile rice. , 1993, The EMBO journal.

[74]  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.

[75]  M. Sugiura,et al.  Both RNA editing and RNA cleavage are required for translation of tobacco chloroplast ndhD mRNA: a possible regulatory mechanism for the expression of a chloroplast operon consisting of functionally unrelated genes , 1997, The EMBO journal.

[76]  M. Hanson,et al.  Developmental co-variation of RNA editing extent of plastid editing sites exhibiting similar cis-elements. , 2003, Nucleic acids research.

[77]  Achim Schnaufer,et al.  Complex management: RNA editing in trypanosomes. , 2005, Trends in biochemical sciences.

[78]  Y. Hiei,et al.  Map-based cloning of a fertility restorer gene, Rf-1, in rice (Oryza sativa L.). , 2004, The Plant journal : for cell and molecular biology.

[79]  J. Farré,et al.  cis Recognition Elements in Plant Mitochondrion RNA Editing , 2001, Molecular and Cellular Biology.

[80]  K. Niyogi,et al.  Arabidopsis Mutants Define a Central Role for the Xanthophyll Cycle in the Regulation of Photosynthetic Energy Conversion , 1998, Plant Cell.

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

[82]  S. Suharsono,et al.  Male-sterility induction in transgenic tobacco plants with an unedited atp9 mitochondrial gene from wheat. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[83]  R. Bock,et al.  In vivo dissection of cis‐acting determinants for plastid RNA editing. , 1996, The EMBO journal.

[84]  A. P. Sane,et al.  The Nucleus-Encoded HCF107 Gene of Arabidopsis Provides a Link between Intercistronic RNA Processing and the Accumulation of Translation-Competent psbH Transcripts in Chloroplasts , 2001, The Plant Cell Online.

[85]  Maureen R. Hanson,et al.  A termination codon is created by RNA editing in the petunia mitochondrial atp9 gene transcript , 2004, Current Genetics.

[86]  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.

[87]  K. Gothandam,et al.  OsPPR1, a pentatricopeptide repeat protein of rice is essential for the chloroplast biogenesis , 2005, Plant Molecular Biology.