Patterns of partial RNA editing in mitochondrial genes of Beta vulgaris

RNA editing is a process that modifies the information in transcripts of almost all angiosperm mitochondrial protein-coding genes. In order to determine the frequency and distribution of mitochondrial RNA editing in Beta vulgaris, cDNAs were sequenced and compared to the published genome sequence. 357 C to U conversions were identified across the 31 known protein genes and pseudogenes in Beta, the fewest so far for a plant mitochondrial genome. Editing patterns in the putative gene orf518 indicate that it is most likely a functional ccmC homolog, indicating that patterns of editing can be a useful determinant of gene functionality. orf518 also contains a triplicated repeat region whose members are nearly identical yet differentially edited, most likely due to differences in the sequence context of the editing sites. In addition, we show that partial editing in Beta is common at silent editing sites but rare at nonsilent editing sites, extending previous observations to a complete plant mitochondrial genome. Finally, the degree of partial editing observed for certain genes was dependent on the choice of primers used, demonstrating that care must be taken when designing primers for use in editing studies.

[1]  M. Senda,et al.  The sugar beet mitochondrial gene for the ATPase alpha-subunit: sequence, transcription and rearrangements in cytoplasmic male-sterile plants , 1993, Current Genetics.

[2]  A. Brennicke,et al.  Distribution of RNA editing sites in Oenothera mitochondrial mRNAs and rRNAs , 1991, Current Genetics.

[3]  A. Brennicke,et al.  RNA editing. , 1999, FEMS microbiology reviews.

[4]  A. Brennicke,et al.  RNA editing of a conserved reading frame in plant mitochondria increases its similarity to two overlapping reading frames in Escherichia coli , 2004, Molecular and General Genetics MGG.

[5]  Akira Sugawara,et al.  The complete nucleotide sequence of the mitochondrial genome of sugar beet (Beta vulgaris L.) reveals a novel gene for tRNACys(GCA) , 2000, Nucleic Acids Res..

[6]  R. Mulligan,et al.  RNA editing intermediates of cox2 transcripts in maize mitochondria. , 1991, Molecular and cellular biology.

[7]  J. Palmer,et al.  Inaugural Article: Punctuated evolution of mitochondrial gene content: High and variable rates of mitochondrial gene loss and transfer to the nucleus during angiosperm evolution , 2002 .

[8]  A. Brennicke,et al.  RNA editing of a group II intron in Oenothera as a prerequisite for splicing , 1995, Molecular and General Genetics MGG.

[9]  K. Oda,et al.  Gene organization and evolution of introns of a liverwort, Marchantia polymorpha, mitochondrial genome , 1993 .

[10]  J. Palmer,et al.  Multiple losses and transfers to the nucleus of two mitochondrial succinate dehydrogenase genes during angiosperm evolution. , 2001, Genetics.

[11]  T. Kubo,et al.  A duplicated sequence in sugarbeet mitochondrial transcripts is differentially edited: analysis of orfB and its derivative orf324 mRNAs. , 1996, Biochimica et biophysica acta.

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

[13]  Y. Onodera,et al.  Heterogeneity of the atp6 Presequences in Normal and Different Sources of Male-Sterile Cytoplasms of Sugar Beet , 1999 .

[14]  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.

[15]  J. Farré,et al.  Different patterns in the recognition of editing sites in plant mitochondria. , 2004, Nucleic acids research.

[16]  Jeffrey P. Mower PREP-Mt: predictive RNA editor for plant mitochondrial genes , 2005, BMC Bioinformatics.

[17]  A. P. de Souza,et al.  Transcription of succinate dehydrogenase subunit 4 (sdh4) gene in potato: detection of extensive RNA editing and co-transcription with cytochrome oxidase subunit III (cox3) gene , 2002, Current Genetics.

[18]  T. Akihama,et al.  Creation of an initiation codon by RNA editing in the coxl transcript from tomato mitochondria , 1995, Current Genetics.

[19]  T. Kubo,et al.  The nad4L-orf25 gene cluster is conserved and expressed in sugar beet mitochondria , 2000, Theoretical and Applied Genetics.

[20]  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.

[21]  A. Brennicke,et al.  The mitochondrial gene encoding ribosomal protein S12 has been translocated to the nuclear genome in Oenothera. , 1992, Nucleic acids research.

[22]  F. Kempken,et al.  RNA editing of sorghum mitochondrial atp6 transcripts changes 15 amino acids and generates a carboxy-terminus identical to yeast , 1991, Current Genetics.

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

[24]  T. Kubo,et al.  Variable number of tandem repeat loci in the mitochondrial genomes of beets , 2000, Current Genetics.

[25]  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.

[26]  T. Kubo,et al.  The sugar beet mitochondrial nad4 gene: an intron loss and its phylogenetic implication in the Caryophyllales , 2002, Theoretical and Applied Genetics.

[27]  P. Covello,et al.  RNA editing in plant mitochondria , 1989, Nature.

[28]  M. Sugiura,et al.  The complete nucleotide sequence and multipartite organization of the tobacco mitochondrial genome: comparative analysis of mitochondrial genomes in higher plants , 2005, Molecular Genetics and Genomics.

[29]  C. Lemieux,et al.  The Mitochondrial Genome of Chara vulgaris: Insights into the Mitochondrial DNA Architecture of the Last Common Ancestor of Green Algae and Land Plants Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.013 , 2003, The Plant Cell Online.

[30]  M. Hanson,et al.  Preferential RNA editing at specific sites within transcripts of two plant mitochondrial genes does not depend on transcriptional context or nuclear genotype , 1996, Current Genetics.

[31]  J. Grienenberger,et al.  Expression of the wheat mitochondrial nad3-rps12 transcription unit: correlation between editing and mRNA maturation. , 1991, The Plant cell.

[32]  R. Emeson,et al.  Functions and mechanisms of RNA editing. , 2000, Annual review of genetics.

[33]  M. Satoh,et al.  The cytoplasmic male-sterile type and normal type mitochondrial genomes of sugar beet share the same complement of genes of known function but differ in the content of expressed ORFs , 2004, Molecular Genetics and Genomics.

[34]  W. Schuster,et al.  Loss of RNA editing of rps1 sequences in Oenothera mitochondria , 1996, Current Genetics.

[35]  L. Marechal-Drouard,et al.  Editing of plant mitochondrial transfer RNAs. , 2001, Acta biochimica Polonica.

[36]  James O. Allen,et al.  Sequence and Comparative Analysis of the Maize NB Mitochondrial Genome1[w] , 2004, Plant Physiology.

[37]  K. Pruitt,et al.  Editing of pre-mRNAs can occur before cis- and trans-splicing in Petunia mitochondria , 1991, Molecular and cellular biology.

[38]  T. Kubo,et al.  The sugar beet mitochondrial genome contains an ORF sharing sequence homology with the gene for the 30 kDa subunit of bovine mitochondrial complex I , 1993, Molecular and General Genetics MGG.

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

[40]  K. Oda,et al.  Gene organization deduced from the complete sequence of liverwort Marchantia polymorpha mitochondrial DNA. A primitive form of plant mitochondrial genome. , 1992, Journal of molecular biology.

[41]  A. Mercado,et al.  Editing status of mat-r transcripts in mitochondria from two plant species: C-to-U changes occur in putative functional RT and maturase domains , 1998, Current Genetics.

[42]  A. Brennicke,et al.  An in vitro RNA editing system from cauliflower mitochondria: editing site recognition parameters can vary in different plant species. , 2005, RNA.

[43]  W Schuster,et al.  RNA editing makes mistakes in plant mitochondria: editing loses sense in transcripts of a rps19 pseudogene and in creating stop codons in coxI and rps3 mRNAs of Oenothera. , 1991, Nucleic acids research.

[44]  P. Figueroa,et al.  Transfer of RPS14 and RPL5 from the mitochondrion to the nucleus in grasses. , 2004, Gene.

[45]  The rpl5-rps 14-cob gene arrangement in Solanum tuberosum: rps14 is a transcribed and unedited pseudogene , 1996, Plant Molecular Biology.

[46]  D. Wolstenholme,et al.  RNA editing of mat-r transcripts in maize and soybean increases similarity of the encoded protein to fungal and bryophyte group II intron maturases: evidence that mat-r encodes a functional protein. , 1994, Nucleic acids research.