Molecular Genetics and Genomics

, Volume 276, Issue 3, pp 285–293 | Cite as

Patterns of partial RNA editing in mitochondrial genes of Beta vulgaris

Original Paper

Abstract

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.

Keywords

Beta vulgaris Plant mitochondria RNA editing Partial editing 

Notes

Acknowledgments

We wish to thank the National Agricultural Research Center for Hokkaido Region (Hokkaido, Japan) for providing the seeds used in this study. This research was supported by NIH Grant R01-GM-70612 to JDP.

Supplementary material

438_2006_139_MOESM1_ESM.pdf (32 kb)
Supplementary material

References

  1. Adams KL, Qiu Y-L, Stoutemyer M, Palmer JD (2002) Punctuated evolution of mitochondrial gene content: high and variable rates of mitochondrial gene loss and transfer to the nucleus during angiosperm evolution. Proc Natl Acad Sci USA 99:9905–9912PubMedCrossRefGoogle Scholar
  2. Adams KL, Rosenblueth M, Qiu Y-L, Palmer JD (2001) Multiple losses and transfers to the nucleus of two mitochondrial succinate dehydrogenase genes during angiosperm evolution. Genetics 158:1289–1300PubMedGoogle Scholar
  3. Begu D, Mercado A, Farre JC, Moenne A, Holuigue L, Araya A, Jordana X (1998) Editing status of mat-r transcripts in mitochondria from two plant species: C-to-U changes occur in putative functional RT and maturase domains. Curr Genet 33:420–428PubMedCrossRefGoogle Scholar
  4. Borner GV, Morl M, Wissinger B, Brennicke A, Schmelzer C (1995) RNA editing of a group II intron in Oenothera as a prerequisite for splicing. Mol Gen Genet 246:739–744PubMedCrossRefGoogle Scholar
  5. Brennicke A, Marchfelder A, Binder S (1999) RNA editing. FEMS Microbiol Rev 23:297–316PubMedCrossRefGoogle Scholar
  6. Clifton SW, Minx P, Fauron CM, Gibson M, Allen JO, Sun H, Thompson M, Barbazuk WB, Kanuganti S, Tayloe C, Meyer L, Wilson RK, Newton KJ (2004) Sequence and comparative analysis of the maize NB mitochondrial genome. Plant Physiol 136:3486–3503PubMedCrossRefGoogle Scholar
  7. Choury D, Farre JC, Jordana X, Araya A (2004) Different patterns in the recognition of editing sites in plant mitochondria. Nucleic Acids Res 32:6397–6406PubMedCrossRefGoogle Scholar
  8. Covello PS, Gray MW (1989) RNA editing in plant mitochondria. Nature 341:662–666PubMedCrossRefGoogle Scholar
  9. Estiati A, Kubo T, Mikami T (1998) The ribosomal protein S7 gene is transcribed and edited in sugar beet mitochondria. Physiol Plant 102:325–327CrossRefGoogle Scholar
  10. Fey J, Weil JH, Tomita K, Cosset A, Dietrich A, Small I, Marechal-Drouard L (2001) Editing of plant mitochondrial transfer RNAs. Acta Biochim Pol 48:383–389PubMedGoogle Scholar
  11. Giege P, Brennicke A (1999) RNA editing in Arabidopsis mitochondria effects 441 C to U changes in ORFs. Proc Natl Acad Sci USA 96:15324–15329PubMedCrossRefGoogle Scholar
  12. Gott JM, Emeson RB (2000) Functions and mechanisms of RNA editing. Annu Rev Genet 34:499–531PubMedCrossRefGoogle Scholar
  13. Grohmann L, Brennicke A, Schuster W (1992) The mitochondrial gene encoding ribosomal protein S12 has been translocated to the nuclear genome in Oenothera. Nucleic Acids Res 20:5641–5646PubMedCrossRefGoogle Scholar
  14. Gualberto JM, Bonnard G, Lamattina L, Grienenberger JM (1991) Expression of the wheat mitochondrial nad3-rps12 transcription unit: correlation between editing and mRNA maturation. Plant Cell 3:1109–1120PubMedCrossRefGoogle Scholar
  15. Gualberto JM, Lamattina L, Bonnard G, Weil JH, Grienenberger JM (1989) RNA editing in wheat mitochondria results in the conservation of protein sequences. Nature 341:660–662PubMedCrossRefGoogle Scholar
  16. Handa H (2003) 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. Nucleic Acids Res 31:5907–5916PubMedCrossRefGoogle Scholar
  17. Hiesel R, Wissinger B, Schuster W, Brennicke A (1989) RNA editing in plant mitochondria. Science 246:1632–1634PubMedCrossRefGoogle Scholar
  18. Itchoda N, Nishizawa S, Nagano H, Kubo T, Mikami T (2002) The sugar beet mitochondrial nad4 gene: an intron loss and its phylogenetic implication in the Caryophyllales. Theor Appl Genet 104:209–213PubMedCrossRefGoogle Scholar
  19. Kadowaki K, Ozawa K, Kazama S, Kubo N, Akihama T (1995) Creation of an initiation codon by RNA editing in the coxI transcript from tomato mitochondria. Curr Genet 28:415–422PubMedCrossRefGoogle Scholar
  20. Kempken F, Mullen JA, Pring DR, Tang HV (1991) RNA editing of sorghum mitochondrial atp6 transcripts changes 15 amino acids and generates a carboxy-terminus identical to yeast. Curr Genet 20:417–422PubMedCrossRefGoogle Scholar
  21. Kubo T, Mikami T (1996) A duplicated sequence in sugarbeet mitochondrial transcripts is differentially edited: analysis of orfB and its derivative orf324 mRNAs. Biochim Biophys Acta 1307:259–262PubMedGoogle Scholar
  22. Kubo T, Mikami T, Kinoshita T (1993) The sugar beet mitochondrial genome contains an ORF sharing sequence homology with the gene for the 30 kDa subunit of bovine mitochondrial complex I. Mol Gen Genet 241:479–481PubMedCrossRefGoogle Scholar
  23. Kubo T, Nishizawa S, Sugawara A, Itchoda N, Estiati A, Mikami T (2000a) The complete nucleotide sequence of the mitochondrial genome of sugar beet (Beta vulgaris L.) reveals a novel gene for tRNACys (GCA). Nucleic Acids Res 28:2571–2576CrossRefGoogle Scholar
  24. Kubo T, Yamamoto MP, Mikami T (2000b) The nad4L-orf25 gene cluster is conserved and expressed in sugar beet mitochondria. Theor Appl Genet 100:214–220CrossRefGoogle Scholar
  25. Mower JP (2005) PREP-Mt: predictive RNA editor for plant mitochondrial genes. BMC Bioinformatics 6:96PubMedCrossRefGoogle Scholar
  26. Mundel C, Schuster W (1996) Loss of RNA editing of rps1 sequences in Oenothera mitochondria. Curr Genet 30:455–460PubMedCrossRefGoogle Scholar
  27. Neuwirt J, Takenaka M, van der Merwe JA, Brennicke A (2005) An in vitro RNA editing system from cauliflower mitochondria: editing site recognition parameters can vary in different plant species. RNA 11:1563–1570PubMedCrossRefGoogle Scholar
  28. Nishizawa S, Kubo T, Mikami T (2000) Variable number of tandem repeat loci in the mitochondrial genomes of beets. Curr Genet 37:34–38PubMedCrossRefGoogle Scholar
  29. Notsu Y, Masood S, Nishikawa T, Kubo N, Akiduki G, Nakazono M, Hirai A, Kadowaki K (2002) The complete sequence of the rice (Oryza sativa L.) mitochondrial genome: frequent DNA sequence acquisition and loss during the evolution of flowering plants. Mol Genet Genomics 268:434–445PubMedCrossRefGoogle Scholar
  30. Oda K, Yamato K, Ohta E, Nakamura Y, Takemura M, Nozato N, Akashi K, Kanegae T, Ogura Y, Kohchi T, Ohyama K (1992) Gene organization deduced from the complete sequence of liverwort Marchantia polymorpha mitochondrial DNA: a primitive form of plant mitochondrial genome. J Mol Biol 223:1–7PubMedCrossRefGoogle Scholar
  31. Ohyama K, Oda K, Ohta E, Takemura M (1993) Gene organization and evolution of introns of a liverwort, Marchantia polymorpha, mitochondrial genome. In: Brennicke A, Kuck U (eds) Plant mitochondria. Verlag Chemie, Weinheim, pp 115–129Google Scholar
  32. Onodera Y, Yamamoto MP, Kubo T, Mikami T (1999) Heterogeneity of the atp6 presequences in normal and different sources of male-sterile cytoplasms of sugar beet. J Plant Physiol 155:656–660Google Scholar
  33. Quinones V, Zanlungo S, Moenne A, Gomez I, Holuigue L, Litvak S, Jordana X (1996) The rpl5-rps14-cob gene arrangement in Solanum tuberosum: rps14 is a transcribed and unedited pseudogene. Plant Mol Biol 31:937–943PubMedCrossRefGoogle Scholar
  34. Sandoval P, Leon G, Gomez I, Carmona R, Figueroa P, Holuigue L, Araya A, Jordana X (2004) Transfer of RPS14 and RPL5 from the mitochondrion to the nucleus in grasses. Gene 324:139–147PubMedCrossRefGoogle Scholar
  35. Satoh M, Kubo T, Nishizawa S, Estiati A, Itchoda N, Mikami T (2004) 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. Mol Genet Genomics 272:247–256PubMedCrossRefGoogle Scholar
  36. Schuster W, Brennicke A (1991) 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. Nucleic Acids Res 19:6923–6928PubMedCrossRefGoogle Scholar
  37. Schuster W, Ternes R, Knoop V, Hiesel R, Wissinger B, Brennicke A (1991) Distribution of RNA editing sites in Oenothera mitochondrial mRNAs and rRNAs. Curr Genet 20:397–404PubMedCrossRefGoogle Scholar
  38. Schuster W, Wissinger B, Unseld M, Brennicke A (1990) Transcripts of the NADH-dehydrogenase subunit 3 gene are differentially edited in Oenothera mitochondria. EMBO J 9:263–269PubMedGoogle Scholar
  39. Senda M, Mikami T, Kinoshita T (1993) The sugar beet mitochondrial gene for the ATPase alpha-subunit: sequence, transcription and rearrangements in cytoplasmic male-sterile plants. Curr Genet 24:164–170PubMedCrossRefGoogle Scholar
  40. Siqueira SF, Dias SM, Hardouin P, Pereira FR, Lejeune B, de Souza AP (2002) 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. Curr Genet 41:282–289PubMedCrossRefGoogle Scholar
  41. Steinhauser S, Beckert S, Capesius I, Malek O, Knoop V (1999) Plant mitochondrial RNA editing. J Mol Evol 48:303–312PubMedCrossRefGoogle Scholar
  42. Sugiyama Y, Watase Y, Nagase M, Makita N, Yagura S, Hirai A, Sugiura M (2005) The complete nucleotide sequence and multipartite organization of the tobacco mitochondrial genome: comparative analysis of mitochondrial genomes in higher plants. Mol Genet Genomics 272:603–615PubMedCrossRefGoogle Scholar
  43. Sunkel S, Brennicke A, Knoop V (1994) RNA editing of a conserved reading frame in plant mitochondria increases its similarity to two overlapping reading frames in Escherichia coli. Mol Gen Genet 242:65–72PubMedGoogle Scholar
  44. Sutton CA, Conklin PL, Pruitt KD, Hanson MR (1991) Editing of pre-mRNAs can occur before cis- and trans-splicing in Petunia mitochondria. Mol Cell Biol 11:4274–4277PubMedGoogle Scholar
  45. Thomson MC, Macfarlane JL, Beagley CT, Wolstenholme DR (1994) 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. Nucleic Acids Res 22:5745–5752PubMedCrossRefGoogle Scholar
  46. Turmel M, Otis C, Lemieux C (2003) The mitochondrial genome of Chara vulgaris: insights into the mitochondrial DNA architecture of the last common ancestor of green algae and land plants. Plant Cell 15:1888–1903PubMedCrossRefGoogle Scholar
  47. Wilson RK, Hanson MR (1996) Preferential RNA editing at specific sites within transcripts of two plant mitochondrial genes does not depend on transcriptional context or nuclear genotype. Curr Genet 30:502–508PubMedCrossRefGoogle Scholar
  48. Yang AJ, Mulligan RM (1991) RNA editing intermediates of cox2 transcripts in maize mitochondria. Mol Cell Biol 11:4278–4281PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  1. 1.Smurfit Institute of GeneticsUniversity of DublinDublin 2Ireland
  2. 2.Department of BiologyIndiana UniversityBloomingtonUSA

Personalised recommendations