Skip to main content
PMC home page
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1996 Jul;16(7):3504–3510. doi: 10.1128/mcb.16.7.3504

A single editing event is a prerequisite for efficient processing of potato mitochondrial phenylalanine tRNA.

L Marechal-Drouard 1, A Cosset 1, C Remacle 1, D Ramamonjisoa 1, A Dietrich 1
PMCID: PMC231345  PMID: 8668166

Abstract

In bean, potato, and Oenothera plants, the C encoded at position 4 (C4) in the mitochondrial tRNA Phe GAA gene is converted into a U in the mature tRNA. This nucleotide change corrects a mismatched C4-A69 base pair which appears when the gene sequence is folded into the cloverleaf structure. C-to-U conversions constitute the most common editing events occurring in plant mitochondrial mRNAs. While most of these conversions introduce changes in the amino acids specified by the mRNA and appear to be essential for the synthesis of functional proteins in plant mitochondria, the putative role of mitochondrial tRNA editing has not yet been defined. Since the edited form of the tRNA has the correct secondary and tertiary structures compared with the nonedited form, the two main processes which might be affected by a nucleotide conversion are aminoacylation and maturation. To test these possibilities, we determined the aminoacylation properties of unedited and edited potato mitochondrial tRNAPhe in vitro transcripts, as well as the processing efficiency of in vitro-synthesized potato mitochondrial tRNAPhe precursors. Reverse transcription-PCR amplification of natural precursors followed by cDNA sequencing was also used to investigate the influence of editing on processing. Our results show that C-to-U conversion at position 4 in the potato mitochondrial tRNA Phe GAA is not required for aminoacylation with phenylalanine but is likely to he essential for efficient processing of this tRNA.

Full Text

The Full Text of this article is available as a PDF (618.2 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Beier H., Lee M. C., Sekiya T., Kuchino Y., Nishimura S. Two nucleotides next to the anticodon of cytoplasmic rat tRNA(Asp) are likely generated by RNA editing. Nucleic Acids Res. 1992 Jun 11;20(11):2679–2683. doi: 10.1093/nar/20.11.2679. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Binder S., Brennicke A. A tRNA gene transcription initiation site is similar to mRNA and rRNA promoters in plant mitochondria. Nucleic Acids Res. 1993 Nov 11;21(22):5012–5019. doi: 10.1093/nar/21.22.5012. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Binder S., Marchfelder A., Brennicke A. RNA editing of tRNA(Phe) and tRNA(Cys) in mitochondria of Oenothera berteriana is initiated in precursor molecules. Mol Gen Genet. 1994 Jul 8;244(1):67–74. doi: 10.1007/BF00280188. [DOI] [PubMed] [Google Scholar]
  4. Binder S., Marchfelder A., Brennicke A., Wissinger B. RNA editing in trans-splicing intron sequences of nad2 mRNAs in Oenothera mitochondria. J Biol Chem. 1992 Apr 15;267(11):7615–7623. [PubMed] [Google Scholar]
  5. Börner G. V., Mörl M., Wissinger B., Brennicke A., Schmelzer C. RNA editing of a group II intron in Oenothera as a prerequisite for splicing. Mol Gen Genet. 1995 Mar 20;246(6):739–744. doi: 10.1007/BF00290721. [DOI] [PubMed] [Google Scholar]
  6. Carneiro V. T., Dietrich A., Maréchal-Drouard L., Cosset A., Pelletier G., Small I. Characterization of some major identity elements in plant alanine and phenylalanine transfer RNAs. Plant Mol Biol. 1994 Dec;26(6):1843–1853. doi: 10.1007/BF00019497. [DOI] [PubMed] [Google Scholar]
  7. Cattaneo R. Different types of messenger RNA editing. Annu Rev Genet. 1991;25:71–88. doi: 10.1146/annurev.ge.25.120191.000443. [DOI] [PubMed] [Google Scholar]
  8. Conklin P. L., Wilson R. K., Hanson M. R. Multiple trans-splicing events are required to produce a mature nad1 transcript in a plant mitochondrion. Genes Dev. 1991 Aug;5(8):1407–1415. doi: 10.1101/gad.5.8.1407. [DOI] [PubMed] [Google Scholar]
  9. Del Sal G., Manfioletti G., Schneider C. The CTAB-DNA precipitation method: a common mini-scale preparation of template DNA from phagemids, phages or plasmids suitable for sequencing. Biotechniques. 1989 May;7(5):514–520. [PubMed] [Google Scholar]
  10. Hanic-Joyce P. J., Gray M. W. Processing of transfer RNA precursors in a wheat mitochondrial extract. J Biol Chem. 1990 Aug 15;265(23):13782–13791. [PubMed] [Google Scholar]
  11. Janke A., Päbo S. Editing of a tRNA anticodon in marsupial mitochondria changes its codon recognition. Nucleic Acids Res. 1993 Apr 11;21(7):1523–1525. doi: 10.1093/nar/21.7.1523. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Joyce P. B., Gray M. W. Chloroplast-like transfer RNA genes expressed in wheat mitochondria. Nucleic Acids Res. 1989 Jul 25;17(14):5461–5476. doi: 10.1093/nar/17.14.5461. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kahle D., Wehmeyer U., Krupp G. Substrate recognition by RNase P and by the catalytic M1 RNA: identification of possible contact points in pre-tRNAs. EMBO J. 1990 Jun;9(6):1929–1937. doi: 10.1002/j.1460-2075.1990.tb08320.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Knoop V., Schuster W., Wissinger B., Brennicke A. Trans splicing integrates an exon of 22 nucleotides into the nad5 mRNA in higher plant mitochondria. EMBO J. 1991 Nov;10(11):3483–3493. doi: 10.1002/j.1460-2075.1991.tb04912.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Lippok B., Brennicke A., Wissinger B. Differential RNA editing in closely related introns in Oenothera mitochondria. Mol Gen Genet. 1994 Apr;243(1):39–46. doi: 10.1007/BF00283874. [DOI] [PubMed] [Google Scholar]
  16. Lonergan K. M., Gray M. W. Editing of transfer RNAs in Acanthamoeba castellanii mitochondria. Science. 1993 Feb 5;259(5096):812–816. doi: 10.1126/science.8430334. [DOI] [PubMed] [Google Scholar]
  17. Lonergan K. M., Gray M. W. Predicted editing of additional transfer RNAs in Acanthamoeba castellanii mitochondria. Nucleic Acids Res. 1993 Sep 11;21(18):4402–4402. doi: 10.1093/nar/21.18.4402. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Marchfelder A., Brennicke A., Binder S. RNA editing is required for efficient excision of tRNA(Phe) from precursors in plant mitochondria. J Biol Chem. 1996 Jan 26;271(4):1898–1903. doi: 10.1074/jbc.271.4.1898. [DOI] [PubMed] [Google Scholar]
  19. Marchfelder A., Brennicke A. Characterization and partial purification of tRNA processing activities from potato mitochondria. Plant Physiol. 1994 Aug;105(4):1247–1254. doi: 10.1104/pp.105.4.1247. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Marechal-Drouard L., Small I., Weil J. H., Dietrich A. Transfer RNA import into plant mitochondria. Methods Enzymol. 1995;260:310–327. doi: 10.1016/0076-6879(95)60148-1. [DOI] [PubMed] [Google Scholar]
  21. Maréchal-Drouard L., Guillemaut P., Cosset A., Arbogast M., Weber F., Weil J. H., Dietrich A. Transfer RNAs of potato (Solanum tuberosum) mitochondria have different genetic origins. Nucleic Acids Res. 1990 Jul 11;18(13):3689–3696. doi: 10.1093/nar/18.13.3689. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Maréchal-Drouard L., Ramamonjisoa D., Cosset A., Weil J. H., Dietrich A. Editing corrects mispairing in the acceptor stem of bean and potato mitochondrial phenylalanine transfer RNAs. Nucleic Acids Res. 1993 Oct 25;21(21):4909–4914. doi: 10.1093/nar/21.21.4909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Mörl M., Dörner M., Päbo S. C to U editing and modifications during the maturation of the mitochondrial tRNA(Asp) in marsupials. Nucleic Acids Res. 1995 Sep 11;23(17):3380–3384. doi: 10.1093/nar/23.17.3380. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Neuburger M., Journet E. P., Bligny R., Carde J. P., Douce R. Purification of plant mitochondria by isopycnic centrifugation in density gradients of Percoll. Arch Biochem Biophys. 1982 Aug;217(1):312–323. doi: 10.1016/0003-9861(82)90507-0. [DOI] [PubMed] [Google Scholar]
  25. Perret V., Garcia A., Grosjean H., Ebel J. P., Florentz C., Giegé R. Relaxation of a transfer RNA specificity by removal of modified nucleotides. Nature. 1990 Apr 19;344(6268):787–789. doi: 10.1038/344787a0. [DOI] [PubMed] [Google Scholar]
  26. Remacle C., Maréchal-Drouard L. Characterization of the potato mitochondrial transcription unit containing 'native' trnS (GCU), trnF (GAA) and trnP (UGG). Plant Mol Biol. 1996 Feb;30(3):553–563. doi: 10.1007/BF00049331. [DOI] [PubMed] [Google Scholar]
  27. Schuster W., Ternes R., Knoop V., Hiesel R., Wissinger B., Brennicke A. Distribution of RNA editing sites in Oenothera mitochondrial mRNAs and rRNAs. Curr Genet. 1991 Nov;20(5):397–404. doi: 10.1007/BF00317068. [DOI] [PubMed] [Google Scholar]
  28. Steinberg S., Misch A., Sprinzl M. Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Res. 1993 Jul 1;21(13):3011–3015. doi: 10.1093/nar/21.13.3011. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Thurlow D. L., Shilowski D., Marsh T. L. Nucleotides in precursor tRNAs that are required intact for catalysis by RNase P RNAs. Nucleic Acids Res. 1991 Feb 25;19(4):885–891. doi: 10.1093/nar/19.4.885. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Wintz H., Grienenberger J. M., Weil J. H., Lonsdale D. M. Location and nucleotide sequence of two tRNA genes and a tRNA pseudo-gene in the maize mitochondrial genome: evidence for the transcription of a chloroplast gene in mitochondria. Curr Genet. 1988 Mar;13(3):247–254. doi: 10.1007/BF00387771. [DOI] [PubMed] [Google Scholar]
  31. Wissinger B., Schuster W., Brennicke A. Trans splicing in Oenothera mitochondria: nad1 mRNAs are edited in exon and trans-splicing group II intron sequences. Cell. 1991 May 3;65(3):473–482. doi: 10.1016/0092-8674(91)90465-b. [DOI] [PubMed] [Google Scholar]
  32. Yokobori S. I., Päbo S. tRNA editing in metazoans. Nature. 1995 Oct 12;377(6549):490–490. doi: 10.1038/377490a0. [DOI] [PubMed] [Google Scholar]
  33. Yokobori S., Päbo S. Transfer RNA editing in land snail mitochondria. Proc Natl Acad Sci U S A. 1995 Oct 24;92(22):10432–10435. doi: 10.1073/pnas.92.22.10432. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Zanlungo S., Quiñones V., Moenne A., Holuigue L., Jordana X. Splicing and editing of rps10 transcripts in potato mitochondria. Curr Genet. 1995 May;27(6):565–571. doi: 10.1007/BF00314449. [DOI] [PubMed] [Google Scholar]

Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis

RESOURCES