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. 1981 Aug;78(8):4743–4747. doi: 10.1073/pnas.78.8.4743

A mitochondrial locus is necessary for the synthesis of mitochondrial tRNA in the yeast Saccharomyces cerevisiae.

N C Martin, K Underbrink-Lyon
PMCID: PMC320239  PMID: 6795621

Abstract

We have used a cloned yeast mitochondrial tRNAUCNSer gene as a probe to detect RNA species that are transcripts from this gene in wild-type Saccharomyces cerevisiae and in petite deletion mutants. In RNA from wild-type cells, the tRNA is the most prominent transcript of the gene. In RNA from deletion mutants that retain this gene but have lost other regions of mtDNA, high molecular weight transcripts containing the tRNAUCNSer sequences accumulate but tRNAUCNSer is not made. tRNAUCNSer synthesis can be restored in these mutants when they are mated to other deletion mutants that retain a different portion of the mitochondrial genome. Protein synthesis is not necessary for the restoration, and the restoration is not due to a nuclear effect or to an effect of mating alone, because strains without mtDNA are not able to restore tRNA synthesis. These results definitively demonstrate the existence of a yeast mitochondrial locus that is necessary for tRNA synthesis and, because the restoration of tRNAUCNSer synthesis appears to result from intergenic complementation, not recombination, indicate that this locus acts in trans.

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Selected References

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

  1. Alwine J. C., Kemp D. J., Stark G. R. Method for detection of specific RNAs in agarose gels by transfer to diazobenzyloxymethyl-paper and hybridization with DNA probes. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5350–5354. doi: 10.1073/pnas.74.12.5350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Berlani R. E., Pentella C., Macino G., Tzagoloff A. Assembly of the mitochondrial membrane system: isolation of mitochondrial transfer ribonucleic acid mutants and characterization of transfer ribonucleic acid genes of Saccharomyces cerevisiae. J Bacteriol. 1980 Mar;141(3):1086–1097. doi: 10.1128/jb.141.3.1086-1097.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bogenhagen D. F., Sakonju S., Brown D. D. A control region in the center of the 5S RNA gene directs specific initiation of transcription: II. The 3' border of the region. Cell. 1980 Jan;19(1):27–35. doi: 10.1016/0092-8674(80)90385-2. [DOI] [PubMed] [Google Scholar]
  4. Bonitz S. G., Tzagoloff A. Assembly of the mitochondrial membrane system. Sequences of yeast mitochondrial tRNA genes. J Biol Chem. 1980 Oct 10;255(19):9075–9081. [PubMed] [Google Scholar]
  5. Bos J. L., Osinga K. A., Van der Horst G., Borst P. Nucleotide sequence of the mitochondrial structural genes for cysteine-tRNA and histidine-tRNA of yeast. Nucleic Acids Res. 1979 Jul 25;6(10):3255–3266. doi: 10.1093/nar/6.10.3255. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bos J. L., Osinga K. A., Van der Horst G., Hecht N. B., Tabak H. F., Van Ommen G. J., Borst P. Splice point sequence and transcripts of the intervening sequence in the mitochondrial 21S ribosomal RNA gene of yeast. Cell. 1980 May;20(1):207–214. doi: 10.1016/0092-8674(80)90248-2. [DOI] [PubMed] [Google Scholar]
  7. Casey J. W., Hsu H. J., Rabinowitz M., Getz G. S., Fukuhara H. Transfer RNA genes in the mitochondrial DNA of cytoplasmic petite mutants of Saccharomyces cerevisiae. J Mol Biol. 1974 Oct 5;88(4):717–733. doi: 10.1016/0022-2836(74)90395-7. [DOI] [PubMed] [Google Scholar]
  8. Church G. M., Slonimski P. P., Gilbert W. Pleiotropic mutations within two yeast mitochondrial cytochrome genes block mRNA processing. Cell. 1979 Dec;18(4):1209–1215. doi: 10.1016/0092-8674(79)90233-2. [DOI] [PubMed] [Google Scholar]
  9. Faye G., Kujawa C., Dujon B., Bolotin-Fukuhara M., Wolf K., Fukuhara H., Slonimski P. P. Localization of the gene coding for the mitochondrial 16 S ribosomal RNA using rho- mutants of Saccharomyces cerevisiae. J Mol Biol. 1975 Nov 25;99(1):203–217. doi: 10.1016/s0022-2836(75)80168-9. [DOI] [PubMed] [Google Scholar]
  10. Faye G., Kujawa C., Fukuhara H. Physical and genetic organization of petite and grande yeast mitochondrial DNA. IV. In vivo transcription products of mitochondrial DNA and localization of 23 S ribosomal RNA in petite mutants of saccharomyces cerevisiae. J Mol Biol. 1974 Sep 5;88(1):185–203. doi: 10.1016/0022-2836(74)90304-0. [DOI] [PubMed] [Google Scholar]
  11. Foury F., Tzagoloff A. Assembly of the mitochondrial membrane system. Genetic complementation of mit- mutations in mitochondrial DNA of Saccharomyces cerevisiae. J Biol Chem. 1978 Jun 10;253(11):3792–3797. [PubMed] [Google Scholar]
  12. Halbreich A., Pajot P., Foucher M., Grandchamp C., Slonimski P. A pathway of cytochrome b mRNA processing in yeast mitochondria: specific splicing steps and an intron-derived circular DNA. Cell. 1980 Feb;19(2):321–329. doi: 10.1016/0092-8674(80)90506-1. [DOI] [PubMed] [Google Scholar]
  13. Kole R., Baer M. F., Stark B. C., Altman S. E. coli RNAase P has a required RNA component. Cell. 1980 Apr;19(4):881–887. doi: 10.1016/0092-8674(80)90079-3. [DOI] [PubMed] [Google Scholar]
  14. Lerner M. R., Boyle J. A., Mount S. M., Wolin S. L., Steitz J. A. Are snRNPs involved in splicing? Nature. 1980 Jan 10;283(5743):220–224. doi: 10.1038/283220a0. [DOI] [PubMed] [Google Scholar]
  15. Lewin A., Morimoto R., Rabinowitz M. Restriction enzyme analysis of mitochondrial DNAs of petite mutants of yeast: classification of petites, and deletion mapping of mitochondrial genes. Mol Gen Genet. 1978 Jul 25;163(3):257–275. doi: 10.1007/BF00271955. [DOI] [PubMed] [Google Scholar]
  16. Li M., Tzagoloff A. Assembly of the mitochondrial membrane system: sequences of yeast mitochondrial valine and an unusual threonine tRNA gene. Cell. 1979 Sep;18(1):47–53. doi: 10.1016/0092-8674(79)90352-0. [DOI] [PubMed] [Google Scholar]
  17. Locker J. Analytical and preparative electrophoresis of RNA in agarose-urea. Anal Biochem. 1979 Oct 1;98(2):358–367. doi: 10.1016/0003-2697(79)90154-4. [DOI] [PubMed] [Google Scholar]
  18. Lopez I. C., Farrelly F., Butow R. A. Trans action and the var1 determinant region on yeast mitochondrial DNA. Specific labeling of mitochondrial translation products in zygotes. J Biol Chem. 1981 Jun 25;256(12):6496–6501. [PubMed] [Google Scholar]
  19. Martin N. C., Miller D., Hartley J., Moynihan P., Donelson J. E. The tRNAAGYSer and tRNACGYArg genes from a gene cluster in yeast mitochondrial DNA. Cell. 1980 Feb;19(2):339–343. doi: 10.1016/0092-8674(80)90508-5. [DOI] [PubMed] [Google Scholar]
  20. Martin N., Rabinowitz M., Fukuhara H. Isoaccepting mitochondrial glutamyl-tRNA species transcribed from different regions of the mitochondrial genome of Saccharomyces cerevisiae. J Mol Biol. 1976 Mar 5;101(3):285–296. doi: 10.1016/0022-2836(76)90148-0. [DOI] [PubMed] [Google Scholar]
  21. Merten S., Synenki R. M., Locker J., Christianson T., Rabinowitz M. Processing of precursors of 21S ribosomal RNA from yeast mitochondria. Proc Natl Acad Sci U S A. 1980 Mar;77(3):1417–1421. doi: 10.1073/pnas.77.3.1417. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Miller D. L., Martin N. C., Pham H. D., Donelson J. E. Sequence analysis of two yeast mitochondrial DNA fragments containing the genes for tRNA Ser UCR and tRNA Phe UUY. J Biol Chem. 1979 Nov 25;254(22):11735–11740. [PubMed] [Google Scholar]
  23. Morimoto R., Locker J., Synenki R. M., Rabinowitz M. Transcription, processing, and mapping of mitochondrial RNA from grande and petite yeast. J Biol Chem. 1979 Dec 25;254(24):12461–12470. [PubMed] [Google Scholar]
  24. Newman D., Pham H. D., Underbrink-Lyon K., Martin N. C. Characterization of tRNA genes in tRNA region II of yeast mitochondrial DNA. Nucleic Acids Res. 1980 Nov 11;8(21):5007–5016. doi: 10.1093/nar/8.21.5007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Rogers D., Bussey H. Fidelity of conjugation in Saccharomyces cerevisiae. Mol Gen Genet. 1978 Jun 14;162(2):173–182. doi: 10.1007/BF00267874. [DOI] [PubMed] [Google Scholar]
  26. Rogers J., Wall R. A mechanism for RNA splicing. Proc Natl Acad Sci U S A. 1980 Apr;77(4):1877–1879. doi: 10.1073/pnas.77.4.1877. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Sakonju S., Bogenhagen D. F., Brown D. D. A control region in the center of the 5S RNA gene directs specific initiation of transcription: I. The 5' border of the region. Cell. 1980 Jan;19(1):13–25. doi: 10.1016/0092-8674(80)90384-0. [DOI] [PubMed] [Google Scholar]
  28. Stark B. C., Kole R., Bowman E. J., Altman S. Ribonuclease P: an enzyme with an essential RNA component. Proc Natl Acad Sci U S A. 1978 Aug;75(8):3717–3721. doi: 10.1073/pnas.75.8.3717. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Stellwag E. J., Dahlberg A. E. Electrophoretic transfer of DNA, RNA and protein onto diazobenzyloxymethyl (DBM) - paper. Nucleic Acids Res. 1980 Jan 25;8(2):299–317. doi: 10.1093/nar/8.2.299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Strausberg R. L., Butow R. A. Expression of petite mitochondrial DNA in vivo: zygotic gene rescue. Proc Natl Acad Sci U S A. 1977 Jul;74(7):2715–2719. doi: 10.1073/pnas.74.7.2715. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Strausberg R. L., Perlman P. S. The effect of zygotic bud position on the transmission of mitochondrial genes in Saccharomyces cerevisiae. Mol Gen Genet. 1978 Jul 11;163(2):131–144. doi: 10.1007/BF00267404. [DOI] [PubMed] [Google Scholar]
  32. Van Ommen G. J., Boer P. H., Groot G. S., De Haan M., Roosendaal E., Grivell L. A., Haid A., Schweyen R. J. Mutations affecting RNA splicing and the interaction of gene expression of the yeast mitochondrial loci cob and oxi-3. Cell. 1980 May;20(1):173–183. doi: 10.1016/0092-8674(80)90245-7. [DOI] [PubMed] [Google Scholar]
  33. Van Ommen G. J., Groot G. S., Grivell L. A. Transcription maps of mtDNAs of two strains of saccharomyces: transcription of strain-specific insertions; Complex RNA maturation and splicing. Cell. 1979 Oct;18(2):511–523. doi: 10.1016/0092-8674(79)90068-0. [DOI] [PubMed] [Google Scholar]
  34. Wesolowski M., Fukuhara H. The genetic map of transfer RNA genes of yeast mitochondria: correction and extension. Mol Gen Genet. 1979 Mar 5;170(3):261–275. doi: 10.1007/BF00267059. [DOI] [PubMed] [Google Scholar]

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