Skip to main content
Genetics logoLink to Genetics
. 1994 Nov;138(3):565–575. doi: 10.1093/genetics/138.3.565

Suppressor Analyses of Temperature-Sensitive Cbp1 Strains of Saccharomyces Cerevisiae: The Product of the Nuclear Gene Soc1 Affects Mitochondrial Cytochrome B mRNA Post-Transcriptionally

R R Staples 1, C L Dieckmann 1
PMCID: PMC1206208  PMID: 7851755

Abstract

The induction of mitochondrial function is dependent upon both nuclearly encoded and mitochondrially encoded gene products. To understand nuclear-mitochondrial interactions, we must first understand gene-specific interactions. The accumulation of mitochondrial cytochrome b (COB) RNA is dependent upon Cbp1p, encoded by the nuclear gene CBP1. Thus, respiration is dependent upon Cbp1p. In this study, suppressors of temperature-sensitive cbp1 (cbp1(ts)) strains were selected for restoration of respiratory capability at the restrictive temperature (Ts(+)). One nuclearly encoded suppressor, extragenic to CBP1, is recessive with respect to the wild-type suppressor allele and is unlinked to other known genetic loci whose gene products are necessary for expression of COB mRNA. The suppressor, called soc1 for Suppressor of cbp1, suppresses several other cbp1(ts) alleles but does not operate via a bypass mechanism. Molecular analyses indicate that soc1 allows the steady-state level of COB mRNA to increase at high temperature but has little or no effect on the levels of COB pre-mRNA. These data have led us to propose that the product of the nuclear gene SOC1 is required for normal turnover of COB mRNA.

Full Text

The Full Text of this article is available as a PDF (3.7 MB).

Selected References

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

  1. Ackerman S. H., Gatti D. L., Gellefors P., Douglas M. G., Tzagoloff A. ATP13, a nuclear gene of Saccharomyces cerevisiae essential for the expression of subunit 9 of the mitochondrial ATPase. FEBS Lett. 1991 Jan 28;278(2):234–238. doi: 10.1016/0014-5793(91)80124-l. [DOI] [PubMed] [Google Scholar]
  2. Adams A. E., Botstein D. Dominant suppressors of yeast actin mutations that are reciprocally suppressed. Genetics. 1989 Apr;121(4):675–683. doi: 10.1093/genetics/121.4.675. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bonitz S. G., Coruzzi G., Thalenfeld B. E., Tzagoloff A., Macino G. Assembly of the mitochondrial membrane system. Physical map of the Oxi3 locus of yeast mitochondrial DNA. J Biol Chem. 1980 Dec 25;255(24):11922–11926. [PubMed] [Google Scholar]
  4. Bonitz S. G., Homison G., Thalenfeld B. E., Tzagoloff A., Nobrega F. G. Assembly of the mitochondrial membrane system. Processing of the apocytochrome b precursor RNAs in Saccharomyces cerevisiae D273-10B. J Biol Chem. 1982 Jun 10;257(11):6268–6274. [PubMed] [Google Scholar]
  5. Christianson T., Edwards J. C., Mueller D. M., Rabinowitz M. Identification of a single transcriptional initiation site for the glutamic tRNA and COB genes in yeast mitochondria. Proc Natl Acad Sci U S A. 1983 Sep;80(18):5564–5568. doi: 10.1073/pnas.80.18.5564. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Coruzzi G., Bonitz S. G., Thalenfeld B. E., Tzagoloff A. Assembly of the mitochondrial membrane system. Analysis of the nucleotide sequence and transcripts in the oxi1 region of yeast mitochondrial DNA. J Biol Chem. 1981 Dec 25;256(24):12780–12787. [PubMed] [Google Scholar]
  7. Dieckmann C. L., Homison G., Tzagoloff A. Assembly of the mitochondrial membrane system. Nucleotide sequence of a yeast nuclear gene (CBP1) involved in 5' end processing of cytochrome b pre-mRNA. J Biol Chem. 1984 Apr 25;259(8):4732–4738. [PubMed] [Google Scholar]
  8. Dieckmann C. L., Koerner T. J., Tzagoloff A. Assembly of the mitochondrial membrane system. CBP1, a yeast nuclear gene involved in 5' end processing of cytochrome b pre-mRNA. J Biol Chem. 1984 Apr 25;259(8):4722–4731. [PubMed] [Google Scholar]
  9. Dieckmann C. L., Mittelmeier T. M. Nuclearly-encoded CBP1 interacts with the 5' end of mitochondrial cytochrome b pre-mRNA. Curr Genet. 1987;12(6):391–397. doi: 10.1007/BF00434815. [DOI] [PubMed] [Google Scholar]
  10. Dieckmann C. L., Tzagoloff A. Assembly of the mitochondrial membrane system. CBP6, a yeast nuclear gene necessary for synthesis of cytochrome b. J Biol Chem. 1985 Feb 10;260(3):1513–1520. [PubMed] [Google Scholar]
  11. Finnegan P. M., Payne M. J., Keramidaris E., Lukins H. B. Characterization of a yeast nuclear gene, AEP2, required for accumulation of mitochondrial mRNA encoding subunit 9 of the ATP synthase. Curr Genet. 1991 Jul;20(1-2):53–61. doi: 10.1007/BF00312765. [DOI] [PubMed] [Google Scholar]
  12. Foury F. Cloning and sequencing of the nuclear gene MIP1 encoding the catalytic subunit of the yeast mitochondrial DNA polymerase. J Biol Chem. 1989 Dec 5;264(34):20552–20560. [PubMed] [Google Scholar]
  13. Gietz R. D., Schiestl R. H. Applications of high efficiency lithium acetate transformation of intact yeast cells using single-stranded nucleic acids as carrier. Yeast. 1991 Apr;7(3):253–263. doi: 10.1002/yea.320070307. [DOI] [PubMed] [Google Scholar]
  14. Liu Y. X., Dieckmann C. L. Overproduction of yeast viruslike particles by strains deficient in a mitochondrial nuclease. Mol Cell Biol. 1989 Aug;9(8):3323–3331. doi: 10.1128/mcb.9.8.3323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Mayer S. A., Dieckmann C. L. The yeast CBP1 gene produces two differentially regulated transcripts by alternative 3'-end formation. Mol Cell Biol. 1989 Oct;9(10):4161–4169. doi: 10.1128/mcb.9.10.4161. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Min J., Zassenhaus H. P. Identification of a protein complex that binds to a dodecamer sequence found at the 3' ends of yeast mitochondrial mRNAs. Mol Cell Biol. 1993 Jul;13(7):4167–4173. doi: 10.1128/mcb.13.7.4167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Mittelmeier T. M., Dieckmann C. L. CBP1 function is required for stability of a hybrid cob-oli1 transcript in yeast mitochondria. Curr Genet. 1990 Dec;18(5):421–428. doi: 10.1007/BF00309911. [DOI] [PubMed] [Google Scholar]
  18. Mittelmeier T. M., Dieckmann C. L. In vivo analysis of sequences necessary for CBP1-dependent accumulation of cytochrome b transcripts in yeast mitochondria. Mol Cell Biol. 1993 Jul;13(7):4203–4213. doi: 10.1128/mcb.13.7.4203. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Mueller D. M., Getz G. S. Transcriptional regulation of the mitochondrial genome of yeast Saccharomyces cerevisiae. J Biol Chem. 1986 Sep 5;261(25):11756–11764. [PubMed] [Google Scholar]
  20. Muroff I., Tzagoloff A. CBP7 codes for a co-factor required in conjunction with a mitochondrial maturase for splicing of its cognate intervening sequence. EMBO J. 1990 Sep;9(9):2765–2773. doi: 10.1002/j.1460-2075.1990.tb07464.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Myers A. M., Pape L. K., Tzagoloff A. Mitochondrial protein synthesis is required for maintenance of intact mitochondrial genomes in Saccharomyces cerevisiae. EMBO J. 1985 Aug;4(8):2087–2092. doi: 10.1002/j.1460-2075.1985.tb03896.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Rödel G., Fox T. D. The yeast nuclear gene CBS1 is required for translation of mitochondrial mRNAs bearing the cob 5' untranslated leader. Mol Gen Genet. 1987 Jan;206(1):45–50. doi: 10.1007/BF00326534. [DOI] [PubMed] [Google Scholar]
  23. Rödel G. Two yeast nuclear genes, CBS1 and CBS2, are required for translation of mitochondrial transcripts bearing the 5'-untranslated COB leader. Curr Genet. 1986;11(1):41–45. doi: 10.1007/BF00389424. [DOI] [PubMed] [Google Scholar]
  24. Staples R. R., Dieckmann C. L. Generation of temperature-sensitive cbp1 strains of Saccharomyces cerevisiae by PCR mutagenesis and in vivo recombination: characteristics of the mutant strains imply that CBP1 is involved in stabilization and processing of cytochrome b pre-mRNA. Genetics. 1993 Dec;135(4):981–991. doi: 10.1093/genetics/135.4.981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Stepien P. P., Margossian S. P., Landsman D., Butow R. A. The yeast nuclear gene suv3 affecting mitochondrial post-transcriptional processes encodes a putative ATP-dependent RNA helicase. Proc Natl Acad Sci U S A. 1992 Aug 1;89(15):6813–6817. doi: 10.1073/pnas.89.15.6813. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Tzagoloff A., Dieckmann C. L. PET genes of Saccharomyces cerevisiae. Microbiol Rev. 1990 Sep;54(3):211–225. doi: 10.1128/mr.54.3.211-225.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Vincent R. D., Hofmann T. J., Zassenhaus H. P. Sequence and expression of NUC1, the gene encoding the mitochondrial nuclease in Saccharomyces cerevisiae. Nucleic Acids Res. 1988 Apr 25;16(8):3297–3312. doi: 10.1093/nar/16.8.3297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Wettstein-Edwards J., Ticho B. S., Martin N. C., Najarian D., Getz G. S. In vitro transcription and promoter strength analysis of five mitochondrial tRNA promoters in yeast. J Biol Chem. 1986 Feb 25;261(6):2905–2911. [PubMed] [Google Scholar]
  29. Zassenhaus H. P., Hofmann T. J., Uthayashanker R., Vincent R. D., Zona M. Construction of a yeast mutant lacking the mitochondrial nuclease. Nucleic Acids Res. 1988 Apr 25;16(8):3283–3296. doi: 10.1093/nar/16.8.3283. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Ziaja K., Michaelis G., Lisowsky T. Nuclear control of the messenger RNA expression for mitochondrial ATPase subunit 9 in a new yeast mutant. J Mol Biol. 1993 Feb 20;229(4):909–916. doi: 10.1006/jmbi.1993.1095. [DOI] [PubMed] [Google Scholar]
  31. de Zamaroczy M., Bernardi G. The primary structure of the mitochondrial genome of Saccharomyces cerevisiae--a review. Gene. 1986;47(2-3):155–177. doi: 10.1016/0378-1119(86)90060-0. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES