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. 1993 May;134(1):21–28. doi: 10.1093/genetics/134.1.21

Nuclear Mutations in Saccharomyces Cerevisiae That Affect the Escape of DNA from Mitochondria to the Nucleus

P E Thorsness 1, T D Fox 1
PMCID: PMC1205423  PMID: 8514129

Abstract

We have inserted a yeast nuclear DNA fragment bearing the TRP1 gene and its associated origin of DNA replication, ARS1, into the functional mitochondrial chromosome of a strain carrying a chromosomal trp1 deletion. TRP1 was not phenotypically expressed within the organelle. However, this Trp(-) strain readily gave rise to respiratory competent Trp(+) clones that contained the TRP1/ARS1 fragment, associated with portions of mitochondrial DNA (mtDNA), replicating in their nuclei. Thus the Trp(+) clones arose as a result of DNA escaping from mitochondria and migrating to the nucleus. We have isolated 21 nuclear mutants in which the rate of mtDNA escape is increased by screening for increased rates of papillation to Trp(+). All 21 mutations were recessive and fell into six complementation groups, termed YME1-YME6. In addition to increasing the rate of mtDNA escape, yme1 mutations also caused a heat-sensitive respiratory deficient phenotype at 37° and a cold-sensitive growth defect on complete glucose medium at 14°. While the other yme mutations had no detectable growth phenotypes, synergistic interactions were observed in two double mutant combinations: a yme1, yme2 double mutant failed to respire at 30° and a yme4, yme6 double mutant failed to respire at all temperatures tested. None of the respiratory defects were caused by loss of functional mtDNA. These findings suggest that yme1, yme2, yme4 and yme6 mutations alter mitochondrial functions and thereby lead to an increased rate of DNA escape from the organelle.

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Selected References

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  1. Anziano P. Q., Butow R. A. Splicing-defective mutants of the yeast mitochondrial COXI gene can be corrected by transformation with a hybrid maturase gene. Proc Natl Acad Sci U S A. 1991 Jul 1;88(13):5592–5596. doi: 10.1073/pnas.88.13.5592. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baker K. P., Schatz G. Mitochondrial proteins essential for viability mediate protein import into yeast mitochondria. Nature. 1991 Jan 17;349(6306):205–208. doi: 10.1038/349205a0. [DOI] [PubMed] [Google Scholar]
  3. Costanzo M. C., Seaver E. C., Fox T. D. At least two nuclear gene products are specifically required for translation of a single yeast mitochondrial mRNA. EMBO J. 1986 Dec 20;5(13):3637–3641. doi: 10.1002/j.1460-2075.1986.tb04693.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Costanzo M. C., Seaver E. C., Fox T. D. The PET54 gene of Saccharomyces cerevisiae: characterization of a nuclear gene encoding a mitochondrial translational activator and subcellular localization of its product. Genetics. 1989 Jun;122(2):297–305. doi: 10.1093/genetics/122.2.297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Farrelly F., Butow R. A. Rearranged mitochondrial genes in the yeast nuclear genome. Nature. 1983 Jan 27;301(5898):296–301. doi: 10.1038/301296a0. [DOI] [PubMed] [Google Scholar]
  6. Folley L. S., Fox T. D. Site-directed mutagenesis of a Saccharomyces cerevisiae mitochondrial translation initiation codon. Genetics. 1991 Nov;129(3):659–668. doi: 10.1093/genetics/129.3.659. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fox T. D., Folley L. S., Mulero J. J., McMullin T. W., Thorsness P. E., Hedin L. O., Costanzo M. C. Analysis and manipulation of yeast mitochondrial genes. Methods Enzymol. 1991;194:149–165. doi: 10.1016/0076-6879(91)94013-3. [DOI] [PubMed] [Google Scholar]
  8. Fox T. D., Sanford J. C., McMullin T. W. Plasmids can stably transform yeast mitochondria lacking endogenous mtDNA. Proc Natl Acad Sci U S A. 1988 Oct;85(19):7288–7292. doi: 10.1073/pnas.85.19.7288. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gellissen G., Bradfield J. Y., White B. N., Wyatt G. R. Mitochondrial DNA sequences in the nuclear genome of a locust. Nature. 1983 Feb 17;301(5901):631–634. doi: 10.1038/301631a0. [DOI] [PubMed] [Google Scholar]
  10. Jacobs H. T., Posakony J. W., Grula J. W., Roberts J. W., Xin J. H., Britten R. J., Davidson E. H. Mitochondrial DNA sequences in the nuclear genome of Strongylocentrotus purpuratus. J Mol Biol. 1983 Apr 25;165(4):609–632. doi: 10.1016/s0022-2836(83)80270-8. [DOI] [PubMed] [Google Scholar]
  11. Johnston S. A., Anziano P. Q., Shark K., Sanford J. C., Butow R. A. Mitochondrial transformation in yeast by bombardment with microprojectiles. Science. 1988 Jun 10;240(4858):1538–1541. doi: 10.1126/science.2836954. [DOI] [PubMed] [Google Scholar]
  12. Lawrence C. W. Classical mutagenesis techniques. Methods Enzymol. 1991;194:273–281. doi: 10.1016/0076-6879(91)94021-4. [DOI] [PubMed] [Google Scholar]
  13. Lee C. A., Beckwith J. Suppression of growth and protein secretion defects in Escherichia coli secA mutants by decreasing protein synthesis. J Bacteriol. 1986 Jun;166(3):878–883. doi: 10.1128/jb.166.3.878-883.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Louis E. J., Haber J. E. Evolutionarily recent transfer of a group I mitochondrial intron to telomere regions in Saccharomyces cerevisiae. Curr Genet. 1991 Nov;20(5):411–415. doi: 10.1007/BF00317070. [DOI] [PubMed] [Google Scholar]
  15. Nugent J. M., Palmer J. D. RNA-mediated transfer of the gene coxII from the mitochondrion to the nucleus during flowering plant evolution. Cell. 1991 Aug 9;66(3):473–481. doi: 10.1016/0092-8674(81)90011-8. [DOI] [PubMed] [Google Scholar]
  16. Szostak J. W., Blackburn E. H. Cloning yeast telomeres on linear plasmid vectors. Cell. 1982 May;29(1):245–255. doi: 10.1016/0092-8674(82)90109-x. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. van den Boogaart P., Samallo J., Agsteribbe E. Similar genes for a mitochondrial ATPase subunit in the nuclear and mitochondrial genomes of Neurospora crassa. Nature. 1982 Jul 8;298(5870):187–189. doi: 10.1038/298187a0. [DOI] [PubMed] [Google Scholar]

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