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Effect of carbon source on the replication and transmission of yeast mitochondrial genomes

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Summary

Genetic crosses were made using strains of Saccharomyces cerevisiae which carried cytoplasmically inherited markers conferring resistance to erythromycin, oligomycin and chloramphenicol. The frequency of transmission of these mitochondrial loci to diploid progeny was found to be influenced by the physiological state of the haploid parents, and was not affected by the cis or trans configuration of the three resistance markers. No recombinational polarity was seen in any of the crosses.

Growth of a haploid parental strain to stationary phase in a yeast extract peptone medium containing glycerol as a carbon source resulted in a high level of transmission of mitochondrial markers when crossed with a strain grown to stationary phase in the same medium but with glucose as carbon source.

When cells were grown under the same conditions as those used in the genetic crosses they were found to contain more mitochondrial DNA relative to nuclear DNA when glycerol was used as a carbon source than when glucose was used. Two criteria were used to determine the amount of mitochondrial DNA present: i) incorporation of radioactive precursors into the different DNA species; and ii) measurement of the mass of DNA from amounts of ultraviolet-absorbing material at the appropriate buoyant densities in isopycnic CsCl gradients.

It is proposed that the two to three fold difference in the ratio of mitochondrial DNA to nuclear DNA in stationary phase cells grown in the presence of glycerol compared to glucose reflects an increased number of mitochondrial genomes in derepressed mitochondria. This difference, by a “genome dosage” effect, could account for the variations in the genetic parameter of the frequency of transmission, i.e., strains grown with glycerol as a carbon source contain more mitochondrial genomes than glucose-grown strains and thus will contribute more mitochondrial markers to the zygote.

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References

  • Avner, P. R., Coen, D., Slonimski, P. P.: Mitochondrial genetics. IV. Allelism and mapping studies of oligomycin resistant mutants in S. cerevisiae. Molec. gen. Genet. 125, 9–52 (1973)

    Google Scholar 

  • Bleeg, H. S., Leth Bak, A., Christiansen, C., Smith, K. E., Stenderup, A.: Mitochondrial DNA and glucose repression in yeast. Biochem. biophys. Res. Commun. 47, 524–530 (1972)

    Google Scholar 

  • Bolotin, M., Coen, D., Deutsch, J., Dujon, B., Netter, P., Petrochilo, E., Slonimski, P. P.: La Recombinaison des mitochondries chez Saccharomyces cerevisiae. Bull. Inst. Past. 69, 215–239 (1971)

    Google Scholar 

  • Coen, D., Deutsch, J., Netter, P., Petrochilo, E., Slonimski, P. P.: Mitochondrial genetics: I. Methodology and phenomenology. In: P. L. Miller, Control of Organelle Development: 24th Symp. Soc. Exptl. Biol. London, p. 449–496, Cambridge: University Press 1970

    Google Scholar 

  • Cottrell, S. F., Avers, C. J.: Evidence of mitochondrial synchrony in synchronous cell cultures of yeast. Biochem. biophys. Res. Commun. 38, 973–980 (1970)

    Google Scholar 

  • Cryer, D. R., Goldthwaite, C. D., Zinker, S., Lam, K., Storm, E., Hirschberg, R., Blamire, J., Finkelstein, D. B., Marmur, J.: Studies on nuclear and mitochondrial DNA of Saccharomyces cerevisiae. Cold Spr. Harb. Symp. quant. Biol. 38, (1973) (in press)

  • Fukuhara, H.: Relative proportions of mitochondrial and nuclear DNA in yeast under various conditions of growth. Europ. J. Biochem. 11, 135–139 (1969)

    Google Scholar 

  • Goldthwaite, C., Cryer, D. R., Marmur, J.: Correlation between mitochondrial physiological state and a cytoplasmic genetic system in yeast. Fed. Proc. 32, 641 abs (1973)

    Google Scholar 

  • Hartwell, L. H.: Biochemical genetics of yeast. Ann. Rev. Genetics 4, 373–396 (1970)

    Google Scholar 

  • Hoffman, H. P., Avers, C. J.: Mitochondrion of yeast: ultrastructural evidence for one giant, branched organelle per cell. Science 181, 749–751 (1973)

    Google Scholar 

  • Hollenberg, C. P., Borst, P., VanBruggen, E. F. J.: Mitochondrial DNA V. A25-μ closed circular duplex DNA molecule in wild-type yeast mitochondria. Structure and genetic complexity. Biochim. biophys. Acta (Amst.) 209, 1–15 (1970)

    Google Scholar 

  • Howell, N., Trembath, M. K., Linnane, A. W., Lukins, H. B.: Biogenesis of mitochondria. 30. An analysis of polarity of mitochondrial gene recombination and transmission. Molec. gen. Genet. 122, 37–51 (1973)

    Google Scholar 

  • Jakob, H.: Technique de synchronisation de la formation des zygotes chez la levure Saccharomyces cerevisiae. C. R. Acad. Sci. (Paris) 254, 3909–3911 (1962)

    Google Scholar 

  • Kaneko, T., Kitamura, K., Yamamoto, Y.: Susceptibilities of yeasts to yeast cell wall lytic enzymes of Arthrobacter luteus. Agr. Biol. Chem. 37, 2295–2302 (1973)

    Google Scholar 

  • Lukins, H. B., Tate, J. R., Saunders, G. W., Linnane, A. W.: The biogenesis of mitochondria. 26. Mitochondrial recombination: the segregation of parental and recombinant mitochondrial genotypes during vegetative division of yeast. Molec. gen. Genet. 120, 17–25 (1973)

    Google Scholar 

  • Mahler, H. R.: Biogenetic autonomy of mitochondria. CRC Critical Reviews in Biochemistry, G. D. Fasman, ed. p. 381–460. vol. 1, Cleveland, Ohio: The Chemical Rubber Co. 1973

    Google Scholar 

  • Meselson, M., Stahl, F. W., Vinograd, J.: Equilibrium sedimentation of macromolecules in density gradients. Proc. nat. Acad. Sci. (Wash.) 43, 581–588 (1957)

    Google Scholar 

  • Mian, F. A., Kuenzi, M. T., Halvorson, H. O.: Studies on mitochondrial membrane proteins in Saccharomyces cerevisiae under different degrees of glucose repression. J. Bacteriol. 115, 876–881 (1973)

    Google Scholar 

  • Moustacchi, E., Williamson, D. H.: Physiological variations in satellite components of yeast DNA detected by density gradient centrifugation. Biochem. biophys. Res. Commun. 23, 56–61 (1966)

    Google Scholar 

  • Nagley, P., Linnane, A. W.: Cellular regulation of mitochondrial DNA synthesis in Saccharomyces cerevisiae. Cell Differentiation 1, 143–148 (1972)

    Google Scholar 

  • Ogur, M., Minckler, S., McLary, D. O.: Desoxyribonucleic acid and the budding cycle in the yeast. J. Bacteriol. 66, 642–645 (1953)

    Google Scholar 

  • Rank, G. H.: Recombination in 3-factor crosses of cytoplasmically inherited antibioticresistance mitochondrial markers in S. cerevisiae. Heredity 30, 265–271 (1973)

    Google Scholar 

  • Saunders, G. W., Gingold, E. B., Trembath, M. K., Lukins, H. B., Linnane, A. W.: Mitochondrial genetics in yeast: segregation of a cytoplasmic determinant in crosses and its loss or retention in the petite. In: Autonomy and biogenesis of mitochondria and chloroplasts, N. K. Boardman, A. W. Linnane and R. M. Smillie. eds., p. 185–193, Amsterdam: North Holland Press 1970

    Google Scholar 

  • Sherman, F., Lawrence, C. W.: Genetics of the yeast Saccharomyces. Handbook of Genetics, vol. 1, ed. Robert C. King, p. 359–393. Van Nostrand Reinhold Co.

  • Slonimski, P. P., Perrodin, G., Croft, J. H.: Ethidium bromide induced mutation of yeast mitochondria: complete transformation of cells into respiratory deficient non-chromosomal “petites”. Bioch. biophys. Res. Commun. 30, 232–239 (1968)

    Google Scholar 

  • Smith, D., Tauro, P., Schweizer, E. Halvorson, H. O.: The replication of mitochondrial DNA during the cell cycle in Saccharomyces lactis. Proc. nat. Acad. Sci. (Wash.) 60, 936–942 (1968)

    Google Scholar 

  • Smith, D. G., Wilkie, D., Srivastava, K. C.: Ultrastructural changes in mitochondria of zygotes in Saccharomyces cerevisiae. Microbios 6, 231–238 (1972)

    Google Scholar 

  • Suda, K., Uchida, A.: Segregation and recombination of cytoplasmic drug-resistance factors in Saccharomyces cerevisiae. Jap. J. Genet. 47, 441–444 (1972)

    Google Scholar 

  • Thomas, D. Y., Wilkie, D.: Recombination of mitochondrial drug-resistance factors in Saccharomyces cerevisiae. Biochem. biophys. Res. Commun. 30, 368–372 (1968)

    Google Scholar 

  • Wilkie, D., Thomas, D. Y.: Mitochondrial genetic analysis by zygote cell lineages in Saccharomyces cerevisiae. Genetics 73, 367–377 (1973)

    Google Scholar 

  • Williamson, D. H.: The effect of environmental and genetic factors on the replication of mitochondrial DNA in yeast. In: P. L. Miller, Control of Organelle Development: 24th Symp. Soc. Exptl. Biol. London, p. 247–276, Cambridge: University Press 1970

    Google Scholar 

  • Williamson, D. H., Scopes, A. W.: The behavior of nucleic acids in synchronously dividing cultures of Saccharomyces cerevisiae. Exp. Cell Res. 20, 338–349 (1960)

    Google Scholar 

  • Wolf, K.,Dujon, B., Slonimski, P. P.: Mitochondrial genetics V. Multifactorial mitochondrial crosses involving a mutation conferring paromomycin-resistance in Saccharomyces cerevisiae. Molec. gen. Genet. 125, 53–90 (1973)

    Google Scholar 

  • Yeast Genetics Supplement, Microbial Genetics Bulletin, No.31, November 1969. Oak Ridge, Tenn.: Biology Division Oak Ridge National Laboratory 1969

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Authors and Affiliations

  1. Department of Biochemistry, Albert Einstein College of Medicine, Bronx, N. Y.

    Claire D. Goldthwaite, Dennis R. Cryer & Julius Marmur

  2. Department of Biochemistry, Albert Einstein College of Medicine, Bronx, N. Y.

    Claire D. Goldthwaite, Dennis R. Cryer & Julius Marmur

  3. Department of Genetics, Albert Einstein College of Medicine, Bronx, N. Y.

    Claire D. Goldthwaite, Dennis R. Cryer & Julius Marmur

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  1. Claire D. Goldthwaite
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  2. Dennis R. Cryer
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  3. Julius Marmur
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Communicated by F. Kaudewitz

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Goldthwaite, C.D., Cryer, D.R. & Marmur, J. Effect of carbon source on the replication and transmission of yeast mitochondrial genomes. Molec. Gen. Genet. 133, 87–104 (1974). https://doi.org/10.1007/BF00264830

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  • DOI: https://doi.org/10.1007/BF00264830

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