Skip to main content
SpringerLink
Log in

Vegetative segregation of mitochondria in yeast: Estimating parameters using a random model

  • Published:
Molecular and General Genetics MGG Aims and scope Submit manuscript

Summary

Yeast zygotes which are heteroplasmic for mitochondrial genes reproduce vegetatively to form clones of diploid progeny which are homoplasmic. This vegetative segregation of mitochondrial genes has been interpreted in terms of a random distribution of mitochondria or mitochondrial genomes between mother and bud at cell division. We have developed equations which permit calculation of the number of segregating units in the zygote and the number of those units which enter the bud, assuming that segregation of the units is genetically random and numerically variable or equal. Use of the equations requires data from partial pedigree analyses: we isolate zygotes, separate the first bud, then determine the frequency of mitochondrial alleles among the progeny of mother cells whose first buds were homoplasmic. Application of this method to data from five crosses suggests that most zygotes have a small number of segregating units (usually less than a dozen) and only one or two enter the first bud. Analysis of the frequency of buds which are nearly but not quite homoplasmic indicates that the segregating units may be mitochondria or portions thereof which include many mitochondrial genomes, all the genomes in a unit being genetically identical in most but not all cases. These results are compatible with, but do not prove, the hypothesis of random vegetative segregation of mitochondria.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Aufderheide, K.J.: Cytoplasmic inheritance of Saccharomyces cerevisiae: Comparison of first zygotic budsite to mitochondrial inheritance patterns. Molec. gen. Genet. 140, 231–241 (1975)

    Google Scholar 

  • Aufderheide, K.J., Johnson, R.G.: Cytoplasmic inheritance in Saccharomyces cerevisiae: Comparison of zygotic mitochondrial inheritance patterns. Molec. gen. Genet. 144, 289–299 (1976)

    Google Scholar 

  • Birky, C.W. Jr.: Mitochondrial genetics in fungi and ciliates. In: The genetics and biogenesis of mitochondria and chloroplasts (C.W. Birky, Jr., P.S. Perlman, and T.J. Byers, eds.), pp. 182–224. Columbus: The Ohio State University Press 1975a

    Google Scholar 

  • Birky, C.W., Jr.: Zygote heterogeneity and uniparental inheritance of mitochondrial genes in yeast. Molec. gen. Genet. 141, 41–58 (1975b)

    Google Scholar 

  • Birky, C.W., Jr., Demko, C.A., Perlman, P.S., Strausberg, R.L.: Uniparental inheritance of mitochondrial genes in yeast: dependence on input bias of mitochondrial DNA, and preliminary investigations of the mechanism. Genetics, in press (1977)

  • Birky, C.W., Jr., Skavaril, R.V.: Maitenance of genetic homogeneity in systems with multiple genomes. Genet. Res. 27, 249–266 (1976)

    Google Scholar 

  • Callen, D.F.: Recombination and segregation of mitochondrial genes in Saccharomyces cerevisiae. Molec. gen. Genet. 134, 49–63 (1974a)

    Google Scholar 

  • Callen, D.F.: Segregation of mitochondrially inherited antibiotic resistance genes in zygote cell lineages of Saccharomyces serevisiae. Molec. gen. Genet. 134, 65–76 (1974b)

    Google Scholar 

  • Coen, D., Deutsch, J., Netter, P., Petrochilo, E., Slonimski, P.P.: Mitochondrial genetics. I. Methodology and phenomenology. Symp. Soc. exp. Biol. 24, 449–496 (1970)

    Google Scholar 

  • Demko, C.A.: The effects of gene dosage on mitochondrial marker transmission in Saccharomyces cerevisiae. M.Sc. Thesis. The Ohio State University, Columbus (1975)

  • Dujon, B., Kruszewska, A., Slonimski, P.P., Bolotin-Fukuhara, M., Coen, D.: Mitochondrial genetics X: Effects of UV irradiation on transmission and recombination of mitochondrial genes in Saccharomyces cerevisiae. Molec. gen. Genet. 137, 29–72 (1975)

    Google Scholar 

  • Dujon, B., Slonimski, P.P.: Mechanisms and rules for transmission, recombination and segregation of mitochondrial genes in Saccharomyces cerevisiae. In: Genetics and biogenesis of chloroplasts and mitochondria (Th. Bücher, W. Neupert, W. Sebald, and S. Werner, eds.), pp. 405–414. Amsterdam: North-Holland Biomedical Press 1976

    Google Scholar 

  • Dujon, B., Slonimski, P.P., Weill, L.: Mitochondrial genetics. IX: A model for recombination and segregation of mitochondrial genomes in Saccharomyces cerevisiae. Genetics 78, 415–437 (1974)

    Google Scholar 

  • Forster, J.L., Kleese, R.A.: The segregation of mitochondrial genes in yeast. II. Analysis of zygote pedigrees of drug-resistant X drug-sensitive crosses. Molec. gen. Genet. 139, 341–355 (1975)

    Google Scholar 

  • 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)

    Google Scholar 

  • Grimes, G.W., Mahler, H.R., Perlman, P.S.: Nuclear gene dosage effects on mitochondrial mass and DNA. J. Cell Biol. 61, 565–574 (1974)

    Google Scholar 

  • Gunge, N.: Effects of elevation of strain-ploidy on transmission and recombination of mitochondrial drug resistance genes in Saccharomyces cerevisiae. Molec. gen Genet. 146, 5–16 (1976)

    Google Scholar 

  • Kirk, J.T.O., Tilney-Bassett, R.A.E.: The plastids. San Francisco: W.H. Freeman and Company 1967

    Google Scholar 

  • Linnane, A.W., Saunders, G.W., Gingold, E.B., Lukins, H.B.: The biogenesis of mitochondria. V. Cytoplasmic inheritance of erythromycin resistance in Saccharomyces cerevisiae. Proc. nat. Acad. Sci. (Wash.) 59, 903–910 (1968)

    Google Scholar 

  • Lukins, H.B., Tate, W.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 

  • Manning, J.E., Wolstenholme, D.R., Richards, O.C.: Circular molecules associated with chloroplasts of spinanch, Spinacia oleracea. J. Cell Biol. 53, 594–601 (1972)

    Google Scholar 

  • Michaelis, P.: The investigation of plasmone segregation by the pattern-analysis. Nucleus 10, 1–14 (1967)

    Google Scholar 

  • Perlman, P.S., Birky, C.W., Jr., Demko, C.A., Strausberg, R.L.: Mitochondrial gene dosage and uniparental inheritance in yeast. In: Genetics and biogenesis of chloroplasts and mitochondria (Th. Bucher, W. Neupert, W. Sebald, and S. Werner, eds.), pp. 405–414. Amsterdam: North-Holland Biomedical Press 1976

    Google Scholar 

  • Perlman, P.S., Birky, C.W., Jr., Strausberg, R.L.: Segregation of mitochondrial markers in yeast. Methods in Enzymology, in press (1977)

  • Rank, G.H., Bech-Hansen, N.T.: Somatic segregation, recombination, asymmetrical distribution and complementation tests of cytoplasmically-inherited antibiotic resistance mitochondrial markers in S. cerevisiae. Genetics 72, 1–15 (1972)

    Google Scholar 

  • Sager, R.: Cytoplasmic Genes and Organelles. New York: Academic Press 1972

    Google Scholar 

  • Sena, E., Welch, J., Fogel, S.: Nuclear and mitochondrial DNA replication during zygote formation and maturation in yeast. Science 194, 433–435 (1976)

    Google Scholar 

  • Singer, B., Sager, R., Ramanis, Z.: Chloroplast genetics of Chlamydomonas. III. Closing the circle. Genetics 83, 341–354 (1976)

    Google Scholar 

  • Strausberg, R.L.: Cellular and partial pedigree analysis of mitochondrial inheritance in Saccharomyces cerevisiae. Ph.D. Thesis, The Ohio State University (1976)

  • Strausberg, R.L., Perlman, P.S.: Cellular analysis of mitochondrial inheritance in Saccharomyces cerevisiae. Genetics 77, s62-63 (abstr.) (1974)

    Google Scholar 

  • Strausberg, R.L., Perlman, P.S.: The effect of zygotic bud position on the transmission of mitochondrial genes in Sacharomyces cerevisiae. Submitted for publication (1977)

  • Thomas, D.Y., Wilkie, D.: Inhibition of mitochondrial synthesis in yeast by erythromycin: cytoplasmic and nuclear factors controlling resistance. Genet. Res. 11, 33–41 (1968)

    Google Scholar 

  • Waxman, M.F., Eaton, N., Wilkie, D.: Effect of antibiotics on the transmission of mitochondrial factors in Saccharomyces cerevisiae. Molec. gen. Genet. 127, 277–284 (1973)

    Google Scholar 

  • Wilkie, D., Thomas, D.Y.: Mitochondrial genetic analysis by zygote cell lineages in Saccharomyces cerevisiae. Genetics 73, 368–377 (1973)

    Google Scholar 

  • Williamson, D.H.: Packaging and recombination of mitochondrial DNA in vegetatively growing yeast cells. In: Genetics, biogenesis and bioenergetics of mitochondria (W. Bandlow, ed.), pp. 117–123. Berlin: Walter D. Gryter 1976

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Genetics and Interdepartmental, Developmental Biology Program, The Ohio State University, 43210, Columbus, Ohio, USA

    C. William Birky Jr., Robert L. Strausberg & Philip S. Perlman

  2. Department of Zoology, Duke University, 27706, Durham, North Carolina, USA

    Jean L. Forster

Authors
  1. C. William Birky Jr.
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Robert L. Strausberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jean L. Forster
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Philip S. Perlman
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Communicated by F. Kaudewitz

Rights and permissions

Reprints and permissions

About this article

Cite this article

Birky, C.W., Strausberg, R.L., Forster, J.L. et al. Vegetative segregation of mitochondria in yeast: Estimating parameters using a random model. Molec. Gen. Genet. 158, 251–261 (1978). https://doi.org/10.1007/BF00267196

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00267196

Keywords

Search

Navigation