Molecular and General Genetics MGG

, Volume 163, Issue 2, pp 131–144

The effect of zygotic bud position on the transmission of mitochondrial genes in Saccharomyces cerevisiae

  • Robert L. Strausberg
  • Philip S. Perlman
Article

Summary

Segregation of mitochondrial genomes in yeast zygotes has been investigated by partial pedigree analysis of crosses involving the markers cap, ery, oli1 and par. The results demonstrate that the segregation pattern of markers is non-random during the first zygote generation and is directly related to slow mixing of the zygote cytoplasm. We have observed that a first bud may be formed at the center or either end of the dumbbell-shaped zygote. Cytoplasmic mixing is particularly slow in those zygotes producing first end buds.

Clones derived from first end buds are usually pure (or nearly so) for a parental genotype and so detectable recombination of mitochondrial markers is reduced in these zygotes. Cells derived from a zygote after removal of a first end bud are predominantly of the other parental genotype. This observation suggests that a large fraction of the available segregating units enters each first bud and illustrates one means of obtaining complete segregation (even in multi-factor crosses) at the first generation. First center buds generally receive mitochondrial markers from both parents and the recombination frequency in such clones (and the clones derived from isolated first center buds) is significantly higher than in similar clones from zygotes with first end buds. Therefore, the distribution of first bud positions within a population of zygotes can influence the recombination frequency between mitochondrial loci. The delay in cytoplasmic mixing in combination with certain patterns of zygotic budding can distort the relationship between input of mitochondrial genomes and the output of a cross.

The phage analogy model of yeast mitochondrial genetics has been re-examined in light of these data. The assumption of rapid panmixis is not supported by the data from any of the crosses analyzed here. Since panmixis is most closely approximated in zygotes with first center buds, crosses with predominantly zygotes of that type may be the ones where the model is most applicable.

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References

  1. Aufderheide, K.J.: Cytoplasmic inheritance in Saccharomyces cerevisiae: Comparison of first zygotic budsite to mitochondrial inheritance patterns. Molec. gen. Genet. 140, 231–241 (1975)Google Scholar
  2. 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
  3. Avner, P.R., Coen, D., Dujon, B., 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
  4. Birky, C.W., Jr.: Mitochondrial genetics in fungi and ciliates. In: Genetics and biogenesis of mitochondria and chloroplasts (Birky, C.W., Jr., Perlman, P.S., Byers, T.J., eds.), pp. 182–224. Columbus: Ohio State University Press 1975aGoogle Scholar
  5. Birky, C.W., Jr.: Effects of glucose repression on the transmission and recombination of mitochondrial genes in yeast (Saccharomyces cerevisiae). Genetics 80, 695–709 (1975b)Google Scholar
  6. Birky, C.W., Jr.: Zygote heterogeneity and uniparental inheritance of mitochondrial genes in yeast. Molec. gen. Genet. 141, 41–58 (1975c)Google Scholar
  7. Birky, C.W., Jr., Demko, C.A., Perlman, P.S., Strausberg, R.L.: Uniparental inheritance of mitochondrial genes in yeast: generality of the phenomenon, dependence on input bias of mitochondrial DNA, and preliminary investigation of the mechanism. Genetics, in press (1978a)Google Scholar
  8. Birky, C.W., Jr., Skavaril, R.V.: Maintenance of genetic homogeneity in systems with multiple genomes. Genet. Res. 27, 249–266 (1976)Google Scholar
  9. Birky, C.W., Jr., Strausberg, R.L., Perlman, P.S., Forster, J.L.: Vegetative segregation of mitochondrial genes in yeast: Estimating the parameters using a random model. Molec. gen. Genet., 158, 251–261 (1978a)Google Scholar
  10. Borst, P., Kroon, A.M.: Mitochondrial DNA: Physiochemical properties, replication and genetic function. Int. Rev. Cytol. 26, 107–190 (1969)Google Scholar
  11. Callen, D.F.: Recombination and segregation of mitochondrial genes in Saccharomyces cerevisiae. Molec. gen. Genet. 134, 49–63 (1974a)Google Scholar
  12. Callen, D.F.: Segregation of mitochondrially inherited antibiotic resistance genes in zygote cell lineages of Saccharomyces cerevisiae. Molec. gen. Genet. 134, 65–76 (1974b)Google Scholar
  13. Coen, D., Deutsch, J., Netter, P., Petrochilo, E., Slonimski, P.P.: Mitochondrial genetics. I. Methodlogy and phenomenology. Symp. Soc. exp. Biol. 24, 449–496 (1970)Google Scholar
  14. Demko, C.A.: The effect of gene dosage on mitochondrial marker transmission in Saccharomyces cerevisiae. M.S. Thesis. Ohio State University: Columbus (1975)Google Scholar
  15. Dujon, B., Kruszewska, A., Slonimski, P.P., Bolotin-Fukuhara, M., Coen, D., Deutsch, J., Netter, P., Weill, L.: 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
  16. 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
  17. Forster, J.L., Kleese, R.A.: The segregation of mitochondrial genes in yeast. I. Analysis of zygote pedigrees of petite x grande crosses. Molec. gen. Genet. 132, 329–339 (1975a)Google Scholar
  18. 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 (1975b)Google Scholar
  19. Fukuhara, H.: Relative properties of mitochondrial and nuclear DNA in yeast under various conditions of growth. Europ. J. Biochem. 11, 135–139 (1969)Google Scholar
  20. Gillham, N.W.: Genetic analysis of the chloroplast and mitochondrial genomes. Ann. Rev. Genet. 8, 349–391 (1974)Google Scholar
  21. 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
  22. 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
  23. Gunge, N.: Genetic analysis of unequal transmission of the mitochondrial markers in Saccharomyces cerevisiae. Molec. gen. Genet. 139, 189–202 (1975)Google Scholar
  24. 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
  25. Hall, R.M., Nagley, P., Linnane, A.W.: Biogenesis of mitochondria XIII. Genetic analysis of the control of cellular mitochondrial DNA levels in Saccharomyces cerevisiae. Molec. gen. Genet. 146, 169–175 (1976)Google Scholar
  26. Hoffman, H.P., Avers, C.J.: Mitochondria of yeast: Ultrastructural evidence for one giant, branched organelle per cell. Science 181, 749–751 (1973)Google Scholar
  27. Kruszewska, A., Szczesnaik, Gajewski, W.: Effect of auxotrophic starvation on mitochondrial marker transmission in the cdc8 mutant of Saccharomyces cerevisiae. Molec. gen. Genet. 148, 65–77 (1976)Google Scholar
  28. Lee, E.H., Johnson, B.F.: Volume-related mitochondrial deoxyribonucleic acid synthesis in zygotes and vegetative cells of Saccharomyces cerevisiae. J. Bact. 129, 1066–1071 (1977)Google Scholar
  29. Linnane, A.W., Howell, N., Lukins, H.B.: Mitochondrial genetics. In: The biogenesis of mitochondria (Kroon, A.M., Saccone, C., eds.), pp. 193–213. New York: Academic Press 1974Google Scholar
  30. 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
  31. Lukins, H.B., Tate, W.R., Saunders, G.W., Linnane, A.W.: The biogenesis of mitochondria 26. Mitochondria recombination: The segregation of parental and recombinant mitochondrial genotypes during vegetative division of yeast. Molec. gen. Genet. 120, 17–26 (1973)Google Scholar
  32. Michaelis, P.: The investigation of plasmone segregation by the pattern-analysis. Nucleus 10, 1–14 (1967)Google Scholar
  33. Perlman, P.S., Birky, C.W., Jr.: Mitochondrial genetics in bakers' yeast: A molecular mechanism for recombinational polarity and suppressiveness. Proc. nat. Acad. Sci. (Wash.) 71, 4612–4616 (1974)Google Scholar
  34. Perlman, P.S., Birky, C.W., Jr., Demko, C.A., Strausberg, R.L.: Confirmations and exceptions to the phage analogy model: Input bias, bud position effects, zygote heterogeneity, and uniparental inheritance. In: Genetics and biogenesis of chloroplasts and mitochondria (Bucher, Th., Neupert, W., Sebald, W., Werner, S., eds.), pp. 405–414. Amsterdam: North Holland Biomedical Press 1976Google Scholar
  35. Perlman, P.S., Birky, C.W. Jr., Strausberg, R.L.: Segregation of mitochondrial markers in yeast. In: Methods in enzymology: Biomembranes (Fleischer, S., Packer, L., eds.). in press (1978)Google Scholar
  36. 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
  37. Sager, R.: Cytoplasmic genes and organelles. New York: Academic Press 1972Google Scholar
  38. Sena, E.: Mitochondrial DNA replication in yeast. Ph.D. Thesis, University of Wisconsin, Madison (1972)Google Scholar
  39. Sena, E., Welsh, J., Fogel, S.: Nuclear and mitochondrial DNA replication during zygote formation and maturation in yeast. Science 194, 433–434 (1976)Google Scholar
  40. Shannon, C., Rao, A., Douglass, S., Criddle, R.S.: Recombination in yeast mitochondrial DNA. J. supramol. Struct. 1, 145–152 (1972)Google Scholar
  41. Smith, D.G., Wilkie, D., Srivastava, K.C.: Ultrastructural changes in mitochondria of zygotes in Saccharomyces cerevisiae. Microbios 6, 231–238 (1972)Google Scholar
  42. Stevens, B.J.: Variation in number and volume of the mitochondria in yeast according to growth conditions. A study based on serial sectioning and computer graphics reconstitution. Biol. Cellulaire 28, 37–56 (1977)Google Scholar
  43. Thomas, D.Y., Wilkie, D.: Recombination of mitochondrial drug-resistance factors in Saccharomyces cerevisiae. Biochem. biophys. Res. Commun. 30, 368–372 (1968a)Google Scholar
  44. Thomas, D.Y., Wilkie, D.: Inhibition of mitochondrial synthesis in yeast by erythromycin: Cytoplasmic and nuclear factors controlling resistance. Genet. Res. 11, 33–41 (1968b)Google Scholar
  45. Waxman, M.F.: The restriction of recombination of mitochondrial DNA molecules in the zygotes of Saccharomyces cerevisiae. Molec. gen. Genet. 141, 285–290 (1975)Google Scholar
  46. 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
  47. Wilkie, D.: Genetic aspects of mitochondria. Proc. Eighth Meeting Fed. Europ. Biochem. Soc. 28, 85–94 (1972)Google Scholar
  48. Wilkie, D., Thomas, D.Y.: Mitochondrial genetic analysis by zygote cell lineages in Saccharomyces cerevisiae. Genetics 73, 368–377 (1973)Google Scholar
  49. Williamson, D.H., Fennell, D.J.: Apparent dispersive replication of yeast mitochondrial DNA as revealed by density labelling experiments. Molec. gen. Genet. 131, 193–207 (1974)Google Scholar
  50. Williamson, D.H., Moustacchi, E., Fennell, D.: A procedure for rapidly extracting and estimating the nuclear and cytoplasmic DNA components of yeast cells. Biochim. biophys. Acta (Amst.) 238, 369–374 (1971)Google Scholar
  51. 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

Copyright information

© Springer-Verlag 1978

Authors and Affiliations

  • Robert L. Strausberg
    • 1
    • 2
  • Philip S. Perlman
    • 1
    • 2
  1. 1.Developmental Biology ProgramThe Ohio State UniversityColumbusUSA
  2. 2.Department of GeneticsThe Ohio State UniversityColumbusUSA
  3. 3.Department of BiochemistryThe University of Texas Health Sciences Center at DallasDallasUSA

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