Skip to main content
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1980 Sep;77(9):5380–5384. doi: 10.1073/pnas.77.9.5380

Preferential inclusion of extrachromosomal genetic elements in yeast meiotic spores.

B J Brewer, W L Fangman
PMCID: PMC350062  PMID: 7001477

Abstract

During meiosis and sporulation in the yeast Saccharomyces cerevisiae, extrachromosomal traits are efficiently transmitted to haploid spores. Although the pattern of inheritance of chromosomal traits reflects the mechanism of regular chromosomal segregation in meiosis, it is not known what processes are reflected by the efficient inheritance of extrachromosomal traits. Because extrachromosomal genetic elements in yeast are present in multiple copies, perpetuation of an extrachromosomal trait could occur by the passive envelopment of a subset of copies or by an active sequestering of all or a subset of copies within the four spores. We show that only subsets of the four extrachromosomal nucleic acids commonly found in yeast are transmitted through meiosis--55% of mitochondrial DNA copies, 82% of the 2-micron DNA plasmids, and about 70% of the L and M double-stranded RNAs. However, electron micrographs of serial sections through yeast asci indicate that the four spore enclose only 30% of the total ascus material. Thus these extrachromosomal elements are preferentially included within the spores, indicating that their inheritance is not a random process. Transmission of mitochondrial DNA can be accounted for by the observed enclosure of 52% of the mitochondrial volume within the spores. The high transmission frequencies of the double-stranded RNAs (which exist as virus-like particles in the cytoplasm) and 2-micron DNA must indicate that either these nucleic acids are actively recruited from the cytoplasm by some mechanism or they are associated in some way with the nucleus during meiosis.

Full text

PDF
5384

Images in this article

Selected References

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

  1. Byers B., Goetsch L. Behavior of spindles and spindle plaques in the cell cycle and conjugation of Saccharomyces cerevisiae. J Bacteriol. 1975 Oct;124(1):511–523. doi: 10.1128/jb.124.1.511-523.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Clark-Walker G. D., Miklos G. L. Localization and quantification of circular DNA in yeast. Eur J Biochem. 1974 Jan 16;41(2):359–365. doi: 10.1111/j.1432-1033.1974.tb03278.x. [DOI] [PubMed] [Google Scholar]
  3. Forte M. A., Fangman W. L. Naturally occurring cross-links in yeast chromosomal DNA. Cell. 1976 Jul;8(3):425–431. doi: 10.1016/0092-8674(76)90155-0. [DOI] [PubMed] [Google Scholar]
  4. Hopper A. K., Magee P. T., Welch S. K., Friedman M., Hall B. D. Macromolecule synthesis and breakdown in relation to sporulation and meiosis in yeast. J Bacteriol. 1974 Aug;119(2):619–628. doi: 10.1128/jb.119.2.619-628.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Livingston D. M., Hahne S. Isolation of a condensed, intracellular form of the 2-micrometer DNA plasmid of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1979 Aug;76(8):3727–3731. doi: 10.1073/pnas.76.8.3727. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Livingston D. M. Inheritance of the 2 micrometer m DNA plasmid from Saccharomyces. Genetics. 1977 May;86(1):73–84. doi: 10.1093/genetics/86.1.73. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Livingston D. M., Kupfer D. M. Control of Saccharomyces cerevisiae 2microN DNA replication by cell division cycle genes that control nuclear DNA replication. J Mol Biol. 1977 Oct 25;116(2):249–260. doi: 10.1016/0022-2836(77)90215-7. [DOI] [PubMed] [Google Scholar]
  8. Moens P. B. Fine structure of ascospore development in the yeast Saccharomyces cerevisiae. Can J Microbiol. 1971 Apr;17(4):507–510. doi: 10.1139/m71-084. [DOI] [PubMed] [Google Scholar]
  9. Moens P. B., Rapport E. Spindles, spindle plaques, and meiosis in the yeast Saccharomyces cerevisiae (Hansen). J Cell Biol. 1971 Aug;50(2):344–361. doi: 10.1083/jcb.50.2.344. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Nelson R. G., Fangman W. L. Nucleosome organization of the yeast 2-micrometer DNA plasmid: a eukaryotic minichromosome. Proc Natl Acad Sci U S A. 1979 Dec;76(12):6515–6519. doi: 10.1073/pnas.76.12.6515. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Oliver S. G., McCREADY S. J., Holm C., Sutherland P. A., McLaughlin C. S., Cox B. S. Biochemical and physiological studies of the yeast virus-like particle. J Bacteriol. 1977 Jun;130(3):1303–1309. doi: 10.1128/jb.130.3.1303-1309.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Roth R., Halvorson H. O. Sporulation of yeast harvested during logarithmic growth. J Bacteriol. 1969 May;98(2):831–832. doi: 10.1128/jb.98.2.831-832.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Wickner R. B. The killer double-stranded RNA plasmids of yeast. Plasmid. 1979 Jul;2(3):303–322. doi: 10.1016/0147-619x(79)90015-5. [DOI] [PubMed] [Google Scholar]
  14. Zakian V. A., Brewer B. J., Fangman W. L. Replication of each copy of the yeast 2 micron DNA plasmid occurs during the S phase. Cell. 1979 Aug;17(4):923–934. doi: 10.1016/0092-8674(79)90332-5. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES