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
. 1985 May;82(10):3350–3354. doi: 10.1073/pnas.82.10.3350

High-frequency meiotic gene conversion between repeated genes on nonhomologous chromosomes in yeast.

S Jinks-Robertson, T D Petes
PMCID: PMC397773  PMID: 3889906

Abstract

We have used a genetic system that allows detection of meiotic recombination events between repeated sequences on nonhomologous chromosomes in the yeast Saccharomyces cerevisiae. We have found that recombination between these sequences occurs at a frequency of about 0.5%, and the events observed were nonreciprocal (gene conversions). Surprisingly, the frequency of conversion between the repeated genes on nonhomologous chromosomes observed in this study is similar to that observed between allelic genes. This result is discussed in connection with the role of the synaptonemal complex in meiotic recombination and with the relationship between reciprocal and nonreciprocal recombination.

Full text

PDF
3350

Images in this article

Selected References

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

  1. Baltimore D. Gene conversion: some implications for immunoglobulin genes. Cell. 1981 Jun;24(3):592–594. doi: 10.1016/0092-8674(81)90082-9. [DOI] [PubMed] [Google Scholar]
  2. Botstein D., Falco S. C., Stewart S. E., Brennan M., Scherer S., Stinchcomb D. T., Struhl K., Davis R. W. Sterile host yeasts (SHY): a eukaryotic system of biological containment for recombinant DNA experiments. Gene. 1979 Dec;8(1):17–24. doi: 10.1016/0378-1119(79)90004-0. [DOI] [PubMed] [Google Scholar]
  3. Byers B., Goetsch L. Electron microscopic observations on the meiotic karyotype of diploid and tetraploid Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1975 Dec;72(12):5056–5060. doi: 10.1073/pnas.72.12.5056. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Carlson M., Botstein D. Two differentially regulated mRNAs with different 5' ends encode secreted with intracellular forms of yeast invertase. Cell. 1982 Jan;28(1):145–154. doi: 10.1016/0092-8674(82)90384-1. [DOI] [PubMed] [Google Scholar]
  5. Carpenter A. T. Meiotic roles of crossing-over and of gene conversion. Cold Spring Harb Symp Quant Biol. 1984;49:23–29. doi: 10.1101/sqb.1984.049.01.005. [DOI] [PubMed] [Google Scholar]
  6. Ernst J. F., Stewart J. W., Sherman F. The cyc1-11 mutation in yeast reverts by recombination with a nonallelic gene: composite genes determining the iso-cytochromes c. Proc Natl Acad Sci U S A. 1981 Oct;78(10):6334–6338. doi: 10.1073/pnas.78.10.6334. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fink G. R., Petes T. D. Gene conversion in the absence of reciprocal recombination. 1984 Aug 30-Sep 5Nature. 310(5980):728–729. doi: 10.1038/310728a0. [DOI] [PubMed] [Google Scholar]
  8. Gillies C. B. Synaptonemal complex and chromosome structure. Annu Rev Genet. 1975;9:91–109. doi: 10.1146/annurev.ge.09.120175.000515. [DOI] [PubMed] [Google Scholar]
  9. Hilger F., Mortimer R. K. Genetic mapping of arg1 and arg8 in Saccharomyces cerevisiae by trisomic analysis combined with interallelic complementation. J Bacteriol. 1980 Jan;141(1):270–274. doi: 10.1128/jb.141.1.270-274.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Jackson J. A., Fink G. R. Gene conversion between duplicated genetic elements in yeast. Nature. 1981 Jul 23;292(5821):306–311. doi: 10.1038/292306a0. [DOI] [PubMed] [Google Scholar]
  11. Klar A. J., Strathern J. N. Resolution of recombination intermediates generated during yeast mating type switching. 1984 Aug 30-Sep 5Nature. 310(5980):744–748. doi: 10.1038/310744a0. [DOI] [PubMed] [Google Scholar]
  12. Klein H. L. Lack of association between intrachromosomal gene conversion and reciprocal exchange. 1984 Aug 30-Sep 5Nature. 310(5980):748–753. doi: 10.1038/310748a0. [DOI] [PubMed] [Google Scholar]
  13. Klein H. L., Petes T. D. Intrachromosomal gene conversion in yeast. Nature. 1981 Jan 15;289(5794):144–148. doi: 10.1038/289144a0. [DOI] [PubMed] [Google Scholar]
  14. Liskay R. M., Stachelek J. L. Evidence for intrachromosomal gene conversion in cultured mouse cells. Cell. 1983 Nov;35(1):157–165. doi: 10.1016/0092-8674(83)90218-0. [DOI] [PubMed] [Google Scholar]
  15. Loh D. Y., Baltimore D. Sexual preference of apparent gene conversion events in MHC genes of mice. Nature. 1984 Jun 14;309(5969):639–640. doi: 10.1038/309639a0. [DOI] [PubMed] [Google Scholar]
  16. Meselson M. S., Radding C. M. A general model for genetic recombination. Proc Natl Acad Sci U S A. 1975 Jan;72(1):358–361. doi: 10.1073/pnas.72.1.358. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Mikus M. D., Petes T. D. Recombination between genes located on nonhomologous chromosomes in Saccharomyces cerevisiae. Genetics. 1982 Jul-Aug;101(3-4):369–404. doi: 10.1093/genetics/101.3-4.369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Moens P. B., Rapport E. Synaptic structures in the nuclei of sporulating yeast, Saccharomyces cerevisiae (Hansen). J Cell Sci. 1971 Nov;9(3):665–677. doi: 10.1242/jcs.9.3.665. [DOI] [PubMed] [Google Scholar]
  19. Munz P., Amstutz H., Kohli J., Leupold U. Recombination between dispersed serine tRNA genes in Schizosaccharomyces pombe. Nature. 1982 Nov 18;300(5889):225–231. doi: 10.1038/300225a0. [DOI] [PubMed] [Google Scholar]
  20. Olson L. W., Zimmermann F. K. Meiotic recombination and synaptonemal complexes in Saccharomyces cerevisiae. Mol Gen Genet. 1978 Oct 30;166(2):151–159. doi: 10.1007/BF00285917. [DOI] [PubMed] [Google Scholar]
  21. Orr-Weaver T. L., Szostak J. W., Rothstein R. J. Yeast transformation: a model system for the study of recombination. Proc Natl Acad Sci U S A. 1981 Oct;78(10):6354–6358. doi: 10.1073/pnas.78.10.6354. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Petes T. D. Unequal meiotic recombination within tandem arrays of yeast ribosomal DNA genes. Cell. 1980 Mar;19(3):765–774. doi: 10.1016/s0092-8674(80)80052-3. [DOI] [PubMed] [Google Scholar]
  23. Potier S., Winsor B., Lacroute F. Genetic selection for reciprocal translocation at chosen chromosomal sites in Saccharomyces cerevisiae. Mol Cell Biol. 1982 Sep;2(9):1025–1032. doi: 10.1128/mcb.2.9.1025. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Roeder G. S., Fink G. R. Movement of yeast transposable elements by gene conversion. Proc Natl Acad Sci U S A. 1982 Sep;79(18):5621–5625. doi: 10.1073/pnas.79.18.5621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Roeder G. S., Smith M., Lambie E. J. Intrachromosomal movement of genetically marked Saccharomyces cerevisiae transposons by gene conversion. Mol Cell Biol. 1984 Apr;4(4):703–711. doi: 10.1128/mcb.4.4.703. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Roman H., Fabre F. Gene conversion and associated reciprocal recombination are separable events in vegetative cells of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1983 Nov;80(22):6912–6916. doi: 10.1073/pnas.80.22.6912. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Rose M., Winston F. Identification of a Ty insertion within the coding sequence of the S. cerevisiae URA3 gene. Mol Gen Genet. 1984;193(3):557–560. doi: 10.1007/BF00382100. [DOI] [PubMed] [Google Scholar]
  28. Rothstein R. J. One-step gene disruption in yeast. Methods Enzymol. 1983;101:202–211. doi: 10.1016/0076-6879(83)01015-0. [DOI] [PubMed] [Google Scholar]
  29. Scherer S., Davis R. W. Recombination of dispersed repeated DNA sequences in yeast. Science. 1980 Sep 19;209(4463):1380–1384. doi: 10.1126/science.6251545. [DOI] [PubMed] [Google Scholar]
  30. Scherer S., Davis R. W. Replacement of chromosome segments with altered DNA sequences constructed in vitro. Proc Natl Acad Sci U S A. 1979 Oct;76(10):4951–4955. doi: 10.1073/pnas.76.10.4951. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Slightom J. L., Blechl A. E., Smithies O. Human fetal G gamma- and A gamma-globin genes: complete nucleotide sequences suggest that DNA can be exchanged between these duplicated genes. Cell. 1980 Oct;21(3):627–638. doi: 10.1016/0092-8674(80)90426-2. [DOI] [PubMed] [Google Scholar]
  32. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  33. Struhl K., Davis R. W. A physical, genetic and transcriptional map of the cloned his3 gene region of Saccharomyces cerevisiae. J Mol Biol. 1980 Jan 25;136(3):309–332. doi: 10.1016/0022-2836(80)90376-9. [DOI] [PubMed] [Google Scholar]
  34. Sugawara N., Szostak J. W. Recombination between sequences in nonhomologous positions. Proc Natl Acad Sci U S A. 1983 Sep;80(18):5675–5679. doi: 10.1073/pnas.80.18.5675. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Szostak J. W., Orr-Weaver T. L., Rothstein R. J., Stahl F. W. The double-strand-break repair model for recombination. Cell. 1983 May;33(1):25–35. doi: 10.1016/0092-8674(83)90331-8. [DOI] [PubMed] [Google Scholar]
  36. Szostak J. W., Wu R. Unequal crossing over in the ribosomal DNA of Saccharomyces cerevisiae. Nature. 1980 Apr 3;284(5755):426–430. doi: 10.1038/284426a0. [DOI] [PubMed] [Google Scholar]
  37. Weiss E. H., Mellor A., Golden L., Fahrner K., Simpson E., Hurst J., Flavell R. A. The structure of a mutant H-2 gene suggests that the generation of polymorphism in H-2 genes may occur by gene conversion-like events. Nature. 1983 Feb 24;301(5902):671–674. doi: 10.1038/301671a0. [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