Skip to main content
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1984 Sep 25;12(18):7199–7213. doi: 10.1093/nar/12.18.7199

Correlation between suppressed meiotic recombination and the lack of DNA strand-breaks in the rRNA genes of Saccharomyces cerevisiae.

A Høgset, T B Oyen
PMCID: PMC320151  PMID: 6384933

Abstract

We have examined whether the suppressed homologous meiotic recombination within the rDNA of S. cerevisiae is reflected by a lack of possibly recombination-initiating strand-breaks in this part of the genome. Our findings indicate that bulk DNA in the ds-break repair deficient mutant rad52/rad52 accumulates a limited number of both ss- and ds-breaks during meiosis as compared to a RAD+/rad52 heterozygote. The rDNA-containing chromosome is however protected against these breaks, and thus this may be an explanation for the suppression of recombination in the rDNA. The fact that ds-breaks seem to be involved gives indirect support to the ds-break-repair model for recombination.

Full text

PDF
7199

Selected References

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

  1. Blamire J., Cryer D. R., Finkelstein D. B., Marmur J. Sedimentation properties of yeast nuclear and mitochondrial DNA. J Mol Biol. 1972 Jun 14;67(1):11–24. doi: 10.1016/0022-2836(72)90382-8. [DOI] [PubMed] [Google Scholar]
  2. Davidow L. S., Byers B. Enhanced gene conversion and postmeiotic segregation in pachytene-arrested Saccharomyces cerevisiae. Genetics. 1984 Feb;106(2):165–183. doi: 10.1093/genetics/106.2.165. [DOI] [PMC free article] [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. Freifelder D. Molecular weights of coliphages and coliphage DNA. IV. Molecular weights of DNA from bacteriophages T4, T5 and T7 and the general problem of determination of M. J Mol Biol. 1970 Dec 28;54(3):567–577. doi: 10.1016/0022-2836(70)90127-0. [DOI] [PubMed] [Google Scholar]
  5. Game J. C., Mortimer R. K. A genetic study of x-ray sensitive mutants in yeast. Mutat Res. 1974 Sep;24(3):281–292. doi: 10.1016/0027-5107(74)90176-6. [DOI] [PubMed] [Google Scholar]
  6. Game J. C., Zamb T. J., Braun R. J., Resnick M., Roth R. M. The Role of Radiation (rad) Genes in Meiotic Recombination in Yeast. Genetics. 1980 Jan;94(1):51–68. doi: 10.1093/genetics/94.1.51. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Green M. H., Medcalf A. S., Arlett C. F., Harcourt S. A., Lehmann A. R. DNA strand breakage caused by dichlorvos, methyl methanesulphonate and iodoacetamide in Escherichia coli and cultured Chinese hamster cells. Mutat Res. 1974 Sep;24(3):365–378. doi: 10.1016/0027-5107(74)90181-x. [DOI] [PubMed] [Google Scholar]
  8. Hotta Y., Stern H. Small nuclear RNA molecules that regulate nuclease accessibility in specific chromatin regions of meiotic cells. Cell. 1981 Dec;27(2 Pt 1):309–319. doi: 10.1016/0092-8674(81)90414-1. [DOI] [PubMed] [Google Scholar]
  9. Howell S. H., Stern H. The appearance of DNA breakage and repair activities in the synchronous meiotic cycle of Lilium. J Mol Biol. 1971 Feb 14;55(3):357–378. doi: 10.1016/0022-2836(71)90323-8. [DOI] [PubMed] [Google Scholar]
  10. Jacobson G. K., Pinon R., Esposito R. E., Esposito M. S. Single-strand scissions of chromosomal DNA during commitment to recombination at meiosis. Proc Natl Acad Sci U S A. 1975 May;72(5):1887–1891. doi: 10.1073/pnas.72.5.1887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kaback D. B., Davidson N. Organization of the ribosomal RNA gene cluster in the yeast Saccharomyces cerevisiae. J Mol Biol. 1980 Apr 25;138(4):745–754. doi: 10.1016/0022-2836(80)90063-7. [DOI] [PubMed] [Google Scholar]
  12. Kane S. M., Roth R. Carbohydrate metabolism during ascospore development in yeast. J Bacteriol. 1974 Apr;118(1):8–14. doi: 10.1128/jb.118.1.8-14.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kostriken R., Strathern J. N., Klar A. J., Hicks J. B., Heffron F. A site-specific endonuclease essential for mating-type switching in Saccharomyces cerevisiae. Cell. 1983 Nov;35(1):167–174. doi: 10.1016/0092-8674(83)90219-2. [DOI] [PubMed] [Google Scholar]
  14. Levin D., Hutchinson F. Relation between single-strand DNA mass and sedimentation distance in alkaline sucrose gradients. J Mol Biol. 1973 Apr 15;75(3):495–502. doi: 10.1016/0022-2836(73)90456-7. [DOI] [PubMed] [Google Scholar]
  15. Malone R. E., Esposito R. E. The RAD52 gene is required for homothallic interconversion of mating types and spontaneous mitotic recombination in yeast. Proc Natl Acad Sci U S A. 1980 Jan;77(1):503–507. doi: 10.1073/pnas.77.1.503. [DOI] [PMC free article] [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. Mortimer R. K., Schild D. Genetic map of Saccharomyces cerevisiae. Microbiol Rev. 1980 Dec;44(4):519–571. doi: 10.1128/mr.44.4.519-571.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Nasmyth K. Molecular analysis of a cell lineage. Nature. 1983 Apr 21;302(5910):670–676. doi: 10.1038/302670a0. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. Orr-Weaver T. L., Szostak J. W. Yeast recombination: the association between double-strand gap repair and crossing-over. Proc Natl Acad Sci U S A. 1983 Jul;80(14):4417–4421. doi: 10.1073/pnas.80.14.4417. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Oyen T. B., Saelid G., Skuladottir G. V. Study of a haploid yeast strain with an unusually high rDNA content. III. Unequal meiotic segregation of the gamma-DNA fraction. Biochim Biophys Acta. 1978 Aug 23;520(1):88–102. doi: 10.1016/0005-2787(78)90010-2. [DOI] [PubMed] [Google Scholar]
  22. Petes T. D., Botstein D. Simple Mendelian inheritance of the reiterated ribosomal DNA of yeast. Proc Natl Acad Sci U S A. 1977 Nov;74(11):5091–5095. doi: 10.1073/pnas.74.11.5091. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Petes T. D., Byers B., Fangman W. L. Size and structure of yeast chromosomal DNA. Proc Natl Acad Sci U S A. 1973 Nov;70(11):3072–3076. doi: 10.1073/pnas.70.11.3072. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Petes T. D. Meiotic mapping of yeast ribosomal deoxyribonucleic acid on chromosome XII. J Bacteriol. 1979 Apr;138(1):185–192. doi: 10.1128/jb.138.1.185-192.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. 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]
  26. Petes T. D. Yeast ribosomal DNA genes are located on chromosome XII. Proc Natl Acad Sci U S A. 1979 Jan;76(1):410–414. doi: 10.1073/pnas.76.1.410. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Piñon R., Salts Y. Isolation of folded chromosomes from the yeast Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1977 Jul;74(7):2850–2854. doi: 10.1073/pnas.74.7.2850. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Prakash S., Prakash L., Burke W., Montelone B. A. Effects of the RAD52 Gene on Recombination in SACCHAROMYCES CEREVISIAE. Genetics. 1980 Jan;94(1):31–50. doi: 10.1093/genetics/94.1.31. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Resnick M. A. Genetic control of radiation sensitivity in Saccharomyces cerevisiae. Genetics. 1969 Jul;62(3):519–531. doi: 10.1093/genetics/62.3.519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Resnick M. A., Kasimos J. N., Game J. C., Braun R. J., Roth R. M. Changes in DNA during meiosis in a repair-deficient mutant (rad 52) of yeast. Science. 1981 May 1;212(4494):543–545. doi: 10.1126/science.7010606. [DOI] [PubMed] [Google Scholar]
  31. Resnick M. A., Martin P. The repair of double-strand breaks in the nuclear DNA of Saccharomyces cerevisiae and its genetic control. Mol Gen Genet. 1976 Jan 16;143(2):119–129. doi: 10.1007/BF00266917. [DOI] [PubMed] [Google Scholar]
  32. Resnick M. A. The repair of double-strand breaks in DNA; a model involving recombination. J Theor Biol. 1976 Jun;59(1):97–106. doi: 10.1016/s0022-5193(76)80025-2. [DOI] [PubMed] [Google Scholar]
  33. Rubin G. M. Preparation of RNA and ribosomes from yeast. Methods Cell Biol. 1975;12:45–64. doi: 10.1016/s0091-679x(08)60951-6. [DOI] [PubMed] [Google Scholar]
  34. SHERMAN F., ROMAN H. Evidence for two types of allelic recombination in yeast. Genetics. 1963 Feb;48:255–261. doi: 10.1093/genetics/48.2.255. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Silva-Lopez E., Zamb T. J., Roth R. Role of premeiotic replication in gene conversion. Nature. 1975 Jan 17;253(5488):212–214. doi: 10.1038/253212a0. [DOI] [PubMed] [Google Scholar]
  36. Simchen G., Piñon R., Salts Y. Sporulation in Saccharomyces cerevisiae: premeiotic DNA synthesis, readiness and commitment. Exp Cell Res. 1972 Nov;75(1):207–218. doi: 10.1016/0014-4827(72)90538-1. [DOI] [PubMed] [Google Scholar]
  37. Stahl F. W. Special sites in generalized recombination. Annu Rev Genet. 1979;13:7–24. doi: 10.1146/annurev.ge.13.120179.000255. [DOI] [PubMed] [Google Scholar]
  38. Strathern J. N., Klar A. J., Hicks J. B., Abraham J. A., Ivy J. M., Nasmyth K. A., McGill C. Homothallic switching of yeast mating type cassettes is initiated by a double-stranded cut in the MAT locus. Cell. 1982 Nov;31(1):183–192. doi: 10.1016/0092-8674(82)90418-4. [DOI] [PubMed] [Google Scholar]
  39. Symington L. S., Fogarty L. M., Kolodner R. Genetic recombination of homologous plasmids catalyzed by cell-free extracts of Saccharomyces cerevisiae. Cell. 1983 Dec;35(3 Pt 2):805–813. doi: 10.1016/0092-8674(83)90113-7. [DOI] [PubMed] [Google Scholar]
  40. Szauter P. An analysis of regional constraints on exchange in Drosophila melanogaster using recombination-defective meiotic mutants. Genetics. 1984 Jan;106(1):45–71. doi: 10.1093/genetics/106.1.45. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. 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]
  42. 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]
  43. Watabe H., Iino T., Kaneko T., Shibata T., Ando T. A new class of site-specific endodeoxyribonucleases. Endo.Sce I isolated from a eukaryote, Saccharomyces cerevisiae. J Biol Chem. 1983 Apr 25;258(8):4663–4665. [PubMed] [Google Scholar]
  44. Watabe H., Shibata T., Ando T. Site-specific endo-deoxyribonucleases in eukaryotes: endonucleases of yeasts, Saccharomyces and Pichia. J Biochem. 1981 Dec;90(6):1623–1632. doi: 10.1093/oxfordjournals.jbchem.a133637. [DOI] [PubMed] [Google Scholar]
  45. Weiffenbach B., Haber J. E. Homothallic mating type switching generates lethal chromosome breaks in rad52 strains of Saccharomyces cerevisiae. Mol Cell Biol. 1981 Jun;1(6):522–534. doi: 10.1128/mcb.1.6.522. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES