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. 1996 Sep;144(1):43–55. doi: 10.1093/genetics/144.1.43

The Efficiency of Meiotic Recombination between Dispersed Sequences in Saccharomyces Cerevisiae Depends upon Their Chromosomal Location

ASH Goldman 1, M Lichten 1
PMCID: PMC1207516  PMID: 8878672

Abstract

To examine constraints imposed on meiotic recombination by homologue pairing, we measured the frequency of recombination between mutant alleles of the ARG4 gene contained in pBR322-based inserts. Inserts were located at identical loci on homologues (allelic recombination) or at different loci on either homologous or heterologous chromosomes (ectopic recombination). Ectopic recombination between interstitially located inserts on heterologous chromosomes had an efficiency of 6-12% compared to allelic recombination. By contrast, ectopic recombination between interstitial inserts located on homologues had relative efficiencies of 47-99%. These findings suggest that when meiotic ectopic recombination occurs, homologous chromosomes are already colocalized. The efficiency of ectopic recombination between inserts on homologues decreased as the physical distance between insert sites was increased. This result is consistent with the suggestion that during meiotic recombination, homologues are not only close to each other, but also are aligned end to end. Finally, the efficiency of ectopic recombination between inserts near telomeres (within 16 kb) was significantly greater than that observed with inserts >50 kb from the nearest telomere. Thus, at the time of recombination, there may be a special relationship between the ends of chromosomes not shared with interstitial regions.

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Selected References

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  1. Bennett M. D. Premeiotic events and meiotic chromosome pairing. Symp Soc Exp Biol. 1984;38:87–121. [PubMed] [Google Scholar]
  2. 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]
  3. Cao L., Alani E., Kleckner N. A pathway for generation and processing of double-strand breaks during meiotic recombination in S. cerevisiae. Cell. 1990 Jun 15;61(6):1089–1101. doi: 10.1016/0092-8674(90)90072-m. [DOI] [PubMed] [Google Scholar]
  4. Collins I., Newlon C. S. Meiosis-specific formation of joint DNA molecules containing sequences from homologous chromosomes. Cell. 1994 Jan 14;76(1):65–75. doi: 10.1016/0092-8674(94)90173-2. [DOI] [PubMed] [Google Scholar]
  5. Datta A., Adjiri A., New L., Crouse G. F., Jinks Robertson S. Mitotic crossovers between diverged sequences are regulated by mismatch repair proteins in Saccaromyces cerevisiae. Mol Cell Biol. 1996 Mar;16(3):1085–1093. doi: 10.1128/mcb.16.3.1085. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Diaz G., Lewis K. R. Interphase chromosome arrangement in Anopheles atroparvus. Chromosoma. 1975 Sep 15;52(1):27–35. doi: 10.1007/BF00285786. [DOI] [PubMed] [Google Scholar]
  7. Dresser M. E., Giroux C. N. Meiotic chromosome behavior in spread preparations of yeast. J Cell Biol. 1988 Mar;106(3):567–573. doi: 10.1083/jcb.106.3.567. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Goyon C., Lichten M. Timing of molecular events in meiosis in Saccharomyces cerevisiae: stable heteroduplex DNA is formed late in meiotic prophase. Mol Cell Biol. 1993 Jan;13(1):373–382. doi: 10.1128/mcb.13.1.373. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hinterberg K., Mattei D., Wellems T. E., Scherf A. Interchromosomal exchange of a large subtelomeric segment in a Plasmodium falciparum cross. EMBO J. 1994 Sep 1;13(17):4174–4180. doi: 10.1002/j.1460-2075.1994.tb06735.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Ibeas J. I., Jimenez J. Electrophoretic karyotype of budding yeasts with intact cell wall. Nucleic Acids Res. 1993 Aug 11;21(16):3902–3902. doi: 10.1093/nar/21.16.3902. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Janse C. J., Mons B. Deletion, insertion and translocation of DNA sequences contribute to chromosome size polymorphism in Plasmodium berghei. Mem Inst Oswaldo Cruz. 1992;87 (Suppl 3):95–100. doi: 10.1590/s0074-02761992000700013. [DOI] [PubMed] [Google Scholar]
  12. Jinks-Robertson S., Petes T. D. Chromosomal translocations generated by high-frequency meiotic recombination between repeated yeast genes. Genetics. 1986 Nov;114(3):731–752. doi: 10.1093/genetics/114.3.731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Johnston M., Andrews S., Brinkman R., Cooper J., Ding H., Dover J., Du Z., Favello A., Fulton L., Gattung S. Complete nucleotide sequence of Saccharomyces cerevisiae chromosome VIII. Science. 1994 Sep 30;265(5181):2077–2082. doi: 10.1126/science.8091229. [DOI] [PubMed] [Google Scholar]
  14. Kleckner N., Weiner B. M. Potential advantages of unstable interactions for pairing of chromosomes in meiotic, somatic, and premeiotic cells. Cold Spring Harb Symp Quant Biol. 1993;58:553–565. doi: 10.1101/sqb.1993.058.01.062. [DOI] [PubMed] [Google Scholar]
  15. Klein F., Laroche T., Cardenas M. E., Hofmann J. F., Schweizer D., Gasser S. M. Localization of RAP1 and topoisomerase II in nuclei and meiotic chromosomes of yeast. J Cell Biol. 1992 Jun;117(5):935–948. doi: 10.1083/jcb.117.5.935. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lichten M., Goyon C., Schultes N. P., Treco D., Szostak J. W., Haber J. E., Nicolas A. Detection of heteroduplex DNA molecules among the products of Saccharomyces cerevisiae meiosis. Proc Natl Acad Sci U S A. 1990 Oct;87(19):7653–7657. doi: 10.1073/pnas.87.19.7653. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Loidl J. The initiation of meiotic chromosome pairing: the cytological view. Genome. 1990 Dec;33(6):759–778. doi: 10.1139/g90-115. [DOI] [PubMed] [Google Scholar]
  18. Murti J. R., Bumbulis M., Schimenti J. C. Gene conversion between unlinked sequences in the germline of mice. Genetics. 1994 Jul;137(3):837–843. doi: 10.1093/genetics/137.3.837. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Nag D. K., Petes T. D. Meiotic recombination between dispersed repeated genes is associated with heteroduplex formation. Mol Cell Biol. 1990 Aug;10(8):4420–4423. doi: 10.1128/mcb.10.8.4420. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Nag D. K., Petes T. D. Physical detection of heteroduplexes during meiotic recombination in the yeast Saccharomyces cerevisiae. Mol Cell Biol. 1993 Apr;13(4):2324–2331. doi: 10.1128/mcb.13.4.2324. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Oliver S. G., van der Aart Q. J., Agostoni-Carbone M. L., Aigle M., Alberghina L., Alexandraki D., Antoine G., Anwar R., Ballesta J. P., Benit P. The complete DNA sequence of yeast chromosome III. Nature. 1992 May 7;357(6373):38–46. doi: 10.1038/357038a0. [DOI] [PubMed] [Google Scholar]
  22. Padmore R., Cao L., Kleckner N. Temporal comparison of recombination and synaptonemal complex formation during meiosis in S. cerevisiae. Cell. 1991 Sep 20;66(6):1239–1256. doi: 10.1016/0092-8674(91)90046-2. [DOI] [PubMed] [Google Scholar]
  23. Palladino F., Laroche T., Gilson E., Pillus L., Gasser S. M. The positioning of yeast telomeres depends on SIR3, SIR4, and the integrity of the nuclear membrane. Cold Spring Harb Symp Quant Biol. 1993;58:733–746. doi: 10.1101/sqb.1993.058.01.081. [DOI] [PubMed] [Google Scholar]
  24. Rockmill B., Roeder G. S. Meiosis in asynaptic yeast. Genetics. 1990 Nov;126(3):563–574. doi: 10.1093/genetics/126.3.563. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Scherthan H., Bähler J., Kohli J. Dynamics of chromosome organization and pairing during meiotic prophase in fission yeast. J Cell Biol. 1994 Oct;127(2):273–285. doi: 10.1083/jcb.127.2.273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Scherthan H., Loidl J., Schuster T., Schweizer D. Meiotic chromosome condensation and pairing in Saccharomyces cerevisiae studied by chromosome painting. Chromosoma. 1992 Oct;101(10):590–595. doi: 10.1007/BF00360535. [DOI] [PubMed] [Google Scholar]
  27. Schwacha A., Kleckner N. Identification of double Holliday junctions as intermediates in meiotic recombination. Cell. 1995 Dec 1;83(5):783–791. doi: 10.1016/0092-8674(95)90191-4. [DOI] [PubMed] [Google Scholar]
  28. Schwacha A., Kleckner N. Identification of joint molecules that form frequently between homologs but rarely between sister chromatids during yeast meiosis. Cell. 1994 Jan 14;76(1):51–63. doi: 10.1016/0092-8674(94)90172-4. [DOI] [PubMed] [Google Scholar]
  29. Selva E. M., New L., Crouse G. F., Lahue R. S. Mismatch correction acts as a barrier to homeologous recombination in Saccharomyces cerevisiae. Genetics. 1995 Mar;139(3):1175–1188. doi: 10.1093/genetics/139.3.1175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Steele D. F., Morris M. E., Jinks-Robertson S. Allelic and ectopic interactions in recombination-defective yeast strains. Genetics. 1991 Jan;127(1):53–60. doi: 10.1093/genetics/127.1.53. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Sun H., Treco D., Schultes N. P., Szostak J. W. Double-strand breaks at an initiation site for meiotic gene conversion. Nature. 1989 Mar 2;338(6210):87–90. doi: 10.1038/338087a0. [DOI] [PubMed] [Google Scholar]
  32. Sym M., Engebrecht J. A., Roeder G. S. ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell. 1993 Feb 12;72(3):365–378. doi: 10.1016/0092-8674(93)90114-6. [DOI] [PubMed] [Google Scholar]
  33. Therman E., Sarto G. E. Premeiotic and early meiotic stages in the pollen mother cells of Eremurus and in human embryonic oocytes. Hum Genet. 1977 Feb 11;35(2):137–151. doi: 10.1007/BF00393963. [DOI] [PubMed] [Google Scholar]
  34. Weiner B. M., Kleckner N. Chromosome pairing via multiple interstitial interactions before and during meiosis in yeast. Cell. 1994 Jul 1;77(7):977–991. doi: 10.1016/0092-8674(94)90438-3. [DOI] [PubMed] [Google Scholar]
  35. Wu T. C., Lichten M. Factors that affect the location and frequency of meiosis-induced double-strand breaks in Saccharomyces cerevisiae. Genetics. 1995 May;140(1):55–66. doi: 10.1093/genetics/140.1.55. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. de Bruin D., Lanzer M., Ravetch J. V. The polymorphic subtelomeric regions of Plasmodium falciparum chromosomes contain arrays of repetitive sequence elements. Proc Natl Acad Sci U S A. 1994 Jan 18;91(2):619–623. doi: 10.1073/pnas.91.2.619. [DOI] [PMC free article] [PubMed] [Google Scholar]

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