Skip to main content
PMC home page
Genetics logoLink to Genetics
. 1994 Nov;138(3):633–647. doi: 10.1093/genetics/138.3.633

Nonhomologous Synapsis and Reduced Crossing over in a Heterozygous Paracentric Inversion in Saccharomyces Cerevisiae

M E Dresser 1, D J Ewing 1, S N Harwell 1, D Coody 1, M N Conrad 1
PMCID: PMC1206214  PMID: 7851761

Abstract

Homologous chromosome synapsis (``homosynapsis'') and crossing over are well-conserved aspects of meiotic chromosome behavior. The long-standing assumption that these two processes are causally related has been challenged recently by observations in Saccharomyces cerevisiae of significant levels of crossing over (1) between small sequences at nonhomologous locations and (2) in mutants where synapsis is abnormal or absent. In order to avoid problems of local sequence effects and of mutation pleiotropy, we have perturbed synapsis by making a set of isogenic strains that are heterozygous and homozygous for a large chromosomal paracentric inversion covering a well marked genetic interval and then measured recombination. We find that reciprocal recombination in the marked interval in heterozygotes is reduced variably across the interval, on average to ~55% of that in the homozygotes, and that positive interference still modulates crossing over. Cytologically, stable synapsis across the interval is apparently heterologous rather than homologous, consistent with the interpretation that stable homosynapsis is required to initiate or consummate a large fraction of the crossing over observed in wild-type strains. When crossing over does occur in heterozygotes, dicentric and acentric chromosomes are formed and can be visualized and quantitated on blots though not demonstrated in viable spores. We find that there is no loss of dicentric chromosomes during the two meiotic divisions and that the acentric chromosome is recovered at only 1/3 to 1/2 of the expected level.

Full Text

The Full Text of this article is available as a PDF (4.9 MB).

Selected References

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

  1. Bishop D. K., Park D., Xu L., Kleckner N. DMC1: a meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression. Cell. 1992 May 1;69(3):439–456. doi: 10.1016/0092-8674(92)90446-j. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. Craymer L. Techniques for manipulating chromosomal rearrangements and their application to Drosophila melanogaster. I. Pericentric inversions. Genetics. 1981 Sep;99(1):75–97. doi: 10.1093/genetics/99.1.75. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Davidow L. S., Goetsch L., Byers B. Preferential Occurrence of Nonsister Spores in Two-Spored Asci of SACCHAROMYCES CEREVISIAE: Evidence for Regulation of Spore-Wall Formation by the Spindle Pole Body. Genetics. 1980 Mar;94(3):581–595. doi: 10.1093/genetics/94.3.581. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Engebrecht J., Hirsch J., Roeder G. S. Meiotic gene conversion and crossing over: their relationship to each other and to chromosome synapsis and segregation. Cell. 1990 Sep 7;62(5):927–937. doi: 10.1016/0092-8674(90)90267-i. [DOI] [PubMed] [Google Scholar]
  6. Game J. C. Pulsed-field gel analysis of the pattern of DNA double-strand breaks in the Saccharomyces genome during meiosis. Dev Genet. 1992;13(6):485–497. doi: 10.1002/dvg.1020130610. [DOI] [PubMed] [Google Scholar]
  7. Game J. C., Sitney K. C., Cook V. E., Mortimer R. K. Use of a ring chromosome and pulsed-field gels to study interhomolog recombination, double-strand DNA breaks and sister-chromatid exchange in yeast. Genetics. 1989 Dec;123(4):695–713. doi: 10.1093/genetics/123.4.695. [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. Haber J. E., Thorburn P. C., Rogers D. Meiotic and mitotic behavior of dicentric chromosomes in Saccharomyces cerevisiae. Genetics. 1984 Feb;106(2):185–205. doi: 10.1093/genetics/106.2.185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hawley R. S., Arbel T. Yeast genetics and the fall of the classical view of meiosis. Cell. 1993 Feb 12;72(3):301–303. doi: 10.1016/0092-8674(93)90108-3. [DOI] [PubMed] [Google Scholar]
  11. Hill A., Bloom K. Acquisition and processing of a conditional dicentric chromosome in Saccharomyces cerevisiae. Mol Cell Biol. 1989 Mar;9(3):1368–1370. doi: 10.1128/mcb.9.3.1368. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hollingsworth N. M., Byers B. HOP1: a yeast meiotic pairing gene. Genetics. 1989 Mar;121(3):445–462. doi: 10.1093/genetics/121.3.445. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. 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]
  14. Kaback D. B., Guacci V., Barber D., Mahon J. W. Chromosome size-dependent control of meiotic recombination. Science. 1992 Apr 10;256(5054):228–232. doi: 10.1126/science.1566070. [DOI] [PubMed] [Google Scholar]
  15. King J. S., Mortimer R. K. A mathematical model of interference for use in constructing linkage maps from tetrad data. Genetics. 1991 Oct;129(2):597–602. doi: 10.1093/genetics/129.2.597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. King J. S., Mortimer R. K. A polymerization model of chiasma interference and corresponding computer simulation. Genetics. 1990 Dec;126(4):1127–1138. doi: 10.1093/genetics/126.4.1127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lichten M., Borts R. H., Haber J. E. Meiotic gene conversion and crossing over between dispersed homologous sequences occurs frequently in Saccharomyces cerevisiae. Genetics. 1987 Feb;115(2):233–246. doi: 10.1093/genetics/115.2.233. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Loidl J., Nairz K., Klein F. Meiotic chromosome synapsis in a haploid yeast. Chromosoma. 1991 May;100(4):221–228. doi: 10.1007/BF00344155. [DOI] [PubMed] [Google Scholar]
  19. Ma C., Mortimer R. K. Empirical equation that can be used to determine genetic map distances from tetrad data. Mol Cell Biol. 1983 Oct;3(10):1886–1887. doi: 10.1128/mcb.3.10.1886. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Maguire M. P., Riess R. W. The relationship of homologous synapsis and crossing over in a maize inversion. Genetics. 1994 May;137(1):281–288. doi: 10.1093/genetics/137.1.281. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Moens P. B., Ashton M. L. Synaptonemal complexes of normal and mutant yeast chromosomes (Saccharomyces cerevisiae). Chromosoma. 1985;91(2):113–120. doi: 10.1007/BF00294054. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. Moses M. J., Poorman P. A., Roderick T. H., Davisson M. T. Synaptonemal complex analysis of mouse chromosomal rearrangements. IV. Synapsis and synaptic adjustment in two paracentric inversions. Chromosoma. 1982;84(4):457–474. doi: 10.1007/BF00292848. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. 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]
  26. Perkins D. D. Biochemical Mutants in the Smut Fungus Ustilago Maydis. Genetics. 1949 Sep;34(5):607–626. doi: 10.1093/genetics/34.5.607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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]
  28. Ross L. O., Treco D., Nicolas A., Szostak J. W., Dawson D. Meiotic recombination on artificial chromosomes in yeast. Genetics. 1992 Jul;131(3):541–550. doi: 10.1093/genetics/131.3.541. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Runge K. W., Zakian V. A. Introduction of extra telomeric DNA sequences into Saccharomyces cerevisiae results in telomere elongation. Mol Cell Biol. 1989 Apr;9(4):1488–1497. doi: 10.1128/mcb.9.4.1488. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Schiestl R. H., Gietz R. D. High efficiency transformation of intact yeast cells using single stranded nucleic acids as a carrier. Curr Genet. 1989 Dec;16(5-6):339–346. doi: 10.1007/BF00340712. [DOI] [PubMed] [Google Scholar]
  31. Sturtevant A H, Beadle G W. The Relations of Inversions in the X Chromosome of Drosophila Melanogaster to Crossing over and Disjunction. Genetics. 1936 Sep;21(5):554–604. doi: 10.1093/genetics/21.5.554. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. 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]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES