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. 1994 Dec 6;91(25):11929–11933. doi: 10.1073/pnas.91.25.11929

Initiation of recombination in Saccharomyces cerevisiae haploid meiosis.

B De Massy 1, F Baudat 1, A Nicolas 1
PMCID: PMC45349  PMID: 7991559

Abstract

In most eukaryotes during prophase I of meiosis, homologous chromosomes pair and recombine by coordinated molecular and cellular processes. To directly test whether or not the early steps of the initiation of recombination depend on the presence of a homologous chromosome, we have examined the formation and processing of DNA double-strand breaks (DSBs, the earliest physical landmark of recombination initiation) in various haploid Saccharomyces cerevisiae strains capable of entering meiosis. We find that DSBs occur in haploid meiosis, showing that the presence of a homolog is not required for DSB formation. DSBs occur at the same positions in haploid and diploid meioses. However, these two types of meiosis exhibit subtle differences with respect to the timing of formation and levels of DSBs. In haploid meiosis, a slower rate of DSB formation and a reduction in the frequency of DSB (at one of the three sites analyzed) were observed. These results might indicate that interactions between homologs play a role in the formation of meiotic DSBs. Furthermore, haploid strains exhibit a pronounced delay in the disappearance of meiotic DSBs compared to diploid strains, which suggests that sister chromatid interactions for DSB repair are inhibited in haploid meiosis.

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Selected References

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

  1. Alani E., Padmore R., Kleckner N. Analysis of wild-type and rad50 mutants of yeast suggests an intimate relationship between meiotic chromosome synapsis and recombination. Cell. 1990 May 4;61(3):419–436. doi: 10.1016/0092-8674(90)90524-i. [DOI] [PubMed] [Google Scholar]
  2. Atcheson C. L., Esposito R. E. Meiotic recombination in yeast. Curr Opin Genet Dev. 1993 Oct;3(5):736–744. doi: 10.1016/s0959-437x(05)80092-9. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. 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]
  5. Cherest H., Surdin-Kerjan Y. Genetic analysis of a new mutation conferring cysteine auxotrophy in Saccharomyces cerevisiae: updating of the sulfur metabolism pathway. Genetics. 1992 Jan;130(1):51–58. doi: 10.1093/genetics/130.1.51. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. 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]
  7. Covitz P. A., Herskowitz I., Mitchell A. P. The yeast RME1 gene encodes a putative zinc finger protein that is directly repressed by a1-alpha 2. Genes Dev. 1991 Nov;5(11):1982–1989. doi: 10.1101/gad.5.11.1982. [DOI] [PubMed] [Google Scholar]
  8. Gilbertson L. A., Stahl F. W. Initiation of meiotic recombination is independent of interhomologue interactions. Proc Natl Acad Sci U S A. 1994 Dec 6;91(25):11934–11937. doi: 10.1073/pnas.91.25.11934. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  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. Herskowitz I. Life cycle of the budding yeast Saccharomyces cerevisiae. Microbiol Rev. 1988 Dec;52(4):536–553. doi: 10.1128/mr.52.4.536-553.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Heude M., Fabre F. a/alpha-control of DNA repair in the yeast Saccharomyces cerevisiae: genetic and physiological aspects. Genetics. 1993 Mar;133(3):489–498. doi: 10.1093/genetics/133.3.489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Jackson J. A., Fink G. R. Meiotic recombination between duplicated genetic elements in Saccharomyces cerevisiae. Genetics. 1985 Feb;109(2):303–332. doi: 10.1093/genetics/109.2.303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kleckner N., Padmore R., Bishop D. K. Meiotic chromosome metabolism: one view. Cold Spring Harb Symp Quant Biol. 1991;56:729–743. doi: 10.1101/sqb.1991.056.01.082. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. 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]
  17. Mitchell A. P., Herskowitz I. Activation of meiosis and sporulation by repression of the RME1 product in yeast. 1986 Feb 27-Mar 5Nature. 319(6056):738–742. doi: 10.1038/319738a0. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Nicolas A., Treco D., Schultes N. P., Szostak J. W. An initiation site for meiotic gene conversion in the yeast Saccharomyces cerevisiae. Nature. 1989 Mar 2;338(6210):35–39. doi: 10.1038/338035a0. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. Resnick M. A., Stasiewicz S., Game J. C. Meiotic DNA metabolism in wild-type and excision-deficient yeast following UV exposure. Genetics. 1983 Aug;104(4):583–601. doi: 10.1093/genetics/104.4.583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Rine J., Herskowitz I. Four genes responsible for a position effect on expression from HML and HMR in Saccharomyces cerevisiae. Genetics. 1987 May;116(1):9–22. doi: 10.1093/genetics/116.1.9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Rocco V., Daly M. J., Matre V., Lichten M., Nicolas A. Identification of two divergently transcribed genes centromere-proximal to the ARG4 locus on chromosome VIII of Saccharomyces cerevisiae. Yeast. 1993 Oct;9(10):1111–1120. doi: 10.1002/yea.320091012. [DOI] [PubMed] [Google Scholar]
  24. Rocco V., de Massy B., Nicolas A. The Saccharomyces cerevisiae ARG4 initiator of meiotic gene conversion and its associated double-strand DNA breaks can be inhibited by transcriptional interference. Proc Natl Acad Sci U S A. 1992 Dec 15;89(24):12068–12072. doi: 10.1073/pnas.89.24.12068. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Roeder G. S. Chromosome synapsis and genetic recombination: their roles in meiotic chromosome segregation. Trends Genet. 1990 Dec;6(12):385–389. doi: 10.1016/0168-9525(90)90297-j. [DOI] [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. Schultes N. P., Szostak J. W. A poly(dA.dT) tract is a component of the recombination initiation site at the ARG4 locus in Saccharomyces cerevisiae. Mol Cell Biol. 1991 Jan;11(1):322–328. doi: 10.1128/mcb.11.1.322. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Schultes N. P., Szostak J. W. Decreasing gradients of gene conversion on both sides of the initiation site for meiotic recombination at the ARG4 locus in yeast. Genetics. 1990 Dec;126(4):813–822. doi: 10.1093/genetics/126.4.813. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. 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]
  30. Sikorski R. S., Hieter P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics. 1989 May;122(1):19–27. doi: 10.1093/genetics/122.1.19. [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. Sun H., Treco D., Szostak J. W. Extensive 3'-overhanging, single-stranded DNA associated with the meiosis-specific double-strand breaks at the ARG4 recombination initiation site. Cell. 1991 Mar 22;64(6):1155–1161. doi: 10.1016/0092-8674(91)90270-9. [DOI] [PubMed] [Google Scholar]
  33. Wagstaff J. E., Klapholz S., Waddell C. S., Jensen L., Esposito R. E. Meiotic exchange within and between chromosomes requires a common Rec function in Saccharomyces cerevisiae. Mol Cell Biol. 1985 Dec;5(12):3532–3544. doi: 10.1128/mcb.5.12.3532. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Wu T. C., Lichten M. Meiosis-induced double-strand break sites determined by yeast chromatin structure. Science. 1994 Jan 28;263(5146):515–518. doi: 10.1126/science.8290959. [DOI] [PubMed] [Google Scholar]
  35. Zenvirth D., Arbel T., Sherman A., Goldway M., Klein S., Simchen G. Multiple sites for double-strand breaks in whole meiotic chromosomes of Saccharomyces cerevisiae. EMBO J. 1992 Sep;11(9):3441–3447. doi: 10.1002/j.1460-2075.1992.tb05423.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. de Massy B., Nicolas A. The control in cis of the position and the amount of the ARG4 meiotic double-strand break of Saccharomyces cerevisiae. EMBO J. 1993 Apr;12(4):1459–1466. doi: 10.1002/j.1460-2075.1993.tb05789.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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