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. 2004 Jul;167(3):1133–1142. doi: 10.1534/genetics.104.026260

A role for DNA polymerase delta in gene conversion and crossing over during meiosis in Saccharomyces cerevisiae.

Laurent Maloisel 1, Jaya Bhargava 1, G Shirleen Roeder 1
PMCID: PMC1470953  PMID: 15280229

Abstract

A screen for mutants of budding yeast defective in meiotic gene conversion identified a novel allele of the POL3 gene. POL3 encodes the catalytic subunit of DNA polymerase delta, an essential DNA polymerase involved in genomic DNA replication. The new allele, pol3-ct, specifies a protein missing the last four amino acids. pol3-ct shows little or no defect in DNA replication, but displays a reduction in the length of meiotic gene conversion tracts and a decrease in crossing over. We propose a model in which DNA synthesis determines the length of strand exchange intermediates and influences their resolution toward crossing over.

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Selected References

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  1. Aguilera A., Klein H. L. Genetic control of intrachromosomal recombination in Saccharomyces cerevisiae. I. Isolation and genetic characterization of hyper-recombination mutations. Genetics. 1988 Aug;119(4):779–790. doi: 10.1093/genetics/119.4.779. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Alani E., Reenan R. A., Kolodner R. D. Interaction between mismatch repair and genetic recombination in Saccharomyces cerevisiae. Genetics. 1994 May;137(1):19–39. doi: 10.1093/genetics/137.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Allers T., Lichten M. Differential timing and control of noncrossover and crossover recombination during meiosis. Cell. 2001 Jul 13;106(1):47–57. doi: 10.1016/s0092-8674(01)00416-0. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. Chua P. R., Roeder G. S. Tam1, a telomere-associated meiotic protein, functions in chromosome synapsis and crossover interference. Genes Dev. 1997 Jul 15;11(14):1786–1800. doi: 10.1101/gad.11.14.1786. [DOI] [PubMed] [Google Scholar]
  6. Conrad M. N., Newlon C. S. Saccharomyces cerevisiae cdc2 mutants fail to replicate approximately one-third of their nuclear genome. Mol Cell Biol. 1983 Jun;3(6):1000–1012. doi: 10.1128/mcb.3.6.1000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Datta A., Schmeits J. L., Amin N. S., Lau P. J., Myung K., Kolodner R. D. Checkpoint-dependent activation of mutagenic repair in Saccharomyces cerevisiae pol3-01 mutants. Mol Cell. 2000 Sep;6(3):593–603. doi: 10.1016/s1097-2765(00)00058-7. [DOI] [PubMed] [Google Scholar]
  8. Detloff P., Petes T. D. Measurements of excision repair tracts formed during meiotic recombination in Saccharomyces cerevisiae. Mol Cell Biol. 1992 Apr;12(4):1805–1814. doi: 10.1128/mcb.12.4.1805. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Detloff P., White M. A., Petes T. D. Analysis of a gene conversion gradient at the HIS4 locus in Saccharomyces cerevisiae. Genetics. 1992 Sep;132(1):113–123. doi: 10.1093/genetics/132.1.113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Fabre F., Boulet A., Faye G. Possible involvement of the yeast POLIII DNA polymerase in induced gene conversion. Mol Gen Genet. 1991 Oct;229(3):353–356. doi: 10.1007/BF00267455. [DOI] [PubMed] [Google Scholar]
  11. Fan Q., Xu F., Petes T. D. Meiosis-specific double-strand DNA breaks at the HIS4 recombination hot spot in the yeast Saccharomyces cerevisiae: control in cis and trans. Mol Cell Biol. 1995 Mar;15(3):1679–1688. doi: 10.1128/mcb.15.3.1679. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Giot L., Chanet R., Simon M., Facca C., Faye G. Involvement of the yeast DNA polymerase delta in DNA repair in vivo. Genetics. 1997 Aug;146(4):1239–1251. doi: 10.1093/genetics/146.4.1239. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hindges R., Hübscher U. DNA polymerase delta, an essential enzyme for DNA transactions. Biol Chem. 1997 May;378(5):345–362. doi: 10.1515/bchm.1997.378.5.345. [DOI] [PubMed] [Google Scholar]
  14. Holmes A. M., Haber J. E. Double-strand break repair in yeast requires both leading and lagging strand DNA polymerases. Cell. 1999 Feb 5;96(3):415–424. doi: 10.1016/s0092-8674(00)80554-1. [DOI] [PubMed] [Google Scholar]
  15. Hunter N., Kleckner N. The single-end invasion: an asymmetric intermediate at the double-strand break to double-holliday junction transition of meiotic recombination. Cell. 2001 Jul 13;106(1):59–70. doi: 10.1016/s0092-8674(01)00430-5. [DOI] [PubMed] [Google Scholar]
  16. Kuzminov A. DNA replication meets genetic exchange: chromosomal damage and its repair by homologous recombination. Proc Natl Acad Sci U S A. 2001 Jul 17;98(15):8461–8468. doi: 10.1073/pnas.151260698. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Merker Jason D., Dominska Margaret, Petes Thomas D. Patterns of heteroduplex formation associated with the initiation of meiotic recombination in the yeast Saccharomyces cerevisiae. Genetics. 2003 Sep;165(1):47–63. doi: 10.1093/genetics/165.1.47. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Nag D. K., White M. A., Petes T. D. Palindromic sequences in heteroduplex DNA inhibit mismatch repair in yeast. Nature. 1989 Jul 27;340(6231):318–320. doi: 10.1038/340318a0. [DOI] [PubMed] [Google Scholar]
  19. Novak J. E., Ross-Macdonald P. B., Roeder G. S. The budding yeast Msh4 protein functions in chromosome synapsis and the regulation of crossover distribution. Genetics. 2001 Jul;158(3):1013–1025. doi: 10.1093/genetics/158.3.1013. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Papazian H P. The Analysis of Tetrad Data. Genetics. 1952 Mar;37(2):175–188. doi: 10.1093/genetics/37.2.175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Pâques F., Haber J. E. Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol Mol Biol Rev. 1999 Jun;63(2):349–404. doi: 10.1128/mmbr.63.2.349-404.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Rockmill B., Lambie E. J., Roeder G. S. Spore enrichment. Methods Enzymol. 1991;194:146–149. doi: 10.1016/0076-6879(91)94012-2. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. Rothstein R. Targeting, disruption, replacement, and allele rescue: integrative DNA transformation in yeast. Methods Enzymol. 1991;194:281–301. doi: 10.1016/0076-6879(91)94022-5. [DOI] [PubMed] [Google Scholar]
  25. Snow R. Maximum likelihood estimation of linkage and interference from tetrad data. Genetics. 1979 May;92(1):231–245. doi: 10.1093/genetics/92.1.231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. 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]
  27. 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]
  28. Sym M., Roeder G. S. Crossover interference is abolished in the absence of a synaptonemal complex protein. Cell. 1994 Oct 21;79(2):283–292. doi: 10.1016/0092-8674(94)90197-x. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. de los Santos Teresa, Hunter Neil, Lee Cindy, Larkin Brittany, Loidl Josef, Hollingsworth Nancy M. The Mus81/Mms4 endonuclease acts independently of double-Holliday junction resolution to promote a distinct subset of crossovers during meiosis in budding yeast. Genetics. 2003 May;164(1):81–94. doi: 10.1093/genetics/164.1.81. [DOI] [PMC free article] [PubMed] [Google Scholar]

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