A site- and strand-specific DNA break confers asymmetric switching potential in fission yeast (original) (raw)

Abstract

Mating-type switching in the fission yeast Schizosaccharomyces pombe results in the transfer of genetic information from one of the two silent cassettes (mat2P or mat3M) to the transcriptionally active locus (mat1). The switching pattern is programmed by an imprinting event which restricts mat1 gene conversion to only one of the two sister cells, leading to asymmetric cell division. Biochemical analysis indicated that the mat1 locus contains a fragile chromosomal site. Southern hybridization and primer extension experiments showed that the fragility consists of a single-strand break (SSB). The nicked DNA is stable throughout the cell cycle. The features of the nick fulfil all the requirements for the 'epigenetic', site and strand-specific chromosome modification at the mat1 locus, providing strong evidence that an SSB can initiate mitotic and meiotic gene conversion during replication.

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Selected References

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  1. Arcangioli B., Klar A. J. A novel switch-activating site (SAS1) and its cognate binding factor (SAP1) required for efficient mat1 switching in Schizosaccharomyces pombe. EMBO J. 1991 Oct;10(10):3025–3032. doi: 10.1002/j.1460-2075.1991.tb07853.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Aves S. J., Durkacz B. W., Carr A., Nurse P. Cloning, sequencing and transcriptional control of the Schizosaccharomyces pombe cdc10 'start' gene. EMBO J. 1985 Feb;4(2):457–463. doi: 10.1002/j.1460-2075.1985.tb03651.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Baum M., Ngan V. K., Clarke L. The centromeric K-type repeat and the central core are together sufficient to establish a functional Schizosaccharomyces pombe centromere. Mol Biol Cell. 1994 Jul;5(7):747–761. doi: 10.1091/mbc.5.7.747. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Beach D. H., Klar A. J. Rearrangements of the transposable mating-type cassettes of fission yeast. EMBO J. 1984 Mar;3(3):603–610. doi: 10.1002/j.1460-2075.1984.tb01855.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Egel R., Beach D. H., Klar A. J. Genes required for initiation and resolution steps of mating-type switching in fission yeast. Proc Natl Acad Sci U S A. 1984 Jun;81(11):3481–3485. doi: 10.1073/pnas.81.11.3481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Grewal S. I., Klar A. J. A recombinationally repressed region between mat2 and mat3 loci shares homology to centromeric repeats and regulates directionality of mating-type switching in fission yeast. Genetics. 1997 Aug;146(4):1221–1238. doi: 10.1093/genetics/146.4.1221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Grewal S. I., Klar A. J. Chromosomal inheritance of epigenetic states in fission yeast during mitosis and meiosis. Cell. 1996 Jul 12;86(1):95–101. doi: 10.1016/s0092-8674(00)80080-x. [DOI] [PubMed] [Google Scholar]
  8. Kelly M., Burke J., Smith M., Klar A., Beach D. Four mating-type genes control sexual differentiation in the fission yeast. EMBO J. 1988 May;7(5):1537–1547. doi: 10.1002/j.1460-2075.1988.tb02973.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Klar A. J., Bonaduce M. J., Cafferkey R. The mechanism of fission yeast mating type interconversion: seal/replicate/cleave model of replication across the double-stranded break site at mat1. Genetics. 1991 Mar;127(3):489–496. doi: 10.1093/genetics/127.3.489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Klar A. J. Differentiated parental DNA strands confer developmental asymmetry on daughter cells in fission yeast. Nature. 1987 Apr 2;326(6112):466–470. doi: 10.1038/326466a0. [DOI] [PubMed] [Google Scholar]
  11. Klar A. J., Miglio L. M. Initiation of meiotic recombination by double-strand DNA breaks in S. pombe. Cell. 1986 Aug 29;46(5):725–731. doi: 10.1016/0092-8674(86)90348-x. [DOI] [PubMed] [Google Scholar]
  12. Klar A. J., Strathern J. N., Abraham J. A. Involvement of double-strand chromosomal breaks for mating-type switching in Saccharomyces cerevisiae. Cold Spring Harb Symp Quant Biol. 1984;49:77–88. doi: 10.1101/sqb.1984.049.01.011. [DOI] [PubMed] [Google Scholar]
  13. Klar A. J. The developmental fate of fission yeast cells is determined by the pattern of inheritance of parental and grandparental DNA strands. EMBO J. 1990 May;9(5):1407–1415. doi: 10.1002/j.1460-2075.1990.tb08256.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Moreno S., Klar A., Nurse P. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 1991;194:795–823. doi: 10.1016/0076-6879(91)94059-l. [DOI] [PubMed] [Google Scholar]
  15. Nasmyth K. Molecular analysis of a cell lineage. Nature. 1983 Apr 21;302(5910):670–676. doi: 10.1038/302670a0. [DOI] [PubMed] [Google Scholar]
  16. Nielsen O., Egel R. Mapping the double-strand breaks at the mating-type locus in fission yeast by genomic sequencing. EMBO J. 1989 Jan;8(1):269–276. doi: 10.1002/j.1460-2075.1989.tb03373.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Russell P., Nurse P. cdc25+ functions as an inducer in the mitotic control of fission yeast. Cell. 1986 Apr 11;45(1):145–153. doi: 10.1016/0092-8674(86)90546-5. [DOI] [PubMed] [Google Scholar]
  18. Schwartz D. C., Cantor C. R. Separation of yeast chromosome-sized DNAs by pulsed field gradient gel electrophoresis. Cell. 1984 May;37(1):67–75. doi: 10.1016/0092-8674(84)90301-5. [DOI] [PubMed] [Google Scholar]
  19. Singh J., Klar A. J. DNA polymerase-alpha is essential for mating-type switching in fission yeast. Nature. 1993 Jan 21;361(6409):271–273. doi: 10.1038/361271a0. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. Styrkársdóttir U., Egel R., Nielsen O. The smt-0 mutation which abolishes mating-type switching in fission yeast is a deletion. Curr Genet. 1993 Feb;23(2):184–186. doi: 10.1007/BF00352020. [DOI] [PubMed] [Google Scholar]
  22. Sutherland G. R., Richards R. I. The molecular basis of fragile sites in human chromosomes. Curr Opin Genet Dev. 1995 Jun;5(3):323–327. doi: 10.1016/0959-437x(95)80046-8. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. Thon G., Friis T. Epigenetic inheritance of transcriptional silencing and switching competence in fission yeast. Genetics. 1997 Mar;145(3):685–696. doi: 10.1093/genetics/145.3.685. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Thon G., Klar A. J. Directionality of fission yeast mating-type interconversion is controlled by the location of the donor loci. Genetics. 1993 Aug;134(4):1045–1054. doi: 10.1093/genetics/134.4.1045. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Waseem N. H., Labib K., Nurse P., Lane D. P. Isolation and analysis of the fission yeast gene encoding polymerase delta accessory protein PCNA. EMBO J. 1992 Dec;11(13):5111–5120. doi: 10.1002/j.1460-2075.1992.tb05618.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Zou H., Rothstein R. Holliday junctions accumulate in replication mutants via a RecA homolog-independent mechanism. Cell. 1997 Jul 11;90(1):87–96. doi: 10.1016/s0092-8674(00)80316-5. [DOI] [PubMed] [Google Scholar]