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. 1997 Aug;146(4):1221–1238. doi: 10.1093/genetics/146.4.1221

A Recombinationally Repressed Region between Mat2 and Mat3 Loci Shares Homology to Centromeric Repeats and Regulates Directionality of Mating-Type Switching in Fission Yeast

SIS Grewal 1, AJS Klar 1
PMCID: PMC1208070  PMID: 9258669

Abstract

Cells of the fission yeast Schizosaccharomyces pombe switch mating type by replacing genetic information at the transcriptionally active mat1 locus with sequences copied from one of two closely linked silent loci, mat2-P or mat3-M. By a process referred to as directionality of switching, cells predominantly switch to the opposite mat1 allele; the mat1-P allele preferentially recombines with mat3, while mat1-M selects the mat2. In contrast to efficient recombination at mat1, recombination within the adjoining mat2-mat3 interval is undetectable. We defined the role of sequences between mat2 and mat3, designated the K-region, in directionality as well as recombinational suppression. Cloning and sequencing analysis revealed that a part of the K-region is homologous to repeat sequences present at centromeres, which also display transcriptional and recombinational suppression. Replacement of 7.5 kb of the K-region with the ura4(+) gene affected directionality in a variegated manner. Analysis of the swi6-mod locus, which was previously shown to affect directionality, in KΔ::ura4(+) strains suggested the existence of at least two overlapping directionality mechanisms. Our work furthers the model that directionality is regulated by cell-type-specific organization of the heterochromatin-like structure in the mating-type region and provides evidence that the K-region contributes to silencing of the mat2-mat3 interval.

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Selected References

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  1. 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]
  2. Bell S. P., Kobayashi R., Stillman B. Yeast origin recognition complex functions in transcription silencing and DNA replication. Science. 1993 Dec 17;262(5141):1844–1849. doi: 10.1126/science.8266072. [DOI] [PubMed] [Google Scholar]
  3. Bresch C., Müller G., Egel R. Genes involved in meiosis and sporulation of a yeast. Mol Gen Genet. 1968;102(4):301–306. doi: 10.1007/BF00433721. [DOI] [PubMed] [Google Scholar]
  4. Chikashige Y., Kinoshita N., Nakaseko Y., Matsumoto T., Murakami S., Niwa O., Yanagida M. Composite motifs and repeat symmetry in S. pombe centromeres: direct analysis by integration of NotI restriction sites. Cell. 1989 Jun 2;57(5):739–751. doi: 10.1016/0092-8674(89)90789-7. [DOI] [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. Ekwall K., Javerzat J. P., Lorentz A., Schmidt H., Cranston G., Allshire R. The chromodomain protein Swi6: a key component at fission yeast centromeres. Science. 1995 Sep 8;269(5229):1429–1431. doi: 10.1126/science.7660126. [DOI] [PubMed] [Google Scholar]
  7. Ekwall K., Ruusala T. Mutations in rik1, clr2, clr3 and clr4 genes asymmetrically derepress the silent mating-type loci in fission yeast. Genetics. 1994 Jan;136(1):53–64. doi: 10.1093/genetics/136.1.53. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Ferris P. J., Goodenough U. W. The mating-type locus of Chlamydomonas reinhardtii contains highly rearranged DNA sequences. Cell. 1994 Mar 25;76(6):1135–1145. doi: 10.1016/0092-8674(94)90389-1. [DOI] [PubMed] [Google Scholar]
  9. Foss M., McNally F. J., Laurenson P., Rine J. Origin recognition complex (ORC) in transcriptional silencing and DNA replication in S. cerevisiae. Science. 1993 Dec 17;262(5141):1838–1844. doi: 10.1126/science.8266071. [DOI] [PubMed] [Google Scholar]
  10. Funabiki H., Hagan I., Uzawa S., Yanagida M. Cell cycle-dependent specific positioning and clustering of centromeres and telomeres in fission yeast. J Cell Biol. 1993 Jun;121(5):961–976. doi: 10.1083/jcb.121.5.961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Goldman A. S., Lichten M. The efficiency of meiotic recombination between dispersed sequences in Saccharomyces cerevisiae depends upon their chromosomal location. Genetics. 1996 Sep;144(1):43–55. doi: 10.1093/genetics/144.1.43. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Haber J. E. Mating-type gene switching in Saccharomyces cerevisiae. Trends Genet. 1992 Dec;8(12):446–452. doi: 10.1016/0168-9525(92)90329-3. [DOI] [PubMed] [Google Scholar]
  14. Hoheisel J. D., Maier E., Mott R., McCarthy L., Grigoriev A. V., Schalkwyk L. C., Nizetic D., Francis F., Lehrach H. High resolution cosmid and P1 maps spanning the 14 Mb genome of the fission yeast S. pombe. Cell. 1993 Apr 9;73(1):109–120. doi: 10.1016/0092-8674(93)90164-l. [DOI] [PubMed] [Google Scholar]
  15. Kaiser P. Pericentric inversions. Problems and significance for clinical genetics. Hum Genet. 1984;68(1):1–47. doi: 10.1007/BF00293869. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. Klar A. J., Bonaduce M. J. swi6, a gene required for mating-type switching, prohibits meiotic recombination in the mat2-mat3 "cold spot" of fission yeast. Genetics. 1991 Dec;129(4):1033–1042. doi: 10.1093/genetics/129.4.1033. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Klar A. J., Hicks J. B., Strathern J. N. Directionality of yeast mating-type interconversion. Cell. 1982 Mar;28(3):551–561. doi: 10.1016/0092-8674(82)90210-0. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. Kupiec M., Petes T. D. Allelic and ectopic recombination between Ty elements in yeast. Genetics. 1988 Jul;119(3):549–559. doi: 10.1093/genetics/119.3.549. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lewis S. M. The mechanism of V(D)J joining: lessons from molecular, immunological, and comparative analyses. Adv Immunol. 1994;56:27–150. doi: 10.1016/s0065-2776(08)60450-2. [DOI] [PubMed] [Google Scholar]
  22. Maier E., Hoheisel J. D., McCarthy L., Mott R., Grigoriev A. V., Monaco A. P., Larin Z., Lehrach H. Complete coverage of the Schizosaccharomyces pombe genome in yeast artificial chromosomes. Nat Genet. 1992 Jul;1(4):273–277. doi: 10.1038/ng0792-273. [DOI] [PubMed] [Google Scholar]
  23. Maundrell K., Hutchison A., Shall S. Sequence analysis of ARS elements in fission yeast. EMBO J. 1988 Jul;7(7):2203–2209. doi: 10.1002/j.1460-2075.1988.tb03059.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Micklem G., Rowley A., Harwood J., Nasmyth K., Diffley J. F. Yeast origin recognition complex is involved in DNA replication and transcriptional silencing. Nature. 1993 Nov 4;366(6450):87–89. doi: 10.1038/366087a0. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. Nakaseko Y., Adachi Y., Funahashi S., Niwa O., Yanagida M. Chromosome walking shows a highly homologous repetitive sequence present in all the centromere regions of fission yeast. EMBO J. 1986 May;5(5):1011–1021. doi: 10.1002/j.1460-2075.1986.tb04316.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Nakaseko Y., Kinoshita N., Yanagida M. A novel sequence common to the centromere regions of Schizosaccharomyces pombe chromosomes. Nucleic Acids Res. 1987 Jun 25;15(12):4705–4715. doi: 10.1093/nar/15.12.4705. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Olsson T., Ekwall K., Ruusala T. The silent P mating type locus in fission yeast contains two autonomously replicating sequences. Nucleic Acids Res. 1993 Feb 25;21(4):855–861. doi: 10.1093/nar/21.4.855. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. 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]
  30. Ruusala T. The mating type in fission yeast is switched independently of its expression. Curr Genet. 1991 Nov;20(5):379–383. doi: 10.1007/BF00317065. [DOI] [PubMed] [Google Scholar]
  31. SanMiguel P., Tikhonov A., Jin Y. K., Motchoulskaia N., Zakharov D., Melake-Berhan A., Springer P. S., Edwards K. J., Lee M., Avramova Z. Nested retrotransposons in the intergenic regions of the maize genome. Science. 1996 Nov 1;274(5288):765–768. doi: 10.1126/science.274.5288.765. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. Singh P. B. Molecular mechanisms of cellular determination: their relation to chromatin structure and parental imprinting. J Cell Sci. 1994 Oct;107(Pt 10):2653–2668. doi: 10.1242/jcs.107.10.2653. [DOI] [PubMed] [Google Scholar]
  34. Stanhope-Baker P., Hudson K. M., Shaffer A. L., Constantinescu A., Schlissel M. S. Cell type-specific chromatin structure determines the targeting of V(D)J recombinase activity in vitro. Cell. 1996 Jun 14;85(6):887–897. doi: 10.1016/s0092-8674(00)81272-6. [DOI] [PubMed] [Google Scholar]
  35. Steiner N. C., Clarke L. A novel epigenetic effect can alter centromere function in fission yeast. Cell. 1994 Dec 2;79(5):865–874. doi: 10.1016/0092-8674(94)90075-2. [DOI] [PubMed] [Google Scholar]
  36. Steiner N. C., Hahnenberger K. M., Clarke L. Centromeres of the fission yeast Schizosaccharomyces pombe are highly variable genetic loci. Mol Cell Biol. 1993 Aug;13(8):4578–4587. doi: 10.1128/mcb.13.8.4578. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Thon G., Klar A. J. The clr1 locus regulates the expression of the cryptic mating-type loci of fission yeast. Genetics. 1992 Jun;131(2):287–296. doi: 10.1093/genetics/131.2.287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Wu X., Haber J. E. A 700 bp cis-acting region controls mating-type dependent recombination along the entire left arm of yeast chromosome III. Cell. 1996 Oct 18;87(2):277–285. doi: 10.1016/s0092-8674(00)81345-8. [DOI] [PubMed] [Google Scholar]

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