Mating-Type Cassettes: Structure, Switching and Silencing

  • Benoit Arcangioli
  • Geneviève Thon


From a single haploid P (plus) or M (minus) cell, S. pombe is able to produce a population of haploids containing both mating types in nearly equal proportions. This ability is widespread among fungi, the presence of both mating types permitting the formation of diploids and eventually spores. Single-cell lineage approaches have revealed the asymmetry and rules of mating-type switching in S. pombe. Genetic and biochemical analyses have identified the organization of the mating-type loci and a number of genes required for the process of switching. They have yielded insights into the molecular mechanism of the switch and into two processes of epigenetic inheritance. The first process exploits the intrinsic asymmetry of DNA synthesis to restrain a gene conversion event to one of two sister chromatids. The second allows the formation and maintenance of a silent chromatin state. The interplay of both epigenetic events provides a striking example of dynamic chromatin choreography allowing progression into the S. pombe developmental program.


Gene Conversion Fission Yeast Schizosaccharomyces Pombe Gene Conversion Event Switching Potential 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Arcangioli B (1998) A site-and strand-specific DNA break confers asymmetric switching potential in fission yeast. EMBO J 17: 4503–4510PubMedCrossRefGoogle Scholar
  2. Arcangioli B (2000) Fate of mati DNA strands during mating-type switching in fission yeast. EMBO Rep 1: 145–150PubMedCrossRefGoogle Scholar
  3. Arcangioli B, Klar AJS (1991) A novel switch-activating site (SAS1) and its cognate binding factor (Sapl) required for efficient matt switching in Schizosaccharomyces pombe. EMBO J 10: 3025–3032PubMedGoogle Scholar
  4. Arcangioli B, de Lahondes R (2000) Fission yeast switches mating-type by a replication-recombination coupled process. EMBO J 19: 1389–1396PubMedCrossRefGoogle Scholar
  5. Arcangioli B, Copeland TD, Klar AJ (1994) Sapl, a protein that binds to sequences required for mating-type switching, is essential for viability in Schizosaccharomyces pombe. Mol Cell Biol 14: 2058–2065PubMedGoogle Scholar
  6. Ayoub N, Goldshmidt I, Cohen A (1999) Position effect variegation at the mating-type locus of fission yeast: a cis-acting element inhibits covariegated expression of genes in the silent and expressed domains. Genetics 152: 495–508PubMedGoogle Scholar
  7. Ayoub N, Goldshmidt I, Lyakhovetsky R, Cohen A (2000) A fission yeast repression element cooperates with centromere-like sequences and defines a mat silent domain boundary. Genetics 156: 983–994PubMedGoogle Scholar
  8. Bannister AJ, Zegerman P, Partridge JF et al. (2001) Selective recognition of methylated lysine 9 on histone H3 by the HPI chromo domain. Nature 410: 120–124PubMedCrossRefGoogle Scholar
  9. Beach DH (1983) Cell type switching by DNA transposition in fission yeast. Nature 305: 682–688CrossRefGoogle Scholar
  10. Beach D, Klar AJ (1984) Rearrangements of the transposable mating-type cassettes of fission yeast. EMBO J 3: 603–610PubMedGoogle Scholar
  11. Beach D, Nurse P, Egel R (1982) Molecular rearrangement of mating-type genes in fission yeast. Nature 296: 682–683PubMedCrossRefGoogle Scholar
  12. Belling J (1933) Crossing over and gene rearrangement in flowering plants. Genetics 18: 388–413PubMedGoogle Scholar
  13. Bjerling P (1998) Positional silencing in the mating-type region of Schizosaccharomyces pombe. PhD Thesis, University of CopenhagenGoogle Scholar
  14. Borgstrom B (1995) Characterization of the Schizosaccharomyces pombe rikl gene. PhD thesis, University of CopenhagenGoogle Scholar
  15. Carr AM (1994) Radiation checkpoints in model systems. Int J Radiat Biol 66: 133–139CrossRefGoogle Scholar
  16. Dalgaard JZ, Klar AJ (1999). Orientation of DNA replication establishes mating-type switching pattern in S. pombe. Nature 400: 181–184PubMedCrossRefGoogle Scholar
  17. Dalgaard JZ, Klar AJ (2000) Swil and Swi3 perform imprinting, pausing and termination of DNA replication in S. pombe. Cell 102: 745–751PubMedCrossRefGoogle Scholar
  18. Dalgaard JZ, Klar AJ (2001) A DNA replication-arrest site RTS1 regulates imprinting by determining the direction of replication at mati in S. pombe. Genes Dev 15: 2060–2068PubMedCrossRefGoogle Scholar
  19. Egel R (1977) Frequency of mating-type switching in homothallic fission yeast. Nature 266: 172–174PubMedCrossRefGoogle Scholar
  20. Egel R (1984) The pedigree pattern of mating-type switching in Schizosaccharomyces pombe. Curr Genet 8: 205–210CrossRefGoogle Scholar
  21. Egel R (1989) Mating-type genes, meiosis and sporulation. In: Nasim A, Young P, Johnson BF (eds) Molecular biology of the fission yeast. Academic Press, San Diego, pp 31–73CrossRefGoogle Scholar
  22. Egel R, Eie B (1987) Cell lineage asymmetry in Schizosaccharomyces pombe: unilateral transmission of a high-frequency state for mating-type switching in diploid pedigrees. Curr Genet 12: 429–433CrossRefGoogle Scholar
  23. Egel R, Gutz H (1981) Gene activation by copy transposition in mating-type switching of a homothallic fission yeast. Curr Genet 12: 5–12CrossRefGoogle Scholar
  24. Egel R, Beach DH, Klar AJ (1984) Genes required for initiation and resolution steps of mating-type switching in fission yeast. Proc Natl Acad Sci USA 81: 3481–3485PubMedCrossRefGoogle Scholar
  25. Egel R, Willer M, Nielsen O (1989) Unblocking of meiotic crossing-over between the silent mating-type cassettes of fission yeast, conditioned by the recessive, pleiotropic mutant rikl. Curr Genet 15: 407–410CrossRefGoogle Scholar
  26. Ekwall K, Ruusala T (1994) Mutations in rikl, clr2, clr3 and clr4 genes asymmetrically derepress the silent mating-type loci in fission yeast. Genetics 136: 53–64PubMedGoogle Scholar
  27. Ekwall K, Javerzat JP, Lorentz A et al. (1995) The chromodomain protein Swi6: a key component at fission yeast centromeres. Science 269: 1429–1431PubMedCrossRefGoogle Scholar
  28. Ekwall K, Nimmo ER, Javerzat JP et al. (1996) Mutations in the fission yeast silencing factors are and rikl + disrupt the localisation of the chromo domain protein Swi6p and impair centromere function. J Cell Sci 109: 2637–2648PubMedGoogle Scholar
  29. Engelke U, Grabowski L, Gutz H et al. (1987) Molecular characterization of h-mutants of Schizosaccharomyces pombe. Curr Genet 18: 535–540CrossRefGoogle Scholar
  30. Foss EJ (2001) Toflp regulates DNA damage responses during S phase in Saccharomyces cerevisiae. Genetics 157: 567–577PubMedGoogle Scholar
  31. Ghazvini M, Ribes V, Arcangioli B (1995) The essential DNA-binding protein Sapl of Schizosaccharomyces pombe contains two independent oligomerization interfaces that dictate the relative orientation of the DNA-binding domain. Mol Cell Biol 15: 4939–4946PubMedGoogle Scholar
  32. Grewal SI, Klar AJ (1996) Chromosomal inheritance of epigenetic states in fission yeast during mitosis and meiosis. Cell 86: 95–101PubMedCrossRefGoogle Scholar
  33. Grewal SI, Klar AJ (1997) 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 146: 1221–1238PubMedGoogle Scholar
  34. Grewal SI, Bonaduce MJ, Klar AJ (1998) Histone deacetylase homologs regulate epigenetic inheritance of transcriptional silencing and chromosome segregation in fission yeast. Genetics 150: 563–576PubMedGoogle Scholar
  35. Gutz H, Schmidt H (1985) Switching genes in Schizosaccharomyces pombe. Curr Genet 9: 325–331CrossRefGoogle Scholar
  36. Halverson D, Gutkin G, Clarke L (2000) A novel member of the Swi6p family of fission yeast chromo domain-containing proteins associates with the centromere in vivo and affects chromosome segregation. Mol Gen Genet 264: 492–505PubMedCrossRefGoogle Scholar
  37. Ivanova AV, Bonaduce MJ, Ivanov SV, Klar AJ (1996) The chromo and SET domains of the C1r4 protein are essential for silencing in fission yeast. Nat Genet 19: 192–195CrossRefGoogle Scholar
  38. Kelly M, Burke J, Smith M et al. (1988) Four mating-type genes control sexual differenciation in the fission yeast. EMBO J 7: 1537–1547PubMedGoogle Scholar
  39. Kim WJ, Lee S, Park MS et al. (2000) Rad22 protein, a Rad52 homologue in Schizosaccharomyces pombe, binds to DNA double-strand breaks. J Biol Chem 275: 35607–35611PubMedCrossRefGoogle Scholar
  40. Klar AJ (1987) Differential parental DNA strands confer developmental asymmetry on daughter cells in fission yeast. Nature 326: 466–470PubMedCrossRefGoogle Scholar
  41. Klar AJ (1990) The developmental fate of fission yeast cells is determined by the pattern of inheritance of parental and grandparental DNA strands. EMBO J 9: 1407–1415PubMedGoogle Scholar
  42. Klar AJ (1992) Molecular genetics of fission yeast cell type: mating type and mating-type interconversion. In: Jones EW, Pringle JR, Broach JR (eds) The molecular and cellular biology of the yeast Saccharomyces - gene expression. CSH Laboratory Press, Cold Spring Harbor, pp 745–777Google Scholar
  43. Klar AJ, Miglio LM (1986) Initiation of meiotic recombination by double-strand DNA breaks in Schizosaccharomyces pombe. Cell 46: 725–731PubMedCrossRefGoogle Scholar
  44. Klar AJ, Bonaduce MJ, Cafferkey R (1991) The mechanism of fission yeast mating-type interconversion: seal/replicate/cleave model of replication across the double-stranded break site at mati. Genetics 127: 489–495PubMedGoogle Scholar
  45. Lachner M, O’Carroll D, Rea S et al. (2001) Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410: 116–20PubMedCrossRefGoogle Scholar
  46. Leupold U (1950) Die Vererbung von Homothallie und Heterothallie bei Schizosaccharomyces pombe. CR Lab Carlsberg Ser Physiol. 24: 381–480Google Scholar
  47. Leupold U (1955) Methodisches zur Genetik von Schizosaccharomyces pombe. Schweiz Z Allg Pathol Bakteriol 18: 161–170Google Scholar
  48. Lorentz A, Heim L, Schmidt H (1992) The switching gene swi6 affects recombination and gene expression in the mating-type region of Schizosaccharomyces pombe. Mol Gen Genet 233: 436–442PubMedCrossRefGoogle Scholar
  49. Lorentz A, Ostermann K, Fleck O, Schmidt H (1994) Switching gene swi6, involved in repression of silent mating-type loci in fission yeast, encodes a homologue of chromatin-associated proteins from Drosophila and mammals. Gene 143: 139–143PubMedCrossRefGoogle Scholar
  50. Meselson M, Stahl FW (1958) The replication of DNA in Escherichia coli. Proc Natl Acad Sci USA 4: 671–682CrossRefGoogle Scholar
  51. Miyata H, Miyata M (1981) Mode of conjugation in homothallic cells of Schizosaccharomyces pombe. J Gen Appl Microbiol 27: 365–369CrossRefGoogle Scholar
  52. Nakayama J, Rice JC, Strahl BD et al. (2001) Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science 292: 110–113PubMedCrossRefGoogle Scholar
  53. Nakayama J, Allshire R, Klar AS, Grewal SI (2001) A role for DNA polymerase a in epigenetic control of transcriptional silencing in fission yeast. EMBO J 20: 2857–2866CrossRefGoogle Scholar
  54. Nielsen O, Egel R (1989). Mapping of the double-strand breaks at the mating-type locus in fission yeast by genomic sequencing. EMBO J 8: 269–276PubMedGoogle Scholar
  55. Nielsen IS, Nielsen O, Murray JO, Thon G (2002) The fission yeast ubiquitin-conjugating enzymes UbcP3, Ubc15, and Rhp6 affect transcriptional silencing of the mating-type region. Eukaryotic Cell 1: 613–625PubMedCrossRefGoogle Scholar
  56. Noma K, Allis CD, Grewal SI (2001) Transitions in distinct histone H3 methylation patterns at the heterochromatin domain boundaries. Science 293: 1150–1155PubMedCrossRefGoogle Scholar
  57. Ostermann K, Lorentz A, Schmidt H (1993) The fission yeast rad22 gene, having a function in mating-type switching and repair of DNA damages, encodes a protein homolog to Rad52 of S. cerevisiae. Nucleic Acids Res 21: 5940–5944PubMedCrossRefGoogle Scholar
  58. Paques F, Haber JE (1997) Two pathways for removal of nonhomologous DNA ends during double-strand break repair in Saccharomyces cerevisiae. Mol Cell Biol 17: 6765–6771PubMedGoogle Scholar
  59. Park H, Sternglanz R (1999) Identification and characterization of the genes for two topoisomerase I-interacting proteins from Saccharomyces cerevisiae. Yeast 15: 35–41PubMedCrossRefGoogle Scholar
  60. Rea S, Eisenhaber F, O’Carroll D et al. (2000) Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406: 593–599PubMedCrossRefGoogle Scholar
  61. Rodel C, Jupitz T, Schmidt H (1997) Complementation of the DNA repair-deficient swi10 mutant of fission yeast by the human ERCC1 gene. Nucleic Acids Res 25: 2823–2827PubMedCrossRefGoogle Scholar
  62. Rudolph C, Fleck 0, Kohli J (1998) Schizosaccharomyces pombe exol is involved in the same mismatch repair pathway as msh2 and pmsl. Curr Genet 34: 343–350Google Scholar
  63. Schmidt H, Kapitza P, Gutz H (1987) Switching genes in Schizosaccharomyces pombe: Their influence on cell viability and recombination. Curr Genet 11: 303–308Google Scholar
  64. Singh J, Klar AJ (1993) DNA polymerase a is essential for mating-type switching in fission yeast. Nature 361: 271–276PubMedCrossRefGoogle Scholar
  65. Strathern JN, Klar AJ, Hicks JB et al. (1982) Homothallic switching of yeast mating type cassettes is initiated by a double-stranded cut in the MAT locus. Cell 31: 183–192PubMedCrossRefGoogle Scholar
  66. Styrkarsdottir U, Egel R, Nielsen 0 (1993) The smt-0 mutation which abolishes mating-type switching in fission yeast is a deletion. Curr Genet 23: 184–186Google Scholar
  67. Thon G, Friis T (1997) Epigenetic inheritance of transcriptional silencing and switching competence in fission yeast. Genetics 145: 685–696PubMedGoogle Scholar
  68. Thon G, Klar AJ (1992) The clri locus regulates the expression of the cryptic mating-type loci of fission yeast. Genetics 131: 287–296PubMedGoogle Scholar
  69. Thon G, Klar AJ (1993) Directionality of fission yeast mating-type interconversion is controlled by the location of the donor loci. Genetics 134: 1045–1054PubMedGoogle Scholar
  70. Thon G, Verhein-Hansen J (2000) Four chromo-domain proteins of Schizosaccharomyces pombe differentially repress transcription at various chromosomal locations. Genetics 155: 551–568PubMedGoogle Scholar
  71. Thon G, Cohen A, Klar AJ (1994) Three additional linkage groups that repress transcription and meiotic recombination in the mating-type region of Schizosaccharomyces pombe. Genetics 138: 29–38PubMedGoogle Scholar
  72. Thon G, Bjerling KP, Nielsen IS (1999) Localization and properties of a silencing element near the mat3-M mating-type cassette of Schizosaccharomyces pombe. Genetics 151: 945–963PubMedGoogle Scholar
  73. Thon G, Bjerling KP, Bünner CM, Verhein-Hansen J (2002) Expression-state boundaries in the mating-type region of fission yeast. Genetics 161: 611–622PubMedGoogle Scholar
  74. Tornier C, Bessone S, Varlet I et al. (2001) Requirement for Msh6, but not for Swi4 (Msh3), in Msh2-dependent repair of base-base mismatches and mononucleotide loops in Schizo-saccharomyces pombe. Genetics 158: 65–75Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2004

Authors and Affiliations

  • Benoit Arcangioli
  • Geneviève Thon

There are no affiliations available

Personalised recommendations