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Chapter 9 : Decisions, Decisions: Donor Preference during Budding Yeast Mating-Type Switching

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Decisions, Decisions: Donor Preference during Budding Yeast Mating-Type Switching, Page 1 of 2

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Abstract:

Mating-type (MAT) switching in the budding yeast has been particularly well studied, both in terms of the homologous recombination mechanism that leads to the switch itself and the remarkable donor preference system that ensures efficient exchange of mating types. For example, mutations that prevent acetylation of four lysines in histone H4 lead to the complete unsilencing of HMLa but have much less effect on the silencing of HMRa. MAT switching occurs by a mechanism of DSB repair known as synthesis-dependent strand annealing (SDSA). There are a number of distinct, slow steps in MAT switching that have been identified by a combination of Southern blot and PCR analyses, as well as by chromatin immunoprecipitation techniques, that monitor the recruitment of recombination proteins to the sequences undergoing recombination/repair. Analysis of various temperature-sensitive mutations in essential DNA replication genes has shown that the short patch of new DNA synthesis in MAT switching does not require the Mcm helicase proteins or Pol-primase or the Cdc7 kinase. The binding of both Fkh1 and Swi4/6 to recombination enhancer (RE) has been evaluated by chromatin immunoprecipitation at different times in the cell cycle. RE represents one of the most fascinating and best-defined -acting loci that control aspects of chromosome positioning, folding, or tethering. The availability of new cytological resources as well as a wide variety of molecular and genetic tools opens the way to a detailed understanding of the ways chromosomes are arranged and constrained in the nucleus.

Citation: Haber J. 2007. Decisions, Decisions: Donor Preference during Budding Yeast Mating-Type Switching, p 159-170. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch9
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Figures

Image of Figure 9.1
Figure 9.1

Mating-type () gene switching in . (A) HO endonuclease cleavage of promotes homologous recombination with one of two donor loci, in this case α, to repair the locus and to replace the Y sequences with Y sequences. Y and Y encode regulators of -, α-, and haploid-specific genes to establish the cell’s mating type. shares homology with both and in the X and Z1 regions and shares additional homology with in W and Z2. Both and are maintained in an unexpressed and heterochromatic state (shown as hatched lines) by Sir2-mediated gene silencing that is organized through the E and I silencer sequences. The preferential use of by cells and the selection of by α cells is controlled by a small -acting RE. (B) Physical monitoring of switching to α. The :: gene was induced for 1 h, and DNA was extracted at intervals for Southern blot analysis. The StyI restriction endonuclease cleaves in Y but not in Yα, so that there are different restriction fragments for and α probed with a -distal probe that also hybridizes with a common, more distal segment. In this experiment was deleted (Southern blot courtesy of Neal Sugawara).

Citation: Haber J. 2007. Decisions, Decisions: Donor Preference during Budding Yeast Mating-Type Switching, p 159-170. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch9
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Image of Figure 9.2
Figure 9.2

Molecular events during switching. Following HO cleavage, the ends of the DSB are resected by 5′ to 3′ exonucleases, leaving 3′ -ended ssDNA that first recruits the ssDNA binding complex, RPA, and then the Rad51 recombinase. The Rad51 nucleoprotein filament engages in a search for homologous sequences that will serve as a template for DSB repair. Rad51 promotes strand exchange and the formation of a D-loop in the Z region. PCNA-dependent DNA synthesis copies the Y sequences into the adjacent W region. Unlike normal semiconservative DNA replication where the newly synthesized strand remains base paired with its template, the new strand is displaced by 3′ to 5′ helicases, allowing it to base-pair with complementary single-stranded W sequences on the opposite side of the DSB. Removal of the nonhomologous 3 -ended segment by Rad1-Rad10 endonuclease, assisted by the mismatch repair proteins, Msh2-Msh3, allows the initiation of the DNA synthesis of the second strand. All newly synthesized DNA ends up in the recipient, leaving the donor unaltered.

Citation: Haber J. 2007. Decisions, Decisions: Donor Preference during Budding Yeast Mating-Type Switching, p 159-170. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch9
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Image of Figure 9.3
Figure 9.3

Kinetics and outcomes of switching influenced by RE. Following HO cleavage, can recombine with either or with α-B (BamHI). A galactose-inducible gene is turned on for 1 h, sufficient to cleave in nearly all cells, as shown in the Southern blots below. Cells are returned to glucose medium to prevent further HO cleavage, and the appearance of DSB repair products can be seen at 3 and 6 h. In cells with an intact RE, 90% of the switches are to (i.e., using ) and a few switch to α-B (using α-B). Fewer than 10% of the cells repair the DSB by nonhomologous end joining, restoring . When RE is deleted (reΔ), nearly all the gene conversions use α-B as the donor. In the Southern blots, DNA is digested with the StyI that does not cleave in Y and with BamHI, allowing all three outcomes to be distinguished. An additional StyI fragment, distal to , also hybridizes to the probe. Southern blots provided by Eric Coïc.

Citation: Haber J. 2007. Decisions, Decisions: Donor Preference during Budding Yeast Mating-Type Switching, p 159-170. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch9
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Image of Figure 9.4
Figure 9.4

DNA sequence elements in the RE. RE is located in a 2.5-kb noncoding region. A minimum enhancer of about 750 bp contains five elements (A, B, C, D, and E) conserved among sensu stricto spp. Regions D and E contain up to 15 repeats of the 4-bp sequence TTT(A/G). Regions A, D, and E contain binding sites for Fkh1, while the SCB sequence in element C (white box) binds Swi4 and Swi6. Region C contains an α2-Mcm1 repressor binding site that prevents other proteins from binding to RE in cells. There is a second α2-Mcm1 binding site on the right side of the element. Several sterile transcripts are found in RE; their role is unknown. RE function can be obtained when the RE region is deleted and replaced by four copies of the A sequence or four or five copies of D or E.

Citation: Haber J. 2007. Decisions, Decisions: Donor Preference during Budding Yeast Mating-Type Switching, p 159-170. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch9
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References

/content/book/10.1128/9781555815837.ch09
1. Althoefer, H.,, A. Schleiffer,, K. Wassmann,, A. Nordheim, and, G. Ammerer. 1995. Mcm1 is required to coordinate G2-specific transcription in Saccharomyces cerevisiae. Mol. Cell. Biol. 15:59175928.
2. Aylon, Y., and, M. Kupiec. 2005. Cell cycle-dependent regulation of double-strand break repair: a role for the CDK. Cell Cycle 4:259261.
3. Bressan, D. A.,, J. Vazquez, and, J. E. Haber. 2004. Mating type-dependent constraints on the mobility of the left arm of yeast chromosome III. J. Cell Biol. 164:361371.
4. Chai, B.,, J. Huang,, B. R. Cairns, and, B. C. Laurent. 2005. Distinct roles for the RSC and Swi/Snf ATP-dependent chromatin remodelers in DNA double-strand break repair. Genes Dev. 19:16561661.
5. Coic, E.,, G. F. Richard, and, J. E. Haber. 2006. Saccharomyces cerevisiae donor preference during mating-type switching is dependent on chromosome architecture and organization. Genetics 173:11971206.
6. Coic, E.,, K. Sun,, C. Wu, and, J. E. Haber. 2006. Cell cycle-dependent regulation of Saccharomyces cerevisiae donor preference during mating-type switching by SBF (Swi4/Swi6) and Fkh1. Mol. Cell. Biol. 26:54705480.
7. Connolly, B.,, C. I. White, and, J. E. Haber. 1988. Physical monitoring of mating type switching in Saccharomyces cerevisiae. Mol. Cell. Biol. 8:23422349.
8. Cosma, M. P. 2004. Daughter-specific repression of Saccharomyces cerevisiae HO: Ash1 is the commander. EMBO Rep. 5:953957.
9. Ercan,, S., J. C. Reese,, J. L. Workman, and, R. T. Simpson. 2005. Yeast recombination enhancer is stimulated by transcription activation. Mol. Cell. Biol. 25:79767987.
10. Haber, J. E. 1998. Mating-type gene switching in Saccharomyces cerevisiae. Annu. Rev. Genet. 32:561599.
11. Haber,, J. E. 1992. Mating-type gene switching in Saccharomyces cerevisiae. Trends Genet. 8:446452.
12. Haber, J. E. 2002. Switching of Saccharomyces cerevisiae mating-type genes, p. 927–952. In R. C. N. Craig,, M. Gellert, and, A. Lambowitz (ed.), Mobile DNA II. ASM Press, Washington, DC.
13. Haber, J. E. 2006. Transpositions and translocations induced by site-specific double-strand breaks in budding yeast. DNA Repair 5:9981009.
14. Harashima,, S., and Y. Oshima. 1980. Functional equivalence and co-dominance of homothallic genes HM alpha/hm alpha and HMa/hma in Saccharomyces yeasts. Genetics 95:819831.
15. Hawthorne, D. C. 1963. A deletion in yeast and its bearing on the structure of the mating type locus. Genetics 48:17271729.
16. Herskowitz,, I. 1989. A regulatory hierarchy for cell specialization in yeast. Nature 342:749757.
17. Hicks, J.,, J. Strathern, and, I. Herskowitz. 1977. The cassette model of mating-type interconversion, p. 457–462. In A. Bukhari,, J. Shapiro, and, S. Adhya (ed.), DNA Insertion Elements, Plasmids, and Episomes. Cold Spring Harbor Press, Cold Spring Harbor, NY.
18. Houston, P. L., and, J. R. Broach. 2006. The dynamics of homologous pairing during mating type interconversion in budding yeast. PLoS Genet. 2:e98.
19. Ira, G.,, A. Pellicioli,, A. Balijja,, X. Wang,, S. Fiorani,, W. Carotenuto,, G. Liberi,, D. Bressan,, L. Wan,, N. M. Hollingsworth,, J. E. Haber, and, M. Foiani. 2004. DNA end resection, homologous recombination and DNA damage checkpoint activation require CDK1. Nature 431:10111017.
20. Ira, G.,, D. Satory, and, J. E. Haber. 2006. Conservative inheritance of newly synthesized DNA in double-strand break-induced gene conversion. Mol. Cell. Biol. 26:9429429.
21. Jensen, R. E., and, I. Herskowitz. 1984. Directionality and regulation of cassette substitution in yeast. Cold Spring Harb. Symp. Quant. Biol. 49:97104.
22. Klar, A. J.,, J. B. Hicks, and, J. N. Strathern. 1982. Directionality of yeast mating-type interconversion. Cell 28:551561.
23. Kostriken, R., and, F. Heffron. 1984. The product of the HO gene is a nuclease: purification and characterization of the enzyme. Cold Spring Harb. Symp. Quant. Biol. 49:8996.
24. Krejci, L.,, S. Van Komen,, Y. Li,, J. Villemain,, M. S. Reddy,, H. Klein,, T. Ellenberger, and, P. Sung. 2003. DNA helicase Srs2 disrupts the Rad51 presynaptic filament. Nature 423:305309.
25. Kumar, R.,, D. M. Reynolds,, A. Shevchenko,, A. Shevchenko,, S. D. Goldstone, and, S. Dalton. 2000. Forkhead transcription factors, Fkh1p and Fkh2p, collaborate with Mcm1p to control transcription required for M-phase. Curr. Biol. 10:896906.
26. Liras, P.,, J. McCusker,, S. Mascioli, and, J. E. Haber. 1978. Characterization of a mutation in yeast causing nonrandom chromosome loss during mitosis. Genetics 88:651671.
27. Long, R. M.,, R. H. Singer,, X. Meng,, I. Gonzalez,, K. Nasmyth, and R. P. Jansen. 1997. Mating type switching in yeast controlled by asymmetric localization of ASH1 mRNA. Science 277:383387.
28. Loo, S., and, J. Rine. 1995. Silencing and heritable domains of gene expression. Annu. Rev. Cell. Dev. Biol. 11:519548.
29. Maher, M.,, F. Cong,, D. Kindelberger,, K. Nasmyth, and, S. Dalton. 1995. Cell cycle-regulated transcription of the CLB2 gene is dependent on Mcm1 and a ternary complex factor. Mol. Cell. Biol. 15:31293137.
30. Nasmyth, K. 1993. Regulating the HO endonuclease in yeast. Curr. Opin. Genet. Dev. 3:286294.
31. Nasmyth,, K. 1987. The determination of mother cell-specific mating type switching in yeast by a specific regulator of HO transcription. EMBO J. 6:243248.
32. Nickoloff, J. A.,, E. Y. Chen, and, F. Heffron. 1986. A 24-base-pair DNA sequence from the MAT locus stimulates intergenic recombination in yeast. Proc. Natl. Acad. Sci. USA 83:78317835.
33. Nickoloff, J. A.,, J. D. Singer,, M. F. Hoekstra, and, F. Heffron. 1989. Double-strand breaks stimulate alternative mechanisms of recombination repair. J. Mol. Biol. 207:527541.
34. Oshima, Y., and, I. Takano. 1971. Mating types in Saccharomyces: their convertibility and homothallism. Genetics 67:327335.
35. Pâques, F., and, J. E. Haber. 1997. Two pathways for removal of nonhomologous DNA ends during double-strand break repair in Saccharomyces cerevisiae. Mol. Cell. Biol. 17:67656771.
36. Pâques, F.,, W. Y. Leung, and, J. E. Haber. 1998. Expansions and contractions in a tandem repeat induced by double-strand break repair. Mol. Cell. Biol. 18:20452054.
37. Pâques, F.,, G.-F. Richard, and, J. E. Haber. 2001. Expansions and contractions in 36-bp minisatellite by gene conversion in yeast. Genetics 158:155166.
38. Park, E. C., and, J. W. Szostak. 1990. Point mutations in the yeast histone H4 gene prevent silencing of the silent mating type locus HML. Mol. Cell. Biol. 10:49324934.
39. Pramila, T.,, W. Wu,, S. Miles,, W. S. Noble, and, L. L. Breeden. 2006. The forkhead transcription factor Hcm1 regulates chromosome segregation genes and fills the S-phase gap in the transcriptional circuitry of the cell cycle. Genes Dev. 20:22662278.
40. Ravindra, A.,, K. Weiss, and, R. T. Simpson. 1999. High-resolution structural analysis of chromatin at specific loci: Saccharomyces cerevisiae silent mating-type locus HMRa. Mol. Cell. Biol. 19:7947950.
41. Ray, B. L.,, C. I. White, and, J. E. Haber. 1991. Heteroduplex formation and mismatch repair of the “stuck” mutation during mating-type switching in Saccharomyces cerevisiae. Mol. Cell. Biol. 11:53725380.
42. Ruan, C.,, J. L. Workman, and, R. T. Simpson. 2005. The DNA repair protein yKu80 regulates the function of recombination enhancer during yeast mating type switching. Mol. Cell. Biol. 25:84768485.
43. Rudin, N., and, J. E. Haber. 1988. Efficient repair of HO-induced chromosomal breaks in Saccharomyces cerevisiae by recombination between flanking homologous sequences. Mol. Cell. Biol. 8:39183928.
44. Strathern, J.,, J. Hicks, and, I. Herskowitz. 1981. Control of cell type in yeast by the mating type locus. The alpha 1-alpha 2 hypothesis. J. Mol. Biol. 147:357372.
45. Strathern, J. N. 1988. Control and execution of mating type switching in Saccharomyces cerevisiae, p. 445–464. In R. Kucherlapati and, G. R. Smith (ed.), Genetic Recombination. American Society for Microbiology, Washington, DC.
46. Sugawara, N.,, F. Paques,, M. Colaiacovo, and, J. E. Haber. 1997. Role of Saccharomyces cerevisiae Msh2 and Msh3 repair proteins in double-strand break-induced recombination. Proc. Natl. Acad. Sci. USA 94:9219219.
47. Sugawara, N.,, X. Wang, and, J. E. Haber. 2003. In vivo roles of Rad52, Rad54, and Rad55 proteins in Rad51-mediated recombination. Mol. Cell 12:209219.
48. Sun, K.,, E. Coic,, Z. Zhou,, P. Durrens, and, J. E. Haber. 2002. Saccharomyces forkhead protein Fkh1 regulates donor preference during mating-type switching through the recombination enhancer. Genes Dev. 16:20852096.
49. Szeto, L.,, M. K. Fafalios,, H. Zhong,, A. K. Vershon, and, J. R. Broach. 1997. Alpha2p controls donor preference during mating type interconversion in yeast by inactivating a recombinational enhancer of chromosome III. Genes Dev. 11:18991911.
50. Takano, I., and, Y. Oshima. 1970. Mutational nature of an allele-specific conversion of the mating type by the homothallic gene HO alpha in Saccharomyces. Genetics 65:421427.
51. Tanaka, K.,, T. Oshima,, H. Araki,, S. Harashima, and, Y. Oshima. 1984. Mating type control in Saccharomyces cerevisiae: a frameshift mutation at the common DNA sequence, X, of the HML alpha locus. Mol. Cell. Biol. 4:203211.
52. Tsong, A. E.,, B. B. Tuch,, H. Li, and, A. D. Johnson. 2006. Evolution of alternative transcriptional circuits with identical logic. Nature 443:415420.
53. Valencia, M.,, M. Bentele,, M. B. Vaze,, G. Herrmann,, E. Kraus,, S. E. Lee,, P. Schar, and, J. E. Haber. 2001. NEJ1 controls non-homologous end joining in Saccharomyces cerevisiae. Nature 414:666669.
54. Vaze, M.,, A. Pellicioli,, S. Lee,, G. Ira,, G. Liberi,, A. Arbel-Eden,, M. Foiani, and, J. Haber. 2002. Recovery from checkpoint-mediated arrest after repair of a double-strand break requires srs2 helicase. Mol. Cell 10:373.
55. Veaute, X.,, J. Jeusset,, C. Soustelle,, S. C. Kowalczykowski,, E. Le Cam, and F. Fabre. 2003. The Srs2 helicase prevents recombination by disrupting Rad51 nucleoprotein filaments. Nature 423:309312.
56. Wang, X., and, J. E. Haber. 2004. Role of Saccharomyces single-stranded DNA-binding protein RPA in the strand invasion step of double-strand break repair. PLoS Biol. 2:104111.
57. Wang, X.,, G. Ira,, J. A. Tercero,, A. M. Holmes,, J. F. Diffley, and, J. E. Haber. 2004. Role of DNA replication proteins in double-strand break-induced recombination in Saccharomyces cerevisiae. Mol. Cell. Biol. 24:68916899.
58. Weiler, K. S., and, J. R. Broach. 1992. Donor locus selection during Saccharomyces cerevisiae mating type interconversion responds to distant regulatory signals. Genetics 132:929942.
59. Weiler, K. S.,, L. Szeto, and, J. R. Broach. 1995. Mutations affecting donor preference during mating type interconversion in Saccharomyces cerevisiae. Genetics 139:14951510.
60. Weiss, K., and, R. T. Simpson. 1998. High-resolution structural analysis of chromatin at specific loci: Saccharomyces cerevisiae silent mating type locus HMLa. Mol. Cell. Biol. 18:53925403.
61. White, C. I., and, J. E. Haber. 1990. Intermediates of recombination during mating type switching in Saccharomyces cerevisiae. EMBO J. 9:663673.
62. Wolner, B., S. van Komen, P. Sung, and C. L. Peterson. 2003. Recruitment of the recombinational repair machinery to a DNA double-strand break in yeast. Mol. Cell 12:221232.
63. Wu, C.,, K. Weiss,, C. Yang,, M. A. Harris,, B. K. Tye,, C. S. Newlon,, R. T. Simpson, and, J. E. Haber. 1998. Mcm1 regulates donor preference controlled by the recombination enhancer in Saccharomyces mating-type switching. Genes Dev. 12:17261737.
64. Wu, X., and, J. E. Haber. 1996. A 700 bp cis-acting region controls mating-type dependent recombination along the entire left arm of yeast chromosome III. Cell 87:277285.
65. Wu, X., and, J. E. Haber. 1995. MATa donor preference in yeast mating-type switching: activation of a large chromosomal region for recombination. Genes Dev. 9:19221932.
66. Wu, X.,, J. K. Moore, and, J. E. Haber. 1996. Mechanism of MAT alpha donor preference during mating-type switching of Saccharomyces cerevisiae. Mol. Cell. Biol. 16:657668.
67. Wu, X.,, C. Wu, and, J. E. Haber. 1997. Rules of donor preference in Saccharomyces mating-type gene switching revealed by a competition assay involving two types of recombination. Genetics 147:399407.
68. Zhou, Z.,, K. Sun,, E. A. Lipstein, and, J. E. Haber. 2001. A Saccharomyces servazzii clone homologous to Saccharomyces cerevisiae chromosome III spanning KAR4, ARS 304 and SPB1 lacks the recombination enhancer but contains an unknown ORF. Yeast 18:789795.
69. Zhu, G.,, P. T. Spellman,, T. Volpe,, P. O. Brown,, D. Botstein,, T. N. Davis, and, B. Futcher. 2000. Two yeast forkhead genes regulate the cell cycle and pseudohyphal growth. Nature 406:9094.

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