Chapter 23 : Mating-type Gene Switching in

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The budding yeast propagates vegetatively either as or α haploids or as /α diploids created by conjugation of the opposite haploid types ( Fig. 1 ). Mating type is determined by two different alleles of the mating-type () locus.

Citation: Lee C, Haber J. 2015. Mating-type Gene Switching in , p 491-514. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0013-2014
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Figure 1

Homothallic life cycle of . A homothallic (pink) mother cell and its new daughter can switch to α (light blue). This lineage is established by the asymmetric partitioning of the mRNA encoding the Ash1 repressor of gene expression in daughter cells (light green). These cells can conjugate to form a zygote that gives rise to /α diploids (lilac), in which gene expression is repressed. Under nitrogen starvation, diploids undergo meiosis and sporulation to produce four haploid spores (two and two α) in an ascus. The spores germinate and grow vegetatively and can repeat the homothallic cycle. Heterothallic cells have stable mating types and grow vegetatively until they exhaust their nutrients and enter stationary phase. Used with permission from the Genetics Society of America.

Citation: Lee C, Haber J. 2015. Mating-type Gene Switching in , p 491-514. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0013-2014
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Figure 2

(A) Arrangement of , , and on chromosome 3. The gene conversion between and α is illustrated. Both and could be transcribed but are silenced by the creation of short regions of heterochromatin (ordered nucleosomes are presented as blue circles) by the interaction of silencing proteins with flanking -acting silencer E and I sequences. The recombination enhancer (RE), located 17 kb centromere-proximal to , acts to promote the usage of as the donor in cells. (B) Control of mating type-specific genes. Transcription of - and α-regulatory genes at occurs from a bidirectional promoter. The Mcm1 protein, in combination with Matα1 and Matα2, activates the transcription of α-specific genes or represses -specific genes, respectively, while a Mat1–Matα2 repressor turns off haploid-specific genes. Mat2 has no known function.

Citation: Lee C, Haber J. 2015. Mating-type Gene Switching in , p 491-514. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0013-2014
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Figure 3

Silencing of and . The processive process of silencing establishment from -E is illustrated. Proteins (ORC proteins, Rap1, and Abf1, all in gray) bound to the three elements [autonomously replicating sequence consensus sequence (ACS), Rap1-binding site, and Abf1-binding site] of the -E silencer recruit Sir1 that in turn recruits the Sir2–Sir3–Sir4 complex. The NAD- dependent HDAC Sir2 deacetylates lysines on the N-terminal tails of histones H3 and H4, which allows the Sir3–Sir4 complex to bind and stabilize the position of the nucleosome. Sir2 can then deactylate the next nucleosome and silencing spreads further. The progressing spread of silencing in the simplified figure is shown only in one direction and from one of the two silencers.

Citation: Lee C, Haber J. 2015. Mating-type Gene Switching in , p 491-514. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0013-2014
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Figure 4

Physical monitoring of switching. Southern blot analysis of I-digested DNA after galactose induction of the HO endonuclease. The probe detects sequences just distal to - Z1/Z2 and shows a difference in the size of the I restriction fragments of and α. In this experiment, an ade3::GAL::HO strain carrying α Δ was used. The cleavage of into a smaller HO-cut segment was followed by the appearance of the α product. (Figure modified from ).

Citation: Lee C, Haber J. 2015. Mating-type Gene Switching in , p 491-514. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0013-2014
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Figure 5

Mechanism of switching. Key steps in the switching of to α by a synthesis-dependent strand-annealing (SDSA) mechanism. An HO-induced DSB is resected by 5′-to-3′ exonucleases or helicase endonucleases to produce a 3′-end single-stranded DNA (ssDNA) tail, on which assembles a Rad51 filament (shown only on one side of the DSB). The Rad51::ssDNA complex engages in a search for homology. Strand invasion of -Z into the homologous -Z can be detected by anti-Rad51 chromatin immunoprecipitation followed by quantitative PCR using the primer pair P and P. Strand invasion can form an interwound (plectonemic) joint molecule (D-loop) that can assemble DNA replication factors to copy the Yα sequences, which can be monitored by a primer extension assay using the primer pair P and P. The D-loop is thought to migrate as DNA synthesis proceeds. Unlike normal replication, the newly copied strand is postulated to dissociate from the template and, when sufficiently extended, anneal with the second end, still blocked from forming a plectonemic structure by the long nonhomologous Y tail. The single-stranded tail is clipped off once strand annealing occurs by the Rad1– Rad10 flap endonuclease, so that the new 3′ end can also be used as a primer to fill in the gap. Consequently, all newly synthesized DNA is found at the locus, while the donor is unaltered. However, a small fraction of DSB repair events apparently proceed by a different repair mechanism involving the formation of a double Holliday junction.

Citation: Lee C, Haber J. 2015. Mating-type Gene Switching in , p 491-514. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0013-2014
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Figure 6

Protein binding to consensus elements in the RE. In cells, Mcm1 binding facilitates the binding of Swi4–Swi6 and multiple copies of Fkh1. These proteins are important for the ability of RE in promoting usage in cells. In α cells, binding of the Matα2–Mcm1 repressor to a 31-bp conserved operator, shared by -specific genes, leads to the formation of highly positioned nucleosomes between the two flanking genes and excludes binding of Fkh1 or Swi4–Swi6.

Citation: Lee C, Haber J. 2015. Mating-type Gene Switching in , p 491-514. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0013-2014
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Figure 7

Role of the recombination enhancer in donor preference. (A) Arrangement of α, , and α–HI (α-). When RE is replaced by four LexA-binding sites (LexA), usage is strongly impaired. Expression of LexA–FHA (the phosphothreonine-binding domain of Fkh1) fusion protein completely rescues usage, while expression of the mutant LexA–FHA, which has lost phosphothreonine-binding activity, fails to rescue it. (B) Southern blot data after induction of switching showing the proportion of HI-digested α or α- DNA in the strains depicted above. (Figure modified from .)

Citation: Lee C, Haber J. 2015. Mating-type Gene Switching in , p 491-514. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0013-2014
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Figure 8

Model for Fkh1-regulated donor preference. A cluster of Fkh1 bound to RE in cells can associate with phosphothreonine residues that are located near the DSB and created by casein kinase II, and possibly other kinases, in response to the DSB. The association of Fkh1 and the DSB, which has been demonstrated by ChIP, tethers within ∼20 kb of the DSB ends and facilitates its use over , located 100 kb away.

Citation: Lee C, Haber J. 2015. Mating-type Gene Switching in , p 491-514. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0013-2014
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1. Klar AJ . 1987. Determination of the yeast cell lineage. Cell 49 : 433 435.[PubMed] [CrossRef]
2. Herskowitz I . 1988. Life cycle of the budding yeast Saccharomyces cerevisiae . Microbiol Rev 52 : 536 553.[PubMed]
3. Haber JE . 2006. Transpositions and translocations induced by site-specific double-strand breaks in budding yeast. DNA Repair 5 : 998 1009.[PubMed] [CrossRef]
4. Haber JE . 2012. Mating-type genes and MAT switching in Saccharomyces cerevisiae . Genetics 191 : 33 64.[PubMed] [CrossRef]
5. Strathern JN, . 1988. Control and execution of mating type switching in Saccharomyces cerevisiae , p 445 464. In Kucherlapati R,, Smith GR (ed), Genetic Recombination. ASM Press, Washington, DC.
6. Haber JE, . 2007. Decisions, decisions: donor preference during budding yeast mating-type switching, p 159 170. In Heitman J,, Kronstad JW,, Taylor JW,, Casselton LA (ed), Sex in Fungi: Molecular Determination and Evolutionary Implications. ASM Press, Washington, DC. [CrossRef]
7. Nasmyth KA . 1982. Molecular genetics of yeast mating type. Annu Rev Genet 16 : 439 500.[PubMed] [CrossRef]
8. Weiss K,, Simpson RT . 1998. High-resolution structural analysis of chromatin at specific loci: Saccharomyces cerevisiae silent mating type locus HMLα. Mol Cell Biol 18 : 5392 5403.[PubMed]
9. Ravindra A,, Weiss K,, Simpson RT . 1999. High-resolution structural analysis of chromatin at specific loci: Saccharomyces cerevisiae silent mating-type locus HMRa. Mol Cell Biol 19 : 7944 7950.[PubMed]
10. Brand AH,, Breeden L,, Abraham J,, Sternglanz R,, Nasmyth K . 1985. Characterization of a “silencer” in yeast: a DNA sequence with properties opposite to those of a transcriptional enhancer. Cell 41 : 41 48.[PubMed] [CrossRef]
11. Schnell R,, Rine J . 1986. A position effect on the expression of a tRNA gene mediated by the SIR genes in Saccharomyces cerevisiae . Mol Cell Biol 6 : 494 501.[PubMed]
12. Connolly B,, White CI,, Haber JE . 1988. Physical monitoring of mating type switching in Saccharomyces cerevisiae . Mol Cell Biol 8 : 2342 2349.[PubMed]
13. Loo S,, Rine J . 1994. Silencers and domains of generalized repression. Science 264 : 1768 1771.[PubMed] [CrossRef]
14. Hagen DC,, Bruhn L,, Westby CA,, Sprague GF Jr . 1993. Transcription of α-specific genes in Saccharomyces cerevisiae: DNA sequence requirements for activity of the coregulator α1. Mol Cell Biol 13 : 6866 6875.[PubMed]
15. Bruhn L,, Sprague GF Jr . 1994. MCM1 point mutants deficient in expression of α-specific genes: residues important for interaction with α1. Mol Cell Biol 14 : 2534 2544.[PubMed] [CrossRef]
16. Smith DL,, Johnson AD . 1992. A molecular mechanism for combinatorial control in yeast: MCM1 protein sets the spacing and orientation of the homeodomains of an α2 dimer. Cell 68 : 133 142.[PubMed] [CrossRef]
17. Keleher CA,, Passmore S,, Johnson AD . 1989. Yeast repressor α 2 binds to its operator cooperatively with yeast protein Mcm1. Mol Cell Biol 9 : 5228 5230.[PubMed]
18. Herschbach BM,, Arnaud MB,, Johnson AD . 1994. Transcriptional repression directed by the yeast α 2 protein in vitro. Nature 370 : 309 311.[PubMed] [CrossRef]
19. Patterton HG,, Simpson RT . 1994. Nucleosomal location of the STE6 TATA box and Matα2p-mediated repression. Mol Cell Biol 14 : 4002 4010.[PubMed]
20. Smith RL,, Johnson AD . 2000. Turning genes off by Ssn6–Tup1: a conserved system of transcriptional repression in eukaryotes. Trends Biochem Sci 25 : 325 330.[PubMed] [CrossRef]
21. Jensen R,, Sprague GF Jr,, Herskowitz I . 1983. Regulation of yeast mating-type interconversion: feedback control of HO gene expression by the mating-type locus. Proc Nat Acad Sci U S A 80 : 3035 3039.[PubMed] [CrossRef]
22. Goutte C,, Johnson AD . 1988. a1 protein alters the DNA binding specificity of α2 repressor. Cell 52 : 875 882.[PubMed] [CrossRef]
23. Li T,, Stark MR,, Johnson AD,, Wolberger C . 1995. Crystal structure of the MATa1/MAT α 2 homeodomain heterodimer bound to DNA. Science 270 : 262 269.[PubMed] [CrossRef]
24. Johnson PR,, Swanson R,, Rakhilina L,, Hochstrasser M . 1998. Degradation signal masking by heterodimerization of MATα2 and MATa1 blocks their mutual destruction by the ubiquitin-proteasome pathway. Cell 94 : 217 227.[PubMed] [CrossRef]
25. Tan S,, Richmond TJ . 1998. Crystal structure of the yeast MATα2/MCM1/DNA ternary complex. Nature 391 : 660 666.[PubMed] [CrossRef]
26. Chant J . 1996. Generation of cell polarity in yeast. Curr Opin Cell Biol 8 : 557 565.[PubMed] [CrossRef]
27. Chant J,, Pringle JR . 1991. Budding and cell polarity in Saccharomyces cerevisiae . Curr Opin Genet Dev 1 : 342 350.[PubMed] [CrossRef]
28. Lord M,, Inose F,, Hiroko T,, Hata T,, Fujita A,, Chant J . 2002. Subcellular localization of Axl1, the cell type-specific regulator of polarity. Curr Biol 12 : 1347 1352.[PubMed] [CrossRef]
29. Frank--Vaillant M,, Marcand S . 2001. NHEJ regulation by mating type is exercised through a novel protein, Lif2p, essential to the ligase IV pathway. Genes Dev 15 : 3005 3012.[PubMed] [CrossRef]
30. Kegel A,, Sjostrand JO,, Astrom SU . 2001. Nej1p, a cell type-specific regulator of nonhomologous end joining in yeast. Curr Biol 11 : 1611 1617.[PubMed] [CrossRef]
31. Ooi SL,, Shoemaker DD,, Boeke JD . 2001. A DNA microarray-based genetic screen for nonhomologous end-joining mutants in Saccharomyces cerevisiae . Science 294 : 2552 2556.[PubMed] [CrossRef]
32. Valencia M,, Bentele M,, Vaze MB,, Herrmann G,, Kraus E,, Lee SE,, Schar P,, Haber JE . 2001. NEJ1 controls non-homologous end joining in Saccharomyces cerevisiae . Nature 414 : 666 669.[PubMed] [CrossRef]
33. Laney JD,, Hochstrasser M . 2003. Ubiquitin-dependent degradation of the yeast Matα2 repressor enables a switch in developmental state. Genes Dev 17 : 2259 2270.[PubMed] [CrossRef]
34. Laney JD,, Mobley EF,, Hochstrasser M . 2006. The short-lived Matα2 transcriptional repressor is protected from degradation in vivo by interactions with its corepressors Tup1 and Ssn6. Mol Cell Biol 26 : 371 380.[PubMed] [CrossRef]
35. Haber JE,, George JP . 1979. A mutation that permits the expression of normally silent copies of mating-type information in Saccharomyces cerevisiae . Genetics 93 : 13 35.[PubMed]
36. Nasmyth K . 1987. The determination of mother cell-specific mating type switching in yeast by a specific regulator of HO transcription. EMBO J 6 : 243 248.[PubMed]
37. Breeden L,, Nasmyth K . 1987. Cell cycle control of the yeast HO gene: cis- and trans- acting regulators. Cell 48 : 389 397.[PubMed] [CrossRef]
38. Nasmyth K,, Stillman D,, Kipling D . 1987. Both positive and negative regulators of HO transcription are required for mother-cell-specific mating-type switching in yeast. Cell 48 : 579 587.[PubMed] [CrossRef]
39. Long RM,, Singer RH,, Meng X,, Gonzalez I,, Nasmyth K,, Jansen RP . 1997. Mating type switching in yeast controlled by asymmetric localization of ASH1 mRNA. Science 277 : 383 387.[PubMed] [CrossRef]
40. Bobola N,, Jansen RP,, Shin TH,, Nasmyth K . 1996. Asymmetric accumulation of Ash1p in postanaphase nuclei depends on a myosin and restricts yeast mating-type switching to mother cells. Cell 84 : 699 709.[PubMed] [CrossRef]
41. Sil A,, Herskowitz I . 1996. Identification of asymmetrically localized determinant, Ash1p, required for lineage-specific transcription of the yeast HO gene. Cell 84 : 711 722.[PubMed] [CrossRef]
42. Shepard KA,, Gerber AP,, Jambhekar A,, Takizawa PA,, Brown PO,, Herschlag D,, DeRisi JL,, Vale RD . 2003. Widespread cytoplasmic mRNA transport in yeast: identification of 22 bud-localized transcripts using DNA microarray analysis. Proc Nat Acad Sci U S A 100 : 11429 11434.[PubMed] [CrossRef]
43. Jambhekar A,, McDermott K,, Sorber K,, Shepard KA,, Vale RD,, Takizawa PA,, DeRisi JL . 2005. Unbiased selection of localization elements reveals cis-acting determinants of mRNA bud localization in Saccharomyces cerevisiae . Proc Nat Acad Sci U S A 102 : 18005 18010.[PubMed] [CrossRef]
44. Kaplun L,, Ivantsiv Y,, Bakhrat A,, Raveh D . 2003. DNA damage response-mediated degradation of Ho endonuclease via the ubiquitin system involves its nuclear export. J Biol Chem 278 : 48727 48734.[PubMed] [CrossRef]
45. Kaplun L,, Ivantsiv Y,, Bakhrat A,, Tzirkin R,, Baranes K,, Shabek N,, Raveh D . 2006. The F-box protein, Ufo1, maintains genome stability by recruiting the yeast mating switch endonuclease, Ho, for rapid proteasome degradation. Isr Med Assoc J 8 : 246 248.[PubMed]
46. Haber JE,, Wolfe KH, . 2005. Evolution and function of HO and VDE endoncucleases in fungi, p 161 175. In Belfort B,, Derbyshire V,, Stodddard B,, Wood D (ed), Homing Endonucleases and Inteins. Springer-Verlag, New York. [CrossRef]
47. Nickoloff JA,, Chen EY,, Heffron F . 1986. A 24-base-pair DNA sequence from the MAT locus stimulates intergenic recombination in yeast. Proc Nat Acad Sci U S A 83 : 7831 7835.[PubMed] [CrossRef]
48. Nickoloff JA,, Singer JD,, Heffron F . 1990. In vivo analysis of the Saccharomyces cerevisiae HO nuclease recognition site by site-directed mutagenesis. Mol Cell Biol 10 : 1174 1179.[PubMed]
49. McNally FJ,, Rine J . 1991. A synthetic silencer mediates SIR-dependent functions in Saccharomyces cerevisiae . Mol Cell Biol 11 : 5648 5659.[PubMed]
50. Laurenson P,, Rine J . 1992. Silencers, silencing, and heritable transcriptional states. Microbiol Rev 56 : 543 560.[PubMed]
51. Sherman JM,, Pillus L . 1997. An uncertain silence. Trends Genet 13 : 308 313.[PubMed] [CrossRef]
52. Astrom SU,, Rine J . 1998. Theme and variation among silencing proteins in Saccharomyces cerevisiae and Kluyveromyces lactis . Genetics 148 : 1021 1029.[PubMed]
53. Grunstein M . 1998. Yeast heterochromatin: regulation of its assembly and inheritance by histones. Cell 93 : 325 328.[PubMed] [CrossRef]
54. Lustig AJ . 1998. Mechanisms of silencing in Saccharomyces cerevisiae . Curr Opin Genet Dev 8 : 233 239.[PubMed] [CrossRef]
55. Stone EM,, Pillus L . 1998. Silent chromatin in yeast: an orchestrated medley featuring Sir3p [corrected]. BioEssays 20 : 30 40.[PubMed] [CrossRef]
56. Rusche LN,, Kirchmaier AL,, Rine J . 2003. The establishment, inheritance, and function of silenced chromatin in Saccharomyces cerevisiae . Annu Rev Biochem 72 : 481 516.[PubMed] [CrossRef]
57. McConnell KH,, Muller P,, Fox CA . 2006. Tolerance of Sir1p/origin recognition complex-dependent silencing for enhanced origin firing at HMRa. Mol Cell Biol 26 : 1955 1966.[PubMed] [CrossRef]
58. Hickman MA,, Froyd CA,, Rusche LN . 2011. Reinventing heterochromatin in budding yeasts: Sir2 and the origin recognition complex take center stage. Eukaryot Cell 10 : 1183 1192.[PubMed] [CrossRef]
59. Thompson--Stewart D,, Karpen GH,, Spradling AC . 1994. A transposable element can drive the concerted evolution of tandemly repetitious DNA. Proc Nat Acad Sci U S A 91 : 9042 9046.[PubMed] [CrossRef]
60. Shei GJ,, Broach JR . 1995. Yeast silencers can act as orientation-dependent gene inactivation centers that respond to environmental signals. Mol Cell Biol 15 : 3496 3506.[PubMed]
61. Maillet L,, Boscheron C,, Gotta M,, Marcand S,, Gilson E,, Gasser SM . 1996. Evidence for silencing compartments within the yeast nucleus: a role for telomere proximity and Sir protein concentration in silencer-mediated repression. Genes Dev 10 : 1796 1811.[PubMed] [CrossRef]
62. Marcand S,, Buck SW,, Moretti P,, Gilson E,, Shore D . 1996. Silencing of genes at nontelomeric sites in yeast is controlled by sequestration of silencing factors at telomeres by Rap 1 protein. Genes Dev 10 : 1297 1309.[PubMed] [CrossRef]
63. Bird AW,, Yu DY,, Pray--Grant MG,, Qiu Q,, Harmon KE,, Megee PC,, Grant PA,, Smith MM,, Christman MF . 2002. Acetylation of histone H4 by Esa1 is required for DNA double- strand break repair. Nature 419 : 411 415.[PubMed] [CrossRef]
64. Wolner B,, Peterson CL . 2005. ATP-dependent and ATP-independent roles for the Rad54 chromatin remodeling enzyme during recombinational repair of a DNA double strand break. J Biol Chem 280 : 10855 10860.[PubMed] [CrossRef]
65. Thompson JS,, Johnson LM,, Grunstein M . 1994. Specific repression of the yeast silent mating locus HMR by an adjacent telomere. Mol Cell Biol 14 : 446 455.[PubMed]
66. Ren J,, Wang CL,, Sternglanz R . 2010. Promoter strength influences the S phase requirement for establishment of silencing at the Saccharomyces cerevisiae silent mating type loci. Genetics 186 : 551 560.[PubMed] [CrossRef]
67. Ishii K,, Arib G,, Lin C,, Van Houwe G,, Laemmli UK . 2002. Chromatin boundaries in budding yeast: the nuclear pore connection. Cell 109 : 551 562.[PubMed] [CrossRef]
68. Donze D,, Adams CR,, Rine J,, Kamakaka RT . 1999. The boundaries of the silenced HMR domain in Saccharomyces cerevisiae . Genes Dev 13 : 698 708.[PubMed] [CrossRef]
69. Dhillon N,, Raab J,, Guzzo J,, Szyjka SJ,, Gangadharan S,, Aparicio OM,, Andrews B,, Kamakaka RT . 2009. DNA polymerase epsilon, acetylases and remodellers cooperate to form a specialized chromatin structure at a tRNA insulator. EMBO J 28 : 2583 2600.[PubMed] [CrossRef]
70. Klar AJ,, Fogel S,, Macleod K . 1979. MAR1—a Regulator of the HMa and HMα loci in Saccharomyces cerevisiae . Genetics 93 : 37 50.[PubMed]
71. Rine J,, Strathern JN,, Hicks JB,, Herskowitz I . 1979. A suppressor of mating-type locus mutations in Saccharomyces cerevisiae: evidence for and identification of cryptic mating-type loci. Genetics 93 : 877 901.[PubMed]
72. Rine J,, Herskowitz I . 1987. Four genes responsible for a position effect on expression from HML and HMR in Saccharomyces cerevisiae . Genetics 116 : 9 22.[PubMed]
73. Pillus L,, Rine J . 1989. Epigenetic inheritance of transcriptional states in S. cerevisiae . Cell 59 : 637 647.[PubMed] [CrossRef]
74. Imai S,, Armstrong CM,, Kaeberlein M,, Guarente L . 2000. Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature 403 : 795 800.[PubMed] [CrossRef]
75. Armache KJ,, Garlick JD,, Canzio D,, Narlikar GJ,, Kingston RE . 2011. Structural basis of silencing: Sir3 BAH domain in complex with a nucleosome at 3.0 Å resolution. Science 334 : 977 982.[PubMed] [CrossRef]
76. Takahashi YH,, Schulze JM,, Jackson J,, Hentrich T,, Seidel C,, Jaspersen SL,, Kobor MS,, Shilatifard A . 2011. Dot1 and histone H3K79 methylation in natural telomeric and HM silencing. Mol Cell 42 : 118 126.[PubMed] [CrossRef]
77. Moazed D,, Kistler A,, Axelrod A,, Rine J,, Johnson AD . 1997. Silent information regulator protein complexes in Saccharomyces cerevisiae: a SIR2/SIR4 complex and evidence for a regulatory domain in SIR4 that inhibits its interaction with SIR3. Proc Nat Acad Sci U S A 94 : 2186 2191.[PubMed] [CrossRef]
78. Tsukamoto Y,, Kato J,, Ikeda H . 1996. Hdf1, a yeast Ku-protein homologue, is involved in illegitimate recombination, but not in homologous recombination. Nucleic Acids Res 24 : 2067 2072.[PubMed] [CrossRef]
79. Taddei A,, Hediger F,, Neumann FR,, Bauer C,, Gasser SM . 2004. Separation of silencing from perinuclear anchoring functions in yeast Ku80, Sir4 and Esc1 proteins. EMBO J 23 : 1301 1312.[PubMed] [CrossRef]
80. Megee PC,, Morgan BA,, Mittman BA,, Smith MM . 1990. Genetic analysis of histone H4: essential role of lysines subject to reversible acetylation. Science 247 : 841 845.[PubMed] [CrossRef]
81. Park EC,, Szostak JW . 1990. Point mutations in the yeast histone H4 gene prevent silencing of the silent mating type locus HML. Mol Cell Biol 10 : 4932 4934.[PubMed]
82. Fisher--Adams G,, Grunstein M . 1995. Yeast histone H4 and H3 N-termini have different effects on the chromatin structure of the GAL1 promoter. EMBO J 14 : 1468 1477.[PubMed]
83. Hecht A,, Laroche T,, Strahl--Bolsinger S,, Gasser SM,, Grunstein M . 1995. Histone H3 and H4 N-termini interact with SIR3 and SIR4 proteins: a molecular model for the formation of heterochromatin in yeast. Cell 80 : 583 592.[PubMed] [CrossRef]
84. Braunstein M,, Sobel RE,, Allis CD,, Turner BM,, Broach JR . 1996. Efficient transcriptional silencing in Saccharomyces cerevisiae requires a heterochromatin histone acetylation pattern. Mol Cell Biol 16 : 4349 4356.[PubMed]
85. Li J,, Coic E,, Lee K,, Lee CS,, Kim JA,, Wu Q,, Haber JE . 2012. Regulation of budding yeast mating-type switching donor preference by the FHA domain of Fkh1. PLoS Genet 8 : e1002630. [PubMed] [CrossRef]
86. Lafon A,, Chang CS,, Scott EM,, Jacobson SJ,, Pillus L . 2007. MYST opportunities for growth control: yeast genes illuminate human cancer gene functions. Oncogene 26 : 5373 5384.[PubMed] [CrossRef]
87. Gasser SM,, Cockell MM . 2001. The molecular biology of the SIR proteins. Gene 279 : 1 16.[PubMed] [CrossRef]
88. Moretti P,, Freeman K,, Coodly L,, Shore D . 1994. Evidence that a complex of SIR proteins interacts with the silencer and telomere-binding protein RAP1. Genes Dev 8 : 2257 2269.[PubMed] [CrossRef]
89. Wotton D,, Shore D . 1997. A novel Rap1p-interacting factor, Rif2p, cooperates with Rif1p to regulate telomere length in Saccharomyces cerevisiae . Genes Dev 11 : 748 760.[PubMed] [CrossRef]
90. Mishra K,, Shore D . 1999. Yeast Ku protein plays a direct role in telomeric silencing and counteracts inhibition by rif proteins. Curr Biol 9 : 1123 1126.[PubMed] [CrossRef]
91. Roy R,, Meier B,, McAinsh AD,, Feldmann HM,, Jackson SP . 2004. Separation-of- function mutants of yeast Ku80 reveal a Yku80p–Sir4p interaction involved in telomeric silencing. J Biol Chem 279 : 86 94.[PubMed] [CrossRef]
92. Ribes--Zamora A,, Mihalek I,, Lichtarge O,, Bertuch AA . 2007. Distinct faces of the Ku heterodimer mediate DNA repair and telomeric functions. Nat Struct Mol Biol 14 : 301 307.[PubMed] [CrossRef]
93. Strahl--Bolsinger S,, Hecht A,, Luo K,, Grunstein M . 1997. SIR2 and SIR4 interactions differ in core and extended telomeric heterochromatin in yeast. Genes Dev 11 : 83 93.[PubMed] [CrossRef]
94. Rusche LN,, Lynch PJ . 2009. Assembling heterochromatin in the appropriate places: a boost is needed. J Cell Physiol 219 : 525 528.[PubMed] [CrossRef]
95. Vandre CL,, Kamakaka RT,, Rivier DH . 2008. The DNA end-binding protein Ku regulates silencing at the internal HML and HMR loci in Saccharomyces cerevisiae . Genetics 180 : 1407 1418.[PubMed] [CrossRef]
96. Takahashi T,, Saito H,, Ikeda Y . 1958. Heterothallic behavior of a homothallic strain in Saccharomyces yeast. Genetics 43 : 249 260.[PubMed]
97. Takano I,, Oshima Y . 1967. An allele specific and a complementary determinant controlling homothallism in Saccharomyces oviformis . Genetics 57 : 875 885.[PubMed]
98. Santa Maria J,, Vidal D . 1970. Segregación anormal del “mating type” en Saccharomyces. Inst Nac Invest Agron Conf 30 : 1 21.
99. Oshima Y,, Takano I . 1971. Mating types in Saccharomyces: their convertibility and homothallism. Genetics 67 : 327 335.[PubMed]
100. Hicks J,, Strathern JN . 1977. Interconversion of mating type in S. cerevisiae and the cassette model for gene transfer. Brookhaven Symp Biol 233 242.[PubMed]
101. Hicks J,, Strathern J,, Herskowitz I, . 1977. The cassette model of mating-type interconversion, p 457 462. In Bukhari A,, Shapiro J,, Adhya S (ed), DNA Insertion Elements, Plasmids and Episomes. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
102. Nasmyth KA,, Tatchell K . 1980. The structure of transposable yeast mating type loci. Cell 19 : 753 764.[PubMed] [CrossRef]
103. Strathern JN,, Spatola E,, McGill C,, Hicks JB . 1980. Structure and organization of transposable mating type cassettes in Saccharomyces yeasts. Proc Nat Acad Sci U S A 77 : 2839 2843.[PubMed] [CrossRef]
104. Astell CR,, Ahlstrom-Jonasson L,, Smith M,, Tatchell K,, Nasmyth KA,, Hall BD . 1981. The sequence of the DNAs coding for the mating-type loci of Saccharomyces cerevisiae . Cell 27 : 15 23.[PubMed] [CrossRef]
105. Tatchell K,, Nasmyth KA,, Hall BD,, Astell C,, Smith M . 1981. In vitro mutation analysis of the mating-type locus in yeast. Cell 27 : 25 35.[PubMed] [CrossRef]
106. Naumov GI,, Tolstorukov II . 1971. [ Discovery of an unstable homothallic strain of Saccharomyces cerevisiae var. elipsoideus .] Nauchnye Doki Vyss Shkoly Biol Nauki 9 : 92 94 (in Russian).[PubMed]
107. Tolstorukov II,, Naumov GI . 1973. [ Comparative genetics of yeasts. XI. A genetic study of autodiploidization in natural homothallic strains of Saccharomyces]. Nauchnye Doki Vyss Shkoly Biol Nauki 117 : 111 115 (in Russian).[PubMed]
108. Hicks J,, Strathern JN,, Klar AJ . 1979. Transposable mating type genes in Saccharomyces cerevisiae . Nature 282 : 478 473.[PubMed] [CrossRef]
109. Klar AJ,, Fogel S,, Radin DN . 1979. Switching of a mating-type a mutant allele in budding yeast Saccharomyces cerevisiae . Genetics 92 : 759 776.[PubMed]
110. Sprague GF Jr,, Rine J,, Herskowitz I . 1981. Homology and non-homology at the yeast mating type locus. Nature 289 : 250 252.[PubMed] [CrossRef]
111. McGill C,, Shafer B,, Strathern J . 1989. Coconversion of flanking sequences with homothallic switching. Cell 57 : 459 467.[CrossRef]
112. Rattray AJ,, Symington LS . 1995. Multiple pathways for homologous recombination in Saccharomyces cerevisiae . Genetics 139 : 45 56.[PubMed]
113. Paques F,, Haber JE . 1999. Multiple pathways of recombination induced by double- strand breaks in Saccharomyces cerevisiae . Microbiology and Molecular Biology Reviews 63 : 349 404.[PubMed]
114. Aylon Y,, Kupiec M . 2004. DSB repair: the yeast paradigm. DNA repair 3 : 797 815.[PubMed] [CrossRef]
115. Krogh BO,, Symington LS . 2004. Recombination proteins in yeast. Annu Rev Genet 38 : 233 271.[PubMed] [CrossRef]
116. Daley JM,, Palmbos PL,, Wu D,, Wilson TE . 2005. Nonhomologous end joining in yeast. Annu Rev Genet 39 : 431 451.[PubMed] [CrossRef]
117. McEachern MJ,, Haber JE . 2006. Break-induced replication and recombinational telomere elongation in yeast. Annu Rev Biochem 75 : 111 135.[PubMed] [CrossRef]
118. Sung P,, Klein H . 2006. Mechanism of homologous recombination: mediators and helicases take on regulatory functions. Nat Rev Mol Cell Biol 7 : 739 750.[PubMed] [CrossRef]
119. Lydeard JR,, Jain S,, Yamaguchi M,, Haber JE . 2007. Break-induced replication and telomerase-independent telomere maintenance require Pol32. Nature 448 : 820 823.[PubMed] [CrossRef]
120. Li X,, Heyer WD . 2008. Homologous recombination in DNA repair and DNA damage tolerance. Cell Res 18 : 99 113.[PubMed] [CrossRef]
121. McVey M,, Lee SE . 2008. MMEJ repair of double-strand breaks (director’s cut): deleted sequences and alternative endings. Trends Genet 24 : 529 538.[PubMed] [CrossRef]
122. San Filippo J,, Sung P,, Klein H . 2008. Mechanism of eukaryotic homologous recombination. Annu Rev Biochem 77 : 229 257.[PubMed] [CrossRef]
123. Jain S,, Sugawara N,, Lydeard J,, Vaze M,, Tanguy Le Gac N,, Haber JE . 2009. A recombination execution checkpoint regulates the choice of homologous recombination pathway during DNA double-strand break repair. Genes Dev 23 : 291 303.[PubMed] [CrossRef]
124. Heyer WD,, Ehmsen KT,, Liu J . 2010. Regulation of homologous recombination in eukaryotes. Annu Rev Genet 44 : 113 139.[PubMed] [CrossRef]
125. Schwartz EK,, Heyer WD . 2011. Processing of joint molecule intermediates by structure-selective endonucleases during homologous recombination in eukaryotes. Chromosoma 120 : 109 127.[PubMed] [CrossRef]
126. Rudin N,, Haber JE . 1988. Efficient repair of HO-induced chromosomal breaks in Saccharomyces cerevisiae by recombination between flanking homologous sequences. Mol Cell Biol 8 : 3918 3928.[PubMed]
127. Nickoloff JA,, Singer JD,, Hoekstra MF,, Heffron F . 1989. Double-strand breaks stimulate alternative mechanisms of recombination repair. J Mol Biol 207 : 527 541.[PubMed] [CrossRef]
128. Ray A,, Machin N,, Stahl FW . 1989. A DNA double chain break stimulates triparental recombination in Saccharomyces cerevisiae . Proc Nat Acad Sci U S A 86 : 6225 6229.[PubMed] [CrossRef]
129. Plessis A,, Perrin A,, Haber JE,, Dujon B . 1992. Site-specific recombination determined by I-SceI, a mitochondrial group I intron-encoded endonuclease expressed in the yeast nucleus. Genetics 130 : 451 460.[PubMed]
130. McGill CB,, Shafer BK,, Derr LK,, Strathern JN . 1993. Recombination initiated by double-strand breaks. Curr Genet 23 : 305 314.[PubMed] [CrossRef]
131. Liefshitz B,, Parket A,, Maya R,, Kupiec M . 1995. The role of DNA repair genes in recombination between repeated sequences in yeast. Genetics 140 : 1199 1211.[PubMed]
132. Weng YS,, Whelden J,, Gunn L,, Nickoloff JA . 1996. Double-strand break-induced mitotic gene conversion: examination of tract polarity and products of multiple recombinational repair events. Curr Genet 29 : 335 343.[PubMed] [CrossRef]
133. Inbar O,, Kupiec M . 1999. Homology search and choice of homologous partner during mitotic recombination. Mol Cell Biol 19 : 4134 4142.[PubMed]
134. Wilson TE . 2002. A genomics-based screen for yeast mutants with an altered recombination/end-joining repair ratio. Genetics 162 : 677 688.[PubMed]
135. Storici F,, Durham CL,, Gordenin DA,, Resnick MA . 2003. Chromosomal site-specific double-strand breaks are efficiently targeted for repair by oligonucleotides in yeast. Proc Nat Acad Sci U S A 100 : 14994 14999. [PubMed] [CrossRef]
136. Lydeard JR,, Lipkin--Moore Z,, Sheu YJ,, Stillman B,, Burgers PM,, Haber JE . 2010. Break-induced replication requires all essential DNA replication factors except those specific for pre-RC assembly. Genes Dev 24 : 1133 1144.[PubMed] [CrossRef]
137. Marrero VA,, Symington LS . 2010. Extensive DNA end processing by exo1 and sgs1 inhibits break-induced replication. PLoS Genetics 6 : e1001007. [PubMed] [CrossRef]
138. Kleckner N . 1996. Meiosis: how could it work? Proc Nat Acad Sci U S A 93 : 8167 8174.[PubMed] [CrossRef]
139. Borner GV,, Kleckner N,, Hunter N . 2004. Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell 117 : 29 45.[PubMed] [CrossRef]
140. Keeney S,, Neale MJ . 2006. Initiation of meiotic recombination by formation of DNA double-strand breaks: mechanism and regulation. Biochem Soc Trans 34 : 523 525.[PubMed] [CrossRef]
141. Longhese MP,, Bonetti D,, Guerini I,, Manfrini N,, Clerici M . 2009. DNA double- strand breaks in meiosis: checking their formation, processing and repair. DNA repair 8 : 1127 1138.[PubMed] [CrossRef]
142. Strathern JN,, Klar AJ,, Hicks JB,, Abraham JA,, Ivy JM,, Nasmyth KA,, McGill C . 1982. Homothallic switching of yeast mating type cassettes is initiated by a double-stranded cut in the MAT locus. Cell 31 : 183 192.[PubMed] [CrossRef]
143. Kostriken R,, Strathern JN,, Klar AJ,, Hicks JB,, Heffron F . 1983. A site-specific endonuclease essential for mating-type switching in Saccharomyces cerevisiae . Cell 35 : 167 174.[PubMed] [CrossRef]
144. Klar AJ,, Hicks JB,, Strathern JN . 1981. Irregular transpositions of mating-type genes in yeast. Cold Spring Harb Symp Quant Biol 45 : 983 990.[PubMed] [CrossRef]
145. Miyazaki T,, Bressan DA,, Shinohara M,, Haber JE,, Shinohara A . 2004. In vivo assembly and disassembly of Rad51 and Rad52 complexes during double-strand break repair. EMBO J 23 : 939 949.[PubMed] [CrossRef]
146. Jensen RE,, Herskowitz I . 1984. Directionality and regulation of cassette substitution in yeast. Cold Spring Harb Symp Quant Biol 49 : 97 104.[PubMed] [CrossRef]
147. Raveh D,, Hughes SH,, Shafer BK,, Strathern JN . 1989. Analysis of the HO-cleaved MAT DNA intermediate generated during the mating type switch in the yeast Saccharomyces cerevisiae . Mol Gen Genet 220 : 33 42.[PubMed]
148. White CI,, Haber JE . 1990. Intermediates of recombination during mating type switching in Saccharomyces cerevisiae . EMBO J 9 : 663 673.[PubMed]
149. Hicks WM,, Yamaguchi M,, Haber JE . 2011. Real-time analysis of double-strand DNA break repair by homologous recombination. Proc Nat Acad Sci U S A 108 : 3108 3115.[PubMed] [CrossRef]
150. Haber JE . 1995. In vivo biochemistry: physical monitoring of recombination induced by site-specific endonucleases. BioEssays 17 : 609 620.[PubMed] [CrossRef]
151. Ira G,, Satory D,, Haber JE . 2006. Conservative inheritance of newly synthesized DNA in double-strand break-induced gene conversion. Mol Cell Biol 26 : 9424 9429.[PubMed] [CrossRef]
152. Cortes--Ledesma F,, Aguilera A . 2006. Double-strand breaks arising by replication through a nick are repaired by cohesin-dependent sister-chromatid exchange. EMBO Reports 7 : 919 926.[PubMed] [CrossRef]
153. Weiffenbach B,, Haber JE . 1981. Homothallic mating type switching generates lethal chromosome breaks in rad52 strains of Saccharomyces cerevisiae . Mol Cell Biol 1 : 522 534.[PubMed]
154. Ray BL,, White CI,, Haber JE . 1991. Heteroduplex formation and mismatch repair of the “stuck” mutation during mating-type switching in Saccharomyces cerevisiae . Mol Cell Biol 11 : 5372 5380.[PubMed]
155. Chen H,, Lisby M,, Symington LS . 2013. RPA coordinates DNA end resection and prevents formation of DNA hairpins. Mol Cell 50 : 589 600.[PubMed] [CrossRef]
156. Fishman-Lobell J,, Rudin N,, Haber JE . 1992. Two alternative pathways of double- strand break repair that are kinetically separable and independently modulated. Mol Cell Biol 12 : 1292 1303.[PubMed]
157. Zhu Z,, Chung WH,, Shim EY,, Lee SE,, Ira G . 2008. Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell 134 : 981 994.[PubMed] [CrossRef]
158. Sugawara N,, Haber JE . 1992. Characterization of double-strand break-induced recombination: homology requirements and single-stranded DNA formation. Mol Cell Biol 12 : 563 575.[PubMed]
159. Ivanov EL,, Sugawara N,, White CI,, Fabre F,, Haber JE . 1994. Mutations in XRS2 and RAD50 delay but do not prevent mating-type switching in Saccharomyces cerevisiae . Mol Cell Biol 14 : 3414 3425.[PubMed]
160. Tsubouchi H,, Ogawa H . 1998. A novel mre11 mutation impairs processing of double-strand breaks of DNA during both mitosis and meiosis. Mol Cell Biol 18 : 260 268.[PubMed]
161. Bressan DA,, Olivares HA,, Nelms BE,, Petrini JH . 1998. Alteration of N-terminal phosphoesterase signature motifs inactivates Saccharomyces cerevisiae Mre11. Genetics 150 : 591 600.[PubMed]
162. Lee SE,, Bressan DA,, Petrini JH,, Haber JE . 2002. Complementation between N- terminal Saccharomyces cerevisiae mre11 alleles in DNA repair and telomere length maintenance. DNA Repair 1 : 27 40.[PubMed] [CrossRef]
163. Nicolette ML,, Lee K,, Guo Z,, Rani M,, Chow JM,, Lee SE,, Paull TT . 2010. Mre11–Rad50–Xrs2 and Sae2 promote 5′ strand resection of DNA double-strand breaks. Nat Struct Mol Biol 17 : 1478 1485.[PubMed] [CrossRef]
164. Moreau S,, Ferguson JR,, Symington LS . 1999. The nuclease activity of Mre11 is required for meiosis but not for mating type switching, end joining, or telomere maintenance. Mol Cell Biol 19 : 556 566.[PubMed]
165. Lobachev K,, Vitriol E,, Stemple J,, Resnick MA,, Bloom K . 2004. Chromosome fragmentation after induction of a double-strand break is an active process prevented by the RMX repair complex. Curr Biol 14 : 2107 2112.[PubMed] [CrossRef]
166. Yu J,, Marshall K,, Yamaguchi M,, Haber JE,, Weil CF . 2004. Microhomology-dependent end joining and repair of transposon-induced DNA hairpins by host factors in Saccharomyces cerevisiae . Mol Cell Biol 24 : 1351 1364.[PubMed] [CrossRef]
167. Clerici M,, Mantiero D,, Lucchini G,, Longhese MP . 2005. The Saccharomyces cerevisiae Sae2 protein promotes resection and bridging of double strand break ends. J Biol Chem 280 : 38631 38638.[PubMed] [CrossRef]
168. Huertas P,, Cortes--Ledesma F,, Sartori AA,, Aguilera A,, Jackson SP . 2008. CDK targets Sae2 to control DNA-end resection and homologous recombination. Nature 455 : 689 692.[PubMed] [CrossRef]
169. Mimitou EP,, Symington LS . 2008. Sae2, Exo1 and Sgs1 collaborate in DNA double- strand break processing. Nature 455 : 770 774.[PubMed] [CrossRef]
170. Niu H,, Chung WH,, Zhu Z,, Kwon Y,, Zhao W,, Chi P,, Prakash R,, Seong C,, Liu D,, Lu L,, Ira G,, Sung P . 2010. Mechanism of the ATP-dependent DNA end-resection machinery from Saccharomyces cerevisiae . Nature 467 : 108 111.[PubMed] [CrossRef]
171. Mimitou EP,, Symington LS . 2010. Ku prevents Exo1 and Sgs1-dependent resection of DNA ends in the absence of a functional MRX complex or Sae2. EMBO J 29 : 3358 3369.[PubMed] [CrossRef]
172. Shim EY,, Chung WH,, Nicolette ML,, Zhang Y,, Davis M,, Zhu Z,, Paull TT,, Ira G,, Lee SE . 2010. Saccharomyces cerevisiae Mre11/Rad50/Xrs2 and Ku proteins regulate association of Exo1 and Dna2 with DNA breaks. EMBO J 29 : 3370 3380.[PubMed] [CrossRef]
173. Diede SJ,, Gottschling DE . 2001. Exonuclease activity is required for sequence addition and Cdc13p loading at a de novo telomere. Curr Biol 11 : 1336 1340.[PubMed] [CrossRef]
174. Aylon Y,, Liefshitz B,, Kupiec M . 2004. The CDK regulates repair of double-strand breaks by homologous recombination during the cell cycle. EMBO J 23 : 4868 4875.[PubMed] [CrossRef]
175. Ira G,, Pellicioli A,, Balijja A,, Wang X,, Fiorani S,, Carotenuto W,, Liberi G,, Bressan D,, Wan L,, Hollingsworth NM,, Haber JE,, Foiani M . 2004. DNA end resection, homologous recombination and DNA damage checkpoint activation require CDK1. Nature 431 : 1011 1017.[PubMed] [CrossRef]
176. Chen X,, Niu H,, Chung WH,, Zhu Z,, Papusha A,, Shim EY,, Lee SE,, Sung P,, Ira G . 2011. Cell cycle regulation of DNA double-strand break end resection by Cdk1-dependent Dna2 phosphorylation. Nat Struct Mol Biol 18 : 1015 1019.[PubMed] [CrossRef]
177. Chen X,, Cui D,, Papusha A,, Zhang X,, Chu CD,, Tang J,, Chen K,, Pan X,, Ira G . 2012. The Fun30 nucleosome remodeller promotes resection of DNA double-strand break ends. Nature 489 : 576 580.[PubMed] [CrossRef]
178. Costelloe T,, Louge R,, Tomimatsu N,, Mukherjee B,, Martini E,, Khadaroo B,, Dubois K,, Wiegant WW,, Thierry A,, Burma S,, van Attikum H,, Llorente B . 2012. The yeast Fun30 and human SMARCAD1 chromatin remodellers promote DNA end resection. Nature 489 : 581 584.[PubMed] [CrossRef]
179. Eapen VV,, Sugawara N,, Tsabar M,, Wu WH,, Haber JE . 2012. The Saccharomyces cerevisiae chromatin remodeler Fun30 regulates DNA end resection and checkpoint deactivation. Mol Cell Biol 32 : 4727 4740.[PubMed] [CrossRef]
180. Neves-Costa A,, Will WR,, Vetter AT,, Miller JR,, Varga--Weisz P . 2009. The SNF2- family member Fun30 promotes gene silencing in heterochromatic loci. PLoS One 4 : e8111. [PubMed] [CrossRef]
181. Awad S,, Ryan D,, Prochasson P,, Owen--Hughes T,, Hassan AH . 2010. The Snf2 homolog Fun30 acts as a homodimeric ATP-dependent chromatin-remodeling enzyme. J Biol Chem 285 : 9477 9484.[PubMed] [CrossRef]
182. Wang X,, Haber JE . 2004. Role of Saccharomyces single-stranded DNA-binding protein RPA in the strand invasion step of double-strand break repair. PLoS Biol 2 : E21. [PubMed] [CrossRef]
183. Sugawara N,, Wang X,, Haber JE . 2003. In vivo roles of Rad52, Rad54, and Rad55 proteins in Rad51-mediated recombination. Mol Cell 12 : 209 219.[PubMed] [CrossRef]
184. Wolner B,, van Komen S,, Sung P,, Peterson CL . 2003. Recruitment of the recombinational repair machinery to a DNA double-strand break in yeast. Mol Cell 12 : 221 232.[PubMed] [CrossRef]
185. Bressan DA,, Vazquez J,, Haber JE . 2004. Mating type-dependent constraints on the mobility of the left arm of yeast chromosome III. J Cell Biol 164 : 361 371.[PubMed] [CrossRef]
186. Houston PL,, Broach JR . 2006. The dynamics of homologous pairing during mating type interconversion in budding yeast. PLoS Genet 2 : e98. [PubMed] [CrossRef]
187. Kim JA,, Hicks WM,, Li J,, Tay SY,, Haber JE . 2011. Protein phosphatases Pph3, Ptc2, and Ptc3 play redundant roles in DNA double-strand break repair by homologous recombination. Mol Cell Biol 31 : 507 516.[PubMed] [CrossRef]
188. Coic E,, Martin J,, Ryu T,, Tay SY,, Kondev J,, Haber JE . 2011. Dynamics of homology searching during gene conversion in Saccharomyces cerevisiae revealed by donor competition. Genetics 189 : 1225 1233.[PubMed] [CrossRef]
189. Fishman-Lobell J,, Haber JE . 1992. Removal of nonhomologous DNA ends in double-strand break recombination: the role of the yeast ultraviolet repair gene RAD1. Science 258 : 480 484.[PubMed] [CrossRef]
190. Lyndaker AM,, Goldfarb T,, Alani E . 2008. Mutants defective in Rad1–Rad10–Slx4 exhibit a unique pattern of viability during mating-type switching in Saccharomyces cerevisiae . Genetics 179 : 1807 1821.[PubMed] [CrossRef]
191. Colaiacovo MP,, Paques F,, Haber JE . 1999. Removal of one nonhomologous DNA end during gene conversion by a RAD1- and MSH2-independent pathway. Genetics 151 : 1409 1423.[PubMed]
192. Li F,, Dong J,, Pan X,, Oum JH,, Boeke JD,, Lee SE . 2008. Microarray-based genetic screen defines SAW1, a gene required for Rad1/Rad10-dependent processing of recombination intermediates. Mol Cell 30 : 325 335.[PubMed] [CrossRef]
193. Toh GW,, Sugawara N,, Dong J,, Toth R,, Lee SE,, Haber JE,, Rouse J . 2010. Mec1/Tel1-dependent phosphorylation of Slx4 stimulates Rad1–Rad10-dependent cleavage of non-homologous DNA tails. DNA Repair 9 : 718 726.[PubMed] [CrossRef]
194. Haber JE,, Ray BL,, Kolb JM,, White CI . 1993. Rapid kinetics of mismatch repair of heteroduplex DNA that is formed during recombination in yeast. Proc Nat Acad Sci U S A 90 : 3363 3367.[PubMed] [CrossRef]
195. Porter SE,, White MA,, Petes TD . 1993. Genetic evidence that the meiotic recombination hotspot at the HIS4 locus of Saccharomyces cerevisiae does not represent a site for a symmetrically processed double-strand break. Genetics 134 : 5 19.[PubMed]
196. Leung W,, Malkova A,, Haber JE . 1997. Gene targeting by linear duplex DNA frequently occurs by assimilation of a single strand that is subject to preferential mismatch correction. Proc Nat Acad Sci U S A 94 : 6851 6856.[PubMed] [CrossRef]
197. Jaskelioff M,, Van Komen S,, Krebs JE,, Sung P,, Peterson CL . 2003. Rad54p is a chromatin remodeling enzyme required for heteroduplex DNA joint formation with chromatin. J Biol Chem 278 : 9212 9218.[PubMed] [CrossRef]
198. Anand RP,, Lovett ST,, Haber JE . 2013. Break-induced DNA replication. Cold Spring Harb Perspect Biol 5 : a010397. [PubMed] [CrossRef]
199. Wang X,, Ira G,, Tercero JA,, Holmes AM,, Diffley JF,, Haber JE . 2004. Role of DNA replication proteins in double-strand break-induced recombination in Saccharomyces cerevisiae . Mol Cell Biol 24 : 6891 6899.[PubMed] [CrossRef]
200. Holmes AM,, Haber JE . 1999. Double-strand break repair in yeast requires both leading and lagging strand DNA polymerases. Cell 96 : 415 424.[PubMed] [CrossRef]
201. Muramatsu S,, Hirai K,, Tak YS,, Kamimura Y,, Araki H . 2010. CDK-dependent complex formation between replication proteins Dpb11, Sld2, Pol ε, and GINS in budding yeast. Genes Dev 24 : 602 612.[PubMed] [CrossRef]
202. Chung WH,, Zhu Z,, Papusha A,, Malkova A,, Ira G . 2010. Defective resection at DNA double-strand breaks leads to de novo telomere formation and enhances gene targeting. PLoS Genet 6 : e1000948. [PubMed] [CrossRef]
203. Wilson MA,, Kwon Y,, Xu Y,, Chung WH,, Chi P,, Niu H,, Mayle R,, Chen X,, Malkova A,, Sung P,, Ira G . 2013. Pif1 helicase and Polδ promote recombination-coupled DNA synthesis via bubble migration. Nature 502 : 393 396.[PubMed] [CrossRef]
204. Hicks WM,, Kim M,, Haber JE . 2010. Increased mutagenesis and unique mutation signature associated with mitotic gene conversion. Science 329 : 82 85.[PubMed] [CrossRef]
205. Stith CM,, Sterling J,, Resnick MA,, Gordenin DA,, Burgers PM . 2008. Flexibility of eukaryotic Okazaki fragment maturation through regulated strand displacement synthesis. J Biol Chem 283 : 34129 40.[PubMed] [CrossRef]
206. Holbeck SL,, Strathern JN . 1997. A role for REV3 in mutagenesis during double- strand break repair in Saccharomyces cerevisiae . Genetics 147 : 1017 1024.[PubMed]
207. Yang Y,, Sterling J,, Storici F,, Resnick MA,, Gordenin DA . 2008. Hypermutability of damaged single-strand DNA formed at double-strand breaks and uncapped telomeres in yeast Saccharomyces cerevisiae . PLoS Genet 4 : e1000264. [PubMed] [CrossRef]
208. Haber JE,, Rogers DT,, McCusker JH . 1980. Homothallic conversions of yeast mating-type genes occur by intrachromosomal recombination. Cell 22 : 277 289.[PubMed] [CrossRef]
209. Klar AJ,, Strathern JN . 1984. Resolution of recombination intermediates generated during yeast mating type switching. Nature 310 : 744 748.[PubMed] [CrossRef]
210. Ira G,, Malkova A,, Liberi G,, Foiani M,, Haber JE . 2003. Srs2 and Sgs1–Top3 suppress crossovers during double-strand break repair in yeast. Cell 115 : 401 411.[PubMed] [CrossRef]
211. Prakash R,, Satory D,, Dray E,, Papusha A,, Scheller J,, Kramer W,, Krejci L,, Klein H,, Haber JE,, Sung P,, Ira G . 2009. Yeast Mph1 helicase dissociates Rad51-made D-loops: implications for crossover control in mitotic recombination. Genes Dev 23 : 67 79.[PubMed] [CrossRef]
212. Klar AJ,, Hicks JB,, Strathern JN . 1982. Directionality of yeast mating-type interconversion. Cell 28 : 551 561.[PubMed] [CrossRef]
213. Weiler KS,, Broach JR . 1992