Skip to main content
PMC home page
Genetics logoLink to Genetics
. 2001 Dec;159(4):1449–1465. doi: 10.1093/genetics/159.4.1449

Multiple regulators of Ty1 transposition in Saccharomyces cerevisiae have conserved roles in genome maintenance.

D T Scholes 1, M Banerjee 1, B Bowen 1, M J Curcio 1
PMCID: PMC1461915  PMID: 11779788

Abstract

Most Ty1 retrotransposons in the genome of Saccharomyces cerevisiae are transpositionally competent but rarely transpose. We screened yeast mutagenized by insertion of the mTn3-lacZ/LEU2 transposon for mutations that result in elevated Ty1 cDNA-mediated mobility, which occurs by cDNA integration or recombination. Here, we describe the characterization of mTn3 insertions in 21 RTT (regulation of Ty1 transposition) genes that result in 5- to 111-fold increases in Ty1 mobility. These 21 RTT genes are EST2, RRM3, NUT2, RAD57, RRD2, RAD50, SGS1, TEL1, SAE2, MED1, MRE11, SCH9, KAP122, and 8 previously uncharacterized genes. Disruption of RTT genes did not significantly increase Ty1 RNA levels but did enhance Ty1 cDNA levels, suggesting that most RTT gene products act at a step after mRNA accumulation but before cDNA integration. The rtt mutations had widely varying effects on integration of Ty1 at preferred target sites. Mutations in RTT101 and NUT2 dramatically stimulated Ty1 integration upstream of tRNA genes. In contrast, a mutation in RRM3 increased Ty1 mobility >100-fold without increasing integration upstream of tRNA genes. The regulation of Ty1 transposition by components of fundamental pathways required for genome maintenance suggests that Ty1 and yeast have coevolved to link transpositional dormancy to the integrity of the genome.

Full Text

The Full Text of this article is available as a PDF (342.4 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Alani E., Cao L., Kleckner N. A method for gene disruption that allows repeated use of URA3 selection in the construction of multiply disrupted yeast strains. Genetics. 1987 Aug;116(4):541–545. doi: 10.1534/genetics.112.541.test. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Balciunas D., Gälman C., Ronne H., Björklund S. The Med1 subunit of the yeast mediator complex is involved in both transcriptional activation and repression. Proc Natl Acad Sci U S A. 1999 Jan 19;96(2):376–381. doi: 10.1073/pnas.96.2.376. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Boeke J. D., Garfinkel D. J., Styles C. A., Fink G. R. Ty elements transpose through an RNA intermediate. Cell. 1985 Mar;40(3):491–500. doi: 10.1016/0092-8674(85)90197-7. [DOI] [PubMed] [Google Scholar]
  4. Boeke J. D., Styles C. A., Fink G. R. Saccharomyces cerevisiae SPT3 gene is required for transposition and transpositional recombination of chromosomal Ty elements. Mol Cell Biol. 1986 Nov;6(11):3575–3581. doi: 10.1128/mcb.6.11.3575. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bork P., Hofmann K., Bucher P., Neuwald A. F., Altschul S. F., Koonin E. V. A superfamily of conserved domains in DNA damage-responsive cell cycle checkpoint proteins. FASEB J. 1997 Jan;11(1):68–76. [PubMed] [Google Scholar]
  6. Brachmann C. B., Davies A., Cost G. J., Caputo E., Li J., Hieter P., Boeke J. D. Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast. 1998 Jan 30;14(2):115–132. doi: 10.1002/(SICI)1097-0061(19980130)14:2<115::AID-YEA204>3.0.CO;2-2. [DOI] [PubMed] [Google Scholar]
  7. Bradshaw V. A., McEntee K. DNA damage activates transcription and transposition of yeast Ty retrotransposons. Mol Gen Genet. 1989 Sep;218(3):465–474. doi: 10.1007/BF00332411. [DOI] [PubMed] [Google Scholar]
  8. Bryk M., Banerjee M., Conte D., Jr, Curcio M. J. The Sgs1 helicase of Saccharomyces cerevisiae inhibits retrotransposition of Ty1 multimeric arrays. Mol Cell Biol. 2001 Aug;21(16):5374–5388. doi: 10.1128/MCB.21.16.5374-5388.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Burns N., Grimwade B., Ross-Macdonald P. B., Choi E. Y., Finberg K., Roeder G. S., Snyder M. Large-scale analysis of gene expression, protein localization, and gene disruption in Saccharomyces cerevisiae. Genes Dev. 1994 May 1;8(9):1087–1105. doi: 10.1101/gad.8.9.1087. [DOI] [PubMed] [Google Scholar]
  10. Conte D., Jr, Barber E., Banerjee M., Garfinkel D. J., Curcio M. J. Posttranslational regulation of Ty1 retrotransposition by mitogen-activated protein kinase Fus3. Mol Cell Biol. 1998 May;18(5):2502–2513. doi: 10.1128/mcb.18.5.2502. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Conte D., Jr, Curcio M. J. Fus3 controls Ty1 transpositional dormancy through the invasive growth MAPK pathway. Mol Microbiol. 2000 Jan;35(2):415–427. doi: 10.1046/j.1365-2958.2000.01710.x. [DOI] [PubMed] [Google Scholar]
  12. Curcio M. J., Garfinkel D. J. Heterogeneous functional Ty1 elements are abundant in the Saccharomyces cerevisiae genome. Genetics. 1994 Apr;136(4):1245–1259. doi: 10.1093/genetics/136.4.1245. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Curcio M. J., Garfinkel D. J. Posttranslational control of Ty1 retrotransposition occurs at the level of protein processing. Mol Cell Biol. 1992 Jun;12(6):2813–2825. doi: 10.1128/mcb.12.6.2813. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Curcio M. J., Garfinkel D. J. Single-step selection for Ty1 element retrotransposition. Proc Natl Acad Sci U S A. 1991 Feb 1;88(3):936–940. doi: 10.1073/pnas.88.3.936. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Curcio M. J., Hedge A. M., Boeke J. D., Garfinkel D. J. Ty RNA levels determine the spectrum of retrotransposition events that activate gene expression in Saccharomyces cerevisiae. Mol Gen Genet. 1990 Jan;220(2):213–221. doi: 10.1007/BF00260484. [DOI] [PubMed] [Google Scholar]
  16. Curcio M. J., Sanders N. J., Garfinkel D. J. Transpositional competence and transcription of endogenous Ty elements in Saccharomyces cerevisiae: implications for regulation of transposition. Mol Cell Biol. 1988 Sep;8(9):3571–3581. doi: 10.1128/mcb.8.9.3571. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Devine S. E., Boeke J. D. Integration of the yeast retrotransposon Ty1 is targeted to regions upstream of genes transcribed by RNA polymerase III. Genes Dev. 1996 Mar 1;10(5):620–633. doi: 10.1101/gad.10.5.620. [DOI] [PubMed] [Google Scholar]
  18. Downs J. A., Jackson S. P. Involvement of DNA end-binding protein Ku in Ty element retrotransposition. Mol Cell Biol. 1999 Sep;19(9):6260–6268. doi: 10.1128/mcb.19.9.6260. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Elledge S. J., Davis R. W. Two genes differentially regulated in the cell cycle and by DNA-damaging agents encode alternative regulatory subunits of ribonucleotide reductase. Genes Dev. 1990 May;4(5):740–751. doi: 10.1101/gad.4.5.740. [DOI] [PubMed] [Google Scholar]
  20. Fabrizio P., Pozza F., Pletcher S. D., Gendron C. M., Longo V. D. Regulation of longevity and stress resistance by Sch9 in yeast. Science. 2001 Apr 5;292(5515):288–290. doi: 10.1126/science.1059497. [DOI] [PubMed] [Google Scholar]
  21. Fiori A., Bianchi M. M., Fabiani L., Falcone C., Francisci S., Palleschi C., Solimando N., Uccelletti D., Frontali L. Disruption of six novel genes from chromosome VII of Saccharomyces cerevisiae reveals one essential gene and one gene which affects the growth rate. Yeast. 2000 Mar 15;16(4):377–386. doi: 10.1002/1097-0061(20000315)16:4<377::AID-YEA537>3.0.CO;2-S. [DOI] [PubMed] [Google Scholar]
  22. Galy V., Olivo-Marin J. C., Scherthan H., Doye V., Rascalou N., Nehrbass U. Nuclear pore complexes in the organization of silent telomeric chromatin. Nature. 2000 Jan 6;403(6765):108–112. doi: 10.1038/47528. [DOI] [PubMed] [Google Scholar]
  23. Gangloff S., McDonald J. P., Bendixen C., Arthur L., Rothstein R. The yeast type I topoisomerase Top3 interacts with Sgs1, a DNA helicase homolog: a potential eukaryotic reverse gyrase. Mol Cell Biol. 1994 Dec;14(12):8391–8398. doi: 10.1128/mcb.14.12.8391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Goyer C., Altmann M., Lee H. S., Blanc A., Deshmukh M., Woolford J. L., Jr, Trachsel H., Sonenberg N. TIF4631 and TIF4632: two yeast genes encoding the high-molecular-weight subunits of the cap-binding protein complex (eukaryotic initiation factor 4F) contain an RNA recognition motif-like sequence and carry out an essential function. Mol Cell Biol. 1993 Aug;13(8):4860–4874. doi: 10.1128/mcb.13.8.4860. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Greenwell P. W., Kronmal S. L., Porter S. E., Gassenhuber J., Obermaier B., Petes T. D. TEL1, a gene involved in controlling telomere length in S. cerevisiae, is homologous to the human ataxia telangiectasia gene. Cell. 1995 Sep 8;82(5):823–829. doi: 10.1016/0092-8674(95)90479-4. [DOI] [PubMed] [Google Scholar]
  26. Gustafsson C. M., Myers L. C., Beve J., Spåhr H., Lui M., Erdjument-Bromage H., Tempst P., Kornberg R. D. Identification of new mediator subunits in the RNA polymerase II holoenzyme from Saccharomyces cerevisiae. J Biol Chem. 1998 Nov 20;273(47):30851–30854. doi: 10.1074/jbc.273.47.30851. [DOI] [PubMed] [Google Scholar]
  27. Haber J. E. The many interfaces of Mre11. Cell. 1998 Nov 25;95(5):583–586. doi: 10.1016/s0092-8674(00)81626-8. [DOI] [PubMed] [Google Scholar]
  28. Huang H., Hong J. Y., Burck C. L., Liebman S. W. Host genes that affect the target-site distribution of the yeast retrotransposon Ty1. Genetics. 1999 Apr;151(4):1393–1407. doi: 10.1093/genetics/151.4.1393. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Huang M., Zhou Z., Elledge S. J. The DNA replication and damage checkpoint pathways induce transcription by inhibition of the Crt1 repressor. Cell. 1998 Sep 4;94(5):595–605. doi: 10.1016/s0092-8674(00)81601-3. [DOI] [PubMed] [Google Scholar]
  30. Ivessa A. S., Zhou J. Q., Zakian V. A. The Saccharomyces Pif1p DNA helicase and the highly related Rrm3p have opposite effects on replication fork progression in ribosomal DNA. Cell. 2000 Feb 18;100(4):479–489. doi: 10.1016/s0092-8674(00)80683-2. [DOI] [PubMed] [Google Scholar]
  31. Ji H., Moore D. P., Blomberg M. A., Braiterman L. T., Voytas D. F., Natsoulis G., Boeke J. D. Hotspots for unselected Ty1 transposition events on yeast chromosome III are near tRNA genes and LTR sequences. Cell. 1993 Jun 4;73(5):1007–1018. doi: 10.1016/0092-8674(93)90278-x. [DOI] [PubMed] [Google Scholar]
  32. Jonniaux J. L., Coster F., Purnelle B., Goffeau A. A 21.7 kb DNA segment on the left arm of yeast chromosome XIV carries WHI3, GCR2, SPX18, SPX19, an homologue to the heat shock gene SSB1 and 8 new open reading frames of unknown function. Yeast. 1994 Dec;10(12):1639–1645. doi: 10.1002/yea.320101213. [DOI] [PubMed] [Google Scholar]
  33. Jordan I. K., McDonald J. F. Evidence for the role of recombination in the regulatory evolution of Saccharomyces cerevisiae Ty elements. J Mol Evol. 1998 Jul;47(1):14–20. doi: 10.1007/pl00006358. [DOI] [PubMed] [Google Scholar]
  34. Kawakami K., Pande S., Faiola B., Moore D. P., Boeke J. D., Farabaugh P. J., Strathern J. N., Nakamura Y., Garfinkel D. J. A rare tRNA-Arg(CCU) that regulates Ty1 element ribosomal frameshifting is essential for Ty1 retrotransposition in Saccharomyces cerevisiae. Genetics. 1993 Oct;135(2):309–320. doi: 10.1093/genetics/135.2.309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Kim J. M., Vanguri S., Boeke J. D., Gabriel A., Voytas D. F. Transposable elements and genome organization: a comprehensive survey of retrotransposons revealed by the complete Saccharomyces cerevisiae genome sequence. Genome Res. 1998 May;8(5):464–478. doi: 10.1101/gr.8.5.464. [DOI] [PubMed] [Google Scholar]
  36. Laloux I., Dubois E., Dewerchin M., Jacobs E. TEC1, a gene involved in the activation of Ty1 and Ty1-mediated gene expression in Saccharomyces cerevisiae: cloning and molecular analysis. Mol Cell Biol. 1990 Jul;10(7):3541–3550. doi: 10.1128/mcb.10.7.3541. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Lee B. S., Bi L., Garfinkel D. J., Bailis A. M. Nucleotide excision repair/TFIIH helicases RAD3 and SSL2 inhibit short-sequence recombination and Ty1 retrotransposition by similar mechanisms. Mol Cell Biol. 2000 Apr;20(7):2436–2445. doi: 10.1128/mcb.20.7.2436-2445.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Lee B. S., Lichtenstein C. P., Faiola B., Rinckel L. A., Wysock W., Curcio M. J., Garfinkel D. J. Posttranslational inhibition of Ty1 retrotransposition by nucleotide excision repair/transcription factor TFIIH subunits Ssl2p and Rad3p. Genetics. 1998 Apr;148(4):1743–1761. doi: 10.1093/genetics/148.4.1743. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Lendvay T. S., Morris D. K., Sah J., Balasubramanian B., Lundblad V. Senescence mutants of Saccharomyces cerevisiae with a defect in telomere replication identify three additional EST genes. Genetics. 1996 Dec;144(4):1399–1412. doi: 10.1093/genetics/144.4.1399. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Leonhardt S. A., Fearson K., Danese P. N., Mason T. L. HSP78 encodes a yeast mitochondrial heat shock protein in the Clp family of ATP-dependent proteases. Mol Cell Biol. 1993 Oct;13(10):6304–6313. doi: 10.1128/mcb.13.10.6304. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Liebman S. W., Newnam G. A ubiquitin-conjugating enzyme, RAD6, affects the distribution of Ty1 retrotransposon integration positions. Genetics. 1993 Mar;133(3):499–508. doi: 10.1093/genetics/133.3.499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Lundblad V., Szostak J. W. A mutant with a defect in telomere elongation leads to senescence in yeast. Cell. 1989 May 19;57(4):633–643. doi: 10.1016/0092-8674(89)90132-3. [DOI] [PubMed] [Google Scholar]
  43. Marcand S., Gilson E., Shore D. A protein-counting mechanism for telomere length regulation in yeast. Science. 1997 Feb 14;275(5302):986–990. doi: 10.1126/science.275.5302.986. [DOI] [PubMed] [Google Scholar]
  44. Morawetz C., Hagen U. Effect of irradiation and mutagenic chemicals on the generation of ADH2- and ADH4-constitutive mutants in yeast: the inducibility of Ty transposition by UV and ethyl methanesulfonate. Mutat Res. 1990 Mar;229(1):69–77. doi: 10.1016/0027-5107(90)90009-s. [DOI] [PubMed] [Google Scholar]
  45. Morillon A., Springer M., Lesage P. Activation of the Kss1 invasive-filamentous growth pathway induces Ty1 transcription and retrotransposition in Saccharomyces cerevisiae. Mol Cell Biol. 2000 Aug;20(15):5766–5776. doi: 10.1128/mcb.20.15.5766-5776.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Morrow D. M., Tagle D. A., Shiloh Y., Collins F. S., Hieter P. TEL1, an S. cerevisiae homolog of the human gene mutated in ataxia telangiectasia, is functionally related to the yeast checkpoint gene MEC1. Cell. 1995 Sep 8;82(5):831–840. doi: 10.1016/0092-8674(95)90480-8. [DOI] [PubMed] [Google Scholar]
  47. Myers L. C., Gustafsson C. M., Bushnell D. A., Lui M., Erdjument-Bromage H., Tempst P., Kornberg R. D. The Med proteins of yeast and their function through the RNA polymerase II carboxy-terminal domain. Genes Dev. 1998 Jan 1;12(1):45–54. doi: 10.1101/gad.12.1.45. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Ohta T., Michel J. J., Schottelius A. J., Xiong Y. ROC1, a homolog of APC11, represents a family of cullin partners with an associated ubiquitin ligase activity. Mol Cell. 1999 Apr;3(4):535–541. doi: 10.1016/s1097-2765(00)80482-7. [DOI] [PubMed] [Google Scholar]
  49. Qian Z., Huang H., Hong J. Y., Burck C. L., Johnston S. D., Berman J., Carol A., Liebman S. W. Yeast Ty1 retrotransposition is stimulated by a synergistic interaction between mutations in chromatin assembly factor I and histone regulatory proteins. Mol Cell Biol. 1998 Aug;18(8):4783–4792. doi: 10.1128/mcb.18.8.4783. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Rattray A. J., McGill C. B., Shafer B. K., Strathern J. N. Fidelity of mitotic double-strand-break repair in Saccharomyces cerevisiae: a role for SAE2/COM1. Genetics. 2001 May;158(1):109–122. doi: 10.1093/genetics/158.1.109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Rattray A. J., Shafer B. K., Garfinkel D. J. The Saccharomyces cerevisiae DNA recombination and repair functions of the RAD52 epistasis group inhibit Ty1 transposition. Genetics. 2000 Feb;154(2):543–556. doi: 10.1093/genetics/154.2.543. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Rempola B., Kaniak A., Migdalski A., Rytka J., Slonimski P. P., di Rago J. P. Functional analysis of RRD1 (YIL153w) and RRD2 (YPL152w), which encode two putative activators of the phosphotyrosyl phosphatase activity of PP2A in Saccharomyces cerevisiae. Mol Gen Genet. 2000 Jan;262(6):1081–1092. doi: 10.1007/pl00008651. [DOI] [PubMed] [Google Scholar]
  53. Ritchie K. B., Petes T. D. The Mre11p/Rad50p/Xrs2p complex and the Tel1p function in a single pathway for telomere maintenance in yeast. Genetics. 2000 May;155(1):475–479. doi: 10.1093/genetics/155.1.475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Rose A. B., Broach J. R. Propagation and expression of cloned genes in yeast: 2-microns circle-based vectors. Methods Enzymol. 1990;185:234–279. doi: 10.1016/0076-6879(90)85024-i. [DOI] [PubMed] [Google Scholar]
  55. Schmitt M., Neupert W., Langer T. Hsp78, a Clp homologue within mitochondria, can substitute for chaperone functions of mt-hsp70. EMBO J. 1995 Jul 17;14(14):3434–3444. doi: 10.1002/j.1460-2075.1995.tb07349.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Sikorski R. S., Hieter P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics. 1989 May;122(1):19–27. doi: 10.1093/genetics/122.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Singer M. S., Gottschling D. E. TLC1: template RNA component of Saccharomyces cerevisiae telomerase. Science. 1994 Oct 21;266(5184):404–409. doi: 10.1126/science.7545955. [DOI] [PubMed] [Google Scholar]
  58. Smith V., Chou K. N., Lashkari D., Botstein D., Brown P. O. Functional analysis of the genes of yeast chromosome V by genetic footprinting. Science. 1996 Dec 20;274(5295):2069–2074. doi: 10.1126/science.274.5295.2069. [DOI] [PubMed] [Google Scholar]
  59. Staleva Staleva L., Venkov P. Activation of Ty transposition by mutagens. Mutat Res. 2001 Mar 1;474(1-2):93–103. doi: 10.1016/s0027-5107(00)00165-2. [DOI] [PubMed] [Google Scholar]
  60. Strambio-de-Castillia C., Blobel G., Rout M. P. Proteins connecting the nuclear pore complex with the nuclear interior. J Cell Biol. 1999 Mar 8;144(5):839–855. doi: 10.1083/jcb.144.5.839. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Tabtiang R. K., Herskowitz I. Nuclear proteins Nut1p and Nut2p cooperate to negatively regulate a Swi4p-dependent lacZ reporter gene in Saccharomyces cerevisiae. Mol Cell Biol. 1998 Aug;18(8):4707–4718. doi: 10.1128/mcb.18.8.4707. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Teng S. C., Zakian V. A. Telomere-telomere recombination is an efficient bypass pathway for telomere maintenance in Saccharomyces cerevisiae. Mol Cell Biol. 1999 Dec;19(12):8083–8093. doi: 10.1128/mcb.19.12.8083. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Titov A. A., Blobel G. The karyopherin Kap122p/Pdr6p imports both subunits of the transcription factor IIA into the nucleus. J Cell Biol. 1999 Oct 18;147(2):235–246. doi: 10.1083/jcb.147.2.235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Toda T., Cameron S., Sass P., Wigler M. SCH9, a gene of Saccharomyces cerevisiae that encodes a protein distinct from, but functionally and structurally related to, cAMP-dependent protein kinase catalytic subunits. Genes Dev. 1988 May;2(5):517–527. doi: 10.1101/gad.2.5.517. [DOI] [PubMed] [Google Scholar]
  65. Tye B. K. MCM proteins in DNA replication. Annu Rev Biochem. 1999;68:649–686. doi: 10.1146/annurev.biochem.68.1.649. [DOI] [PubMed] [Google Scholar]
  66. Wang Y. X., Zhao H., Harding T. M., Gomes de Mesquita D. S., Woldringh C. L., Klionsky D. J., Munn A. L., Weisman L. S. Multiple classes of yeast mutants are defective in vacuole partitioning yet target vacuole proteins correctly. Mol Biol Cell. 1996 Sep;7(9):1375–1389. doi: 10.1091/mbc.7.9.1375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Watt P. M., Hickson I. D., Borts R. H., Louis E. J. SGS1, a homologue of the Bloom's and Werner's syndrome genes, is required for maintenance of genome stability in Saccharomyces cerevisiae. Genetics. 1996 Nov;144(3):935–945. doi: 10.1093/genetics/144.3.935. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Wilke C. M., Adams J. Fitness effects of Ty transposition in Saccharomyces cerevisiae. Genetics. 1992 May;131(1):31–42. doi: 10.1093/genetics/131.1.31. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Winzeler E. A., Shoemaker D. D., Astromoff A., Liang H., Anderson K., Andre B., Bangham R., Benito R., Boeke J. D., Bussey H. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science. 1999 Aug 6;285(5429):901–906. doi: 10.1126/science.285.5429.901. [DOI] [PubMed] [Google Scholar]
  70. Wotton D., Shore D. A novel Rap1p-interacting factor, Rif2p, cooperates with Rif1p to regulate telomere length in Saccharomyces cerevisiae. Genes Dev. 1997 Mar 15;11(6):748–760. doi: 10.1101/gad.11.6.748. [DOI] [PubMed] [Google Scholar]
  71. Xu H., Boeke J. D. Localization of sequences required in cis for yeast Ty1 element transposition near the long terminal repeats: analysis of mini-Ty1 elements. Mol Cell Biol. 1990 Jun;10(6):2695–2702. doi: 10.1128/mcb.10.6.2695. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES