Ume6 is required for the MATa/MATα cellular identity and transcriptional silencing in Kluyveromyces lactis

Genetics

Volumn 184, Issue 4, 2010, Pages 999-1011

  Barsoum, E ^a   Sjostrand J O O ^a   Astrom S U ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR SIN3A; BACTERIAL PROTEIN; FUNGAL PROTEIN; REPRESSOR PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN; SIR2 PROTEIN, KLUYVEROMYCES LACTIS; SIRTUIN; UME6 PROTEIN, S CEREVISIAE;

ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; GENE CONTROL; GENE DELETION; GENE EXPRESSION; GENE MUTATION; GENE REPRESSION; GENE SILENCING; KLUYVEROMYCES LACTIS; MATING TYPE; MEIOSIS; NONHUMAN; POLYPLOIDY; PRIORITY JOURNAL; UNSCHEDULED MEIOTIC GENE EXPRESSION 6; YEAST; AMINO ACID SEQUENCE; BACTERIAL SPORE; CHEMISTRY; CYTOLOGY; FERTILITY; GENE EXPRESSION REGULATION; GENE LOCUS; GENETIC TRANSCRIPTION; GENETICS; HAPLOIDY; INFERTILITY; KLUYVEROMYCES; METABOLISM; MOLECULAR GENETICS; MUTATION; PHYSIOLOGY;

KLUYVEROMYCES LACTIS; SACCHAROMYCETALES;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; FERTILITY; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GENE SILENCING; GENETIC LOCI; HAPLOIDY; INFERTILITY; KLUYVEROMYCES; MEIOSIS; MOLECULAR SEQUENCE DATA; MUTATION; REPRESSOR PROTEINS; SACCHAROMYCES CEREVISIAE PROTEINS; SIRTUINS; SPORES, BACTERIAL; TRANSCRIPTION, GENETIC;

EID: 77955879115     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.110.114678     Document Type: Article

References (61)

1. ANDERSON, S. F., C. M. STEBER, R. E. ESPOSITO and J. E. COLEMAN, 1995 UME6, a negative regulator of meiosis in Saccharomyces cerevisiae, contains a C-terminal Zn2Cys6 binuclear cluster that binds the URS1 DNA sequence in a zinc-dependent manner. Protein Sci. 4: 1832-1843.
2. ÅSTRÖM, S. U., and J. RINE, 1998 Theme and variation among silencing proteins in Saccharomyces cerevisiae and Kluyveromyces lactis. Genetics 148: 1021-1029.
3. ÅSTRÖM, S. U., A. KEGEL, J. O. SJOSTRAND and J. RINE, 2000 Kluyveromyces lactis Sir2p regulates cation sensitivity and maintains a specialized chromatin structure at the cryptic α-locus. Genetics 156: 81-91.
4. AUSUBEL, F. M., 1999 Short Protocols in Molecular Biology: A Compendium of Methods From Current Protocols in Molecular Biology. John Wiley & Sons, New York.
5. BAHLER, J., J. Q. WU, M. S. LONGTINE, N. G. SHAH, A. MCKENZIE, III et al., 1998 Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast 14: 943-951.
6. BARSOUM, E., P. MARTINEZ and S. U. Åström, 2010 Alpha3, a transposable element that promotes host sexual reproduction. Genes Dev. 24: 33-44.
7. BRAND, A. H., G. MICKLEM and K. NASMYTH, 1987 A yeast silencer contains sequences that can promote autonomous plasmid replication and transcriptional activation. Cell 51: 709-719.
8. BUCKINGHAM, L. E., H. T. WANG, R. T. ELDER, R. M. MCCARROLL, M. R. SLATER et al., 1990 Nucleotide sequence and promoter analysis of SPO13, a meiosis-specific gene of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 87: 9406-9410.
9. CARROZZA, M. J., L. FLORENS, S. K. SWANSON, W. J. SHIA, S. ANDERSON et al., 2005 Stable incorporation of sequence specific repressors Ash1 and Ume6 into the Rpd3L complex. Biochim. Biophys. Acta 1731: 77-87; discussion 75-76.
10. CHEN, X. J., and G. D. CLARK-WALKER, 1994 sir2 mutants of Kluyveromyces lactis are hypersensitive to DNA-targeting drugs. Mol. Cell. Biol. 14: 4501-4508.
11. CLIFTEN, P., P. SUDARSANAM, A. DESIKAN, L. FULTON, B. FULTON et al., 2003 Finding functional features in Saccharomyces genomes by phylogenetic footprinting. Science 301: 71-76.
12. COCKELL, M., F. PALLADINO, T. LAROCHE, G. KYRION, C. LIU et al., 1995 The carboxy termini of Sir4 and Rap1 affect Sir3 localization: evidence for a multicomponent complex required for yeast telomeric silencing. J. Cell Biol. 129: 909-924.
13. ENGEBRECHT, J., and G. S. ROEDER, 1990 MER1, a yeast gene required for chromosome pairing and genetic recombination, is induced in meiosis. Mol. Cell. Biol. 10: 2379-2389.
14. FABRE, E., H. MULLER, P. THERIZOLS, I. LAFONTAINE, B. DUJON et al., 2005 Comparative genomics in hemiascomycete yeasts: evolution of sex, silencing, and subtelomeres. Mol. Biol. Evol. 22: 856-873.
15. GALGOCZY, D. J., A. CASSIDY-STONE, M. LLINAS, S. M. O'ROURKE, I. HERSKOWITZ et al., 2004 Genomic dissection of the cell-type-specification circuit in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 101: 18069-18074.
16. GARDNER, K. A., AND C. A. FOX, 2001 The Sir1 protein's association with a silenced chromosome domain. Genes Dev. 15: 147-157.
17. GELLI, A., 2002 Rst1 and Rst2 are required for the a/alpha diploid cell type in yeast. Mol. Microbiol. 46: 845-854.
18. GHIDELLI, S., D. DONZE, N. DHILLON and R. T. KAMAKAKA, 2001 Sir2p exists in two nucleosome-binding complexes with distinct deacetylase activities. EMBO J. 20: 4522-4535.
19. GOLDMARK, J. P., T. G. FAZZIO, P. W. ESTEP, G. M. CHURCH and T. TSUKIYAMA, 2000 The Isw2 chromatin remodeling complex represses early meiotic genes upon recruitment by Ume6p. Cell 103: 423-433.
20. GOLDSTEIN, A. L., and J. H. MCCUSKER, 1999 Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15: 1541-1553.
21. HECHT, A., T. LAROCHE, S. STRAHL-BOLSINGER, S. M. GASSER and M. GRUNSTEIN, 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.
22. HECHT, A., S. STRAHL-BOLSINGER and M. GRUNSTEIN, 1996 Spreading of transcriptional repressor SIR3 from telomeric heterochromatin. Nature 383: 92-96.
23. HERSKOWITZ, I., 1988 Life cycle of the budding yeast Saccharomyces cerevisiae. Microbiol. Rev. 52: 536-553.
24. HICKMAN, M. A., and L. N. RUSCHE, 2009 The Sir2-Sum1 complex represses transcription using both promoter-specific and longrange mechanisms to regulate cell identity and sexual cycle in the yeast Kluyveromyces lactis. PLoS Genet. 5: e1000710.
25. IMAI, S., C. M. ARMSTRONG, M. KAEBERLEIN and L. GUARENTE, 2000 Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature 403: 795-800. (Pubitemid 30111843)
26. KADOSH, D., and K. STRUHL, 1997 Repression by Ume6 involves recruitment of a complex containing Sin3 corepressor and Rpd3 histone deacetylase to target promoters. Cell 89: 365-371.
27. KADOSH, D., and K. STRUHL, 1998 Targeted recruitment of the Sin3- Rpd3 histone deacetylase complex generates a highly localized domain of repressed chromatin in vivo. Mol. Cell. Biol. 18: 5121-5127.
28. KAWASAKI, L., A. L. SAVINON-TEJEDA, L. ONGAY-LARIOS, J. RAMIREZ and R. CORIA, 2005 The Gbeta(KlSte4p) subunit of the heterotrimeric G protein has a positive and essential role in the induction of mating in the yeast Kluyveromyces lactis. Yeast 22: 947-956.
29. KEGEL, A., P. MARTINEZ, S. D. CARTER and S. U. ÅSTRÖM, 2006 Genome wide distribution of illegitimate recombination events in Kluyveromyces lactis. Nucleic Acids Res. 34: 1633-1645.
30. KELLIS, M., N. PATTERSON, M. ENDRIZZI, B. BIRREN and E. S. LANDER, 2003 Sequencing and comparison of yeast species to identify genes and regulatory elements. Nature 423: 241-254.
31. KELLIS, M., B. W. BIRREN and E. S. LANDER, 2004 Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae. Nature 428: 617-624.
32. LANDRY, J., A. SUTTON, S. T. TAFROV, R. C. HELLER, J. STEBBINS et al., 2000 The silencing protein SIR2 and its homologs are NAD-dependent protein deacetylases. Proc. Natl. Acad. Sci. USA 97: 5807-5811.
33. LAURENSON, P., AND J. RINE, 1991 SUM1-1: a suppressor of silencing defects in Saccharomyces cerevisiae. Genetics 129: 685-696.
34. LEVINE, M., and R. TJIAN, 2003 Transcription regulation and animal diversity. Nature 424: 147-151.
35. LIVI, G. P., J. B. HICKS and A. J. KLAR, 1990 The sum1-1 mutation affects silent mating-type gene transcription in Saccharomyces cerevisiae. Mol. Cell. Biol. 10: 409-412.
36. MALATHI, K., Y. XIAO and A. P. MITCHELL, 1997 Interaction of yeast repressor-activator protein Ume6p with glycogen synthase kinase 3 homolog Rim11p. Mol. Cell. Biol. 17: 7230-7236.
37. MALLORY, M. J., K. F. COOPER and R. STRICH, 2007 Meiosis-specific destruction of the Ume6p repressor by the Cdc20-directed APC/ C. Mol. Cell 27: 951-961.
38. MOAZED, D., A. KISTLER, A. AXELROD, J. RINE and A. D. JOHNSON, 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. Natl. Acad. Sci. USA 94: 2186-2191.
39. MORETTI, P., K. FREEMAN, L. COODLY and D. SHORE, 1994 Evidence that a complex of SIR proteins interacts with the silencer and telomere-binding protein RAP1. Genes Dev. 8: 2257-2269.
40. OLSON, K. A., C. NELSON, G. TAI, W. HUNG, C. YONG et al., 2000 Two regulators of Ste12p inhibit pheromone-responsive transcription by separate mechanisms. Mol. Cell. Biol. 20: 4199-4209.
41. RINE, J., and I. HERSKOWITZ, 1987 Four genes responsible for a position effect on expression from HML and HMR in Saccharomyces cerevisiae. Genetics 116: 9-22.
42. ROTHSTEIN, R. J., 1983 One-step gene disruption in yeast. Methods Enzymol. 101: 202-211.
43. RUBIN-BEJERANO, I., S. MANDEL, K. ROBZYK and Y. KASSIR, 1996 Induction of meiosis in Saccharomyces cerevisiae depends on conversion of the transcriptional represssor Ume6 to a positive regulator by its regulated association with the transcriptional activator Ime1. Mol. Cell. Biol. 16: 2518-2526.
44. RUNDLETT, S. E., A. A. CARMEN, N. SUKA, B. M. TURNER and M. GRUNSTEIN, 1998 Transcriptional repression by UME6 involves deacetylation of lysine 5 of histone H4 by RPD3. Nature 392: 831-835. (Pubitemid 28225326)
45. RUSCHE, L. N., A. L. KIRCHMAIER and J. RINE, 2002 Ordered nucleation and spreading of silenced chromatin in Saccharomyces cerevisiae. Mol. Biol. Cell 13: 2207-2222.
46. RUSCHE, L. N., A. L. KIRCHMAIER and J. RINE, 2003 The establishment, inheritance, and function of silenced chromatin in Saccharomyces cerevisiae. Annu. Rev. Biochem. 72: 481-516.
47. SCHIESTL, R. H., and R. D. GIETZ, 1989 High efficiency transformation of intact yeast cells using single stranded nucleic acids as a carrier. Curr. Genet. 16: 339-346.
48. SHORE, D., and K. NASMYTH, 1987 Purification and cloning of a DNA binding protein from yeast that binds to both silencer and activator elements. Cell 51: 721-732.
49. SJÖSTRAND, J. O., A. KEGEL and S. U. ÅSTRÖM, 2002 Functional diversity of silencers in budding yeasts. Eukaryot. Cell 1: 548-557.
50. SMITH, J. S., C. B. BRACHMANN, I. CELIC, M. A. KENNA, S. MUHAMMAD et al., 2000 A phylogenetically conserved NAD+-dependent protein deacetylase activity in the Sir2 protein family. Proc. Natl. Acad. Sci. USA 97: 6658-6663.
51. STEBER, C. M., and R. E. ESPOSITO, 1995 UME6 is a central component of a developmental regulatory switch controlling meiosis-specific gene expression. Proc. Natl. Acad. Sci. USA 92: 12490-12494.
52. STRICH, R., R. T. SUROSKY, C. STEBER, E. DUBOIS, F. MESSENGUY et al., 1994 UME6 is a key regulator of nitrogen repression and meiotic development. Genes Dev. 8: 796-810.
53. TEYTELMAN, L., M. B. EISEN and J. RINE, 2008 Silent but not static: accelerated base-pair substitution in silenced chromatin of budding yeasts. PLoS Genet. 4: e1000247.
54. TRIOLO, T., and R. STERNGLANZ, 1996 Role of interactions between the origin recognition complex and SIR1 in transcriptional silencing. Nature 381: 251-253.
55. TSONG, A. E., M. G. MILLER, R. M. RAISNER and A. D. JOHNSON, 2003 Evolution of a combinatorial transcriptional circuit: a case study in yeasts. Cell 115: 389-399.
56. TSONG, A. E., B. B. TUCH, H. LI and A. D. JOHNSON, 2006 Evolution of alternative transcriptional circuits with identical logic. Nature 443: 415-420.
57. WASHBURN, B. K., and R. E. ESPOSITO, 2001 Identification of the Sin3-binding site in Ume6 defines a two-step process for conversion of Ume6 from a transcriptional repressor to an activator in yeast. Mol. Cell. Biol. 21: 2057-2069.
58. WHITEWAY, M., L. HOUGAN, D. DIGNARD, D. Y. THOMAS, L. BELL et al., 1989 The STE4 and STE18 genes of yeast encode potential beta and gamma subunits of the mating factor receptor-coupled G protein. Cell 56: 467-477.
59. WILLIAMS, R. M., M. PRIMIG, B. K. WASHBURN, E. A. WINZELER, M. BELLIS et al., 2002 The Ume6 regulon coordinates metabolic and meiotic gene expression in yeast. Proc. Natl. Acad. Sci. USA 99: 13431-13436.
60. XIAO, Y., and A. P. MITCHELL, 2000 Shared roles of yeast glycogen synthase kinase 3 family members in nitrogen-responsive phosphorylation of meiotic regulator Ume6p. Mol. Cell. Biol. 20: 5447-5453.
61. XU, L., M. AJIMURA, R. PADMORE, C. KLEIN and N. KLECKNER, 1995 NDT80, a meiosis-specific gene required for exit from pachytene in Saccharomyces cerevisiae. Mol. Cell. Biol. 15: 6572-6581.