Reinventing heterochromatin in budding yeasts: Sir2 and the origin recognition complex take center stage

Eukaryotic Cell

Volumn 10, Issue 9, 2011, Pages 1183-1192

  Hickman, Meleah A ^b   Froyd, Cara A ^a   Rusche, Laura N ^a  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HETEROCHROMATIN SPECIFIC NONHISTONE CHROMOSOMAL PROTEIN HP 1; HETEROCHROMATIN-SPECIFIC NONHISTONE CHROMOSOMAL PROTEIN HP-1; NONHISTONE PROTEIN; ORIGIN RECOGNITION COMPLEX; SILENT INFORMATION REGULATOR PROTEIN; SIR2 PROTEIN, S CEREVISIAE; SIRTUIN 2;

GENE DUPLICATION; GENE SILENCING; GENETICS; HETEROCHROMATIN; METABOLISM; REVIEW; SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES; SCHIZOSACCHAROMYCES;

CHROMOSOMAL PROTEINS, NON-HISTONE; GENE DUPLICATION; GENE SILENCING; HETEROCHROMATIN; ORIGIN RECOGNITION COMPLEX; SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES; SCHIZOSACCHAROMYCES; SILENT INFORMATION REGULATOR PROTEINS, SACCHAROMYCES CEREVISIAE; SIRTUIN 2;

ANIMALIA; FUNGI; SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES; SCHIZOSACCHAROMYCES POMBE;

EID: 80052355543     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.05123-11     Document Type: Review

References (118)

1. Aguilaniu, H., L. Gustafsson, M. Rigoulet, and T. Nystrom. 2003. Asymmetric inheritance of oxidatively damaged proteins during cytokinesis. Science 299:1751-1753.
2. Alsford, S., T. Kawahara, C. Isamah, and D. Horn. 2007. A sirtuin in the African trypanosome is involved in both DNA repair and telomeric gene silencing but is not required for antigenic variation. Mol. Microbiol. 63: 724-736.
3. Ansari, A., and M. R. Gartenberg. 1997. The yeast silent information regulator Sir4p anchors and partitions plasmids. Mol. Cell. Biol. 17:7061-7068.
4. Astrom, S. U., T. W. Cline, and J. Rine. 2003. The Drosophila melanogaster sir2' gene is nonessential and has only minor effects on position-effect variegation. Genetics 163:931-937.
5. Astrom, 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 alpha-locus. Genetics 156:81-91.
6. Astrom, S. U., and J. Rine. 1998. Theme and variation among silencing proteins in Saccharomyces cerevisiae and Kluyveromyces lactis. Genetics 148:1021-1029.
7. Auth, T., E. Kunkel, and F. Grummt. 2006. Interaction between HP1alpha and replication proteins in mammalian cells. Exp. Cell Res. 312:3349-3359.
8. Barsoum, E., P. Martinez, and S. U. Astrom. 2010. Alpha3, a transposable element that promotes host sexual reproduction. Genes Dev. 24:33-44.
9. Barsoum, E., J. O. Sjostrand, and S. U. Astrom. 2010. Ume6 is required for the MATa/MATalpha-cellular identity and transcriptional silencing in Kluyveromyces lactis. Genetics 184:999-1011.
10. Baum, M., K. Sanyal, P. K. Mishra, N. Thaler, and J. Carbon. 2006. Formation of functional centromeric chromatin is specified epigenetically in Candida albicans. Proc. Natl. Acad. Sci. U. S. A. 103:14877-14882.
11. Bedalov, A., M. Hirao, J. Posakony, M. Nelson, and J. A. Simon. 2003. NAD+-dependent deacetylase Hst1p controls biosynthesis and cellular NAD+ levels in Saccharomyces cerevisiae. Mol. Cell. Biol. 23:7044-7054.
12. Bell, S. P., J. Mitchell, J. Leber, R. Kobayashi, and B. Stillman. 1995. The multidomain structure of Orc1p reveals similarity to regulators of DNA replication and transcriptional silencing. Cell 83:563-568.
13. Booth, L. N., B. B. Tuch, and A. D. Johnson. 2010. Intercalation of a new tier of transcription regulation into an ancient circuit. Nature 468:959-963.
14. Bose, M. E., et al. 2004. The Origin Recognition Complex and Sir4 protein recruit Sir1p to yeast silent chromatin through independent interactions requiring a common Sir1p domain. Mol. Cell. Biol. 24:774-786.
15. Brachmann, C. B., et al. 1995. The SIR2 gene family, conserved from bacteria to humans, functions in silencing, cell cycle progression, and chromosome stability. Genes Dev. 9:2888-2902.
16. Buchberger, J. R., et al. 2008. Sir3-nucleosome interactions in spreading of silent chromatin in Saccharomyces cerevisiae. Mol. Cell. Biol. 28:6903-6918.
17. Butler, G., et al. 2004. Evolution of the MAT locus and its Ho endonuclease in yeast species. Proc. Natl. Acad. Sci. U. S. A. 101:1632-1637.
18. Butler, G., et al. 2009. Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature 459:657-662.
19. Byrne, K. P., and K. H. Wolfe. 2005. The Yeast Gene Order Browser: combining curated homology and syntenic context reveals gene fate in polyploid species. Genome Res. 15:1456-1461.
20. Carmen, A. A., L. Milne, and M. Grunstein. 2002. Acetylation of the yeast histone H4 N terminus regulates its binding to heterochromatin protein SIR3. J. Biol. Chem. 277:4778-4781.
21. Castano, I., et al. 2005. Telomere length control and transcriptional regulation of subtelomeric adhesins in Candida glabrata. Mol. Microbiol. 55: 1246-1258.
22. Chang, J. F., et al. 2003. Structure of the coiled-coil dimerization motif of Sir4 and its interaction with Sir3. Structure 11:637-649.
23. 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.
24. Conant, G. C., and K. H. Wolfe. 2008. Turning a hobby into a job: how duplicated genes find new functions. Nat. Rev. Genet. 9:938-950.
25. Connelly, J. J., et al. 2006. Structure and function of the Saccharomyces cerevisiae Sir3 BAH domain. Mol. Cell. Biol. 26:3256-3265.
26. De Las Penas, A., et al. 2003. Virulence-related surface glycoproteins in the yeast pathogen Candida glabrata are encoded in subtelomeric clusters and subject to RAP1-and SIR-dependent transcriptional silencing. Genes Dev. 17:2245-2258.
27. Deng, Z., J. Dheekollu, D. Broccoli, A. Dutta, and P. M. Lieberman. 2007. The origin recognition complex localizes to telomere repeats and prevents telomere-circle formation. Curr. Biol. 17:1989-1995.
28. Dietrich, F. S., et al. 2004. The Ashbya gossypii genome as a tool for mapping the ancient Saccharomyces cerevisiae genome. Science 304:304-307.
29. Di Rienzi, S. C., et al. 2011. Genetic, genomic, and molecular tools for studying the protoploid yeast, L. waltii. Yeast 28:137-151.
30. Domergue, R., et al. 2005. Nicotinic acid limitation regulates silencing of Candida adhesins during UTI. Science 308:866-870.
31. Drinnenberg, I. A., et al. 2009. RNAi in budding yeast. Science 326:544-550.
32. Dujon, B. 2005. Hemiascomycetous yeasts at the forefront of comparative genomics. Curr. Opin. Genet. Dev. 15:614-620.
33. Dujon, B. 2006. Yeasts illustrate the molecular mechanisms of eukaryotic genome evolution. Trends Genet. 22:375-387.
34. Duraisingh, M. T., et al. 2005. Heterochromatin silencing and locus repositioning linked to regulation of virulence genes in Plasmodium falciparum. Cell 121:13-24.
35. Enomoto, S., S. D. Johnston, and J. Berman. 2000. Identification of a novel allele of SIR3 defective in the maintenance, but not the establishment, of silencing in Saccharomyces cerevisiae. Genetics 155:523-538.
36. Fabre, E., et al. 2005. Comparative genomics in hemiascomycete yeasts: evolution of sex, silencing, and subtelomeres. Mol. Biol. Evol. 22:856-873.
37. Fidel, P. L., Jr., J. A. Vazquez, and J. D. Sobel. 1999. Candida glabrata: review of epidemiology, pathogenesis, and clinical disease with comparison to C. albicans. Clin. Microbiol. Rev. 12:80-96.
38. Force, A., et al. 1999. Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531-1545.
39. Freeman-Cook, L. L., et al. 2005. Conserved locus-specific silencing functions of Schizosaccharomyces pombe sir2+. Genetics 169:1243-1260.
40. Freitas-Junior, L. H., et al. 2005. Telomeric heterochromatin propagation and histone acetylation control mutually exclusive expression of antigenic variation genes in malaria parasites. Cell 121:25-36.
41. Froyd, C. A., and L. N. Rusche. 2011. The duplicated deacetylases Sir2 and Hst1 subfunctionalized by acquiring complementary inactivating mutations. Mol. Cell. Biol. 31:3351-3365.
42. Fu, X. H., F. L. Meng, Y. Hu, and J. Q. Zhou. 2008. Candida albicans, a distinctive fungal model for cellular aging study. Aging Cell 7:746-757.
43. Furuyama, T., R. Banerjee, T. R. Breen, and P. J. Harte. 2004. SIR2 is required for polycomb silencing and is associated with an E(Z) histone methyltransferase complex. Curr. Biol. 14:1812-1821.
44. Gallagher, J. E., J. E. Babiarz, L. Teytelman, K. H. Wolfe, and J. Rine. 2009. Elaboration, diversification and regulation of the Sir1 family of silencing proteins in Saccharomyces. Genetics 181:1477-1491.
45. Gardner, K. A., J. Rine, and C. A. Fox. 1999. A region of the Sir1 protein dedicated to recognition of a silencer and required for interaction with the Orc1 protein in Saccharomyces cerevisiae. Genetics 151:31-44.
46. Greig, D. 2009. Reproductive isolation in Saccharomyces. Heredity 102: 39-44.
47. Greiss, S., and A. Gartner. 2009. Sirtuin/Sir2 phylogeny, evolutionary considerations and structural conservation. Mol. Cells 28:407-415.
48. Grewal, S. I., and J. C. Rice. 2004. Regulation of heterochromatin by histone methylation and small RNAs. Curr. Opin. Cell Biol. 16:230-238.
49. Gurevich, R., S. Smolikov, H. Maddar, and A. Krauskopf. 2003. Mutant telomeres inhibit transcriptional silencing at native telomeres of the yeast Kluyveromyces lactis. Mol. Genet. Genomics 268:729-738.
50. Hahn, M. W. 2009. Distinguishing among evolutionary models for the maintenance of gene duplicates. J. Hered. 100:605-617.
51. He, X., and J. Zhang. 2005. Rapid subfunctionalization accompanied by prolonged and substantial neofunctionalization in duplicate gene evolution. Genetics 169:1157-1164.
52. 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.
53. Heckman, D. S., et al. 2001. Molecular evidence for the early colonization of land by fungi and plants. Science 293:1129-1133.
54. Hedges, S. B. 2002. The origin and evolution of model organisms. Nat. Rev. Genet. 3:838-849.
55. Herman, A., and H. Roman. 1966. Allele specific determinants of homothallism in Saccharomyces lactis. Genetics 53:727-740.
56. Hickman, M. A., and L. N. Rusche. 2007. Substitution as a mechanism for genetic robustness: the duplicated deacetylases Hst1p and Sir2p in Saccharomyces cerevisiae. PLoS Genet. 3:e126.
57. Hickman, M. A., and L. N. Rusche. 2009. The Sir2-Sum1 complex represses transcription using both promoter-specific and long-range mechanisms to regulate cell identity and sexual cycle in the yeast Kluyveromyces lactis. PLoS Genet. 5:e1000710.
58. Hickman, M. A., and L. N. Rusche. 2010. Transcriptional silencing functions of the yeast protein Orc1/Sir3 subfunctionalized after gene duplication. Proc. Natl. Acad. Sci. U. S. A. 107:19384-19389.
59. Hnisz, D., T. Schwarzmuller, and K. Kuchler. 2009. Transcriptional loops meet chromatin: a dual-layer network controls white-opaque switching in Candida albicans. Mol. Microbiol. 74:1-15.
60. Hoppe, G. J., et al. 2002. Steps in assembly of silent chromatin in yeast: Sir3-independent binding of a Sir2/Sir4 complex to silencers and role for Sir2-dependent deacetylation. Mol. Cell. Biol. 22:4167-4180.
61. Hou, Z., et al. 2009. Phylogenetic conservation and homology modeling help reveal a novel domain within the budding yeast heterochromatin protein Sir1. Mol. Cell. Biol. 29:687-702.
62. Iraqui, I., et al. 2005. The Yak1p kinase controls expression of adhesins and biofilm formation in Candida glabrata in a Sir4p-dependent pathway. Mol. Microbiol. 55:1259-1271.
63. Kaeberlein, M., M. McVey, and L. Guarente. 1999. The SIR2/3/4 complex and SIR2 alone promote longevity in Saccharomyces cerevisiae by two different mechanisms. Genes Dev. 13:2570-2580.
64. Kaur, R., R. Domergue, M. L. Zupancic, and B. P. Cormack. 2005. A yeast by any other name: Candida glabrata and its interaction with the host. Curr. Opin. Microbiol. 8:378-384.
65. 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.
66. Koren, A., et al. 2010. Epigenetically-inherited centromere and neocentromere DNA replicates earliest in S-phase. PLoS Genet. 6:e1001068.
67. Kurtzman, C. P. 2003. Phylogenetic circumscription of Saccharomyces, Kluyveromyces and other members of the Saccharomycetaceae, and the proposal of the new genera Lachancea, Nakaseomyces, Naumovia, Vanderwaltozyma and Zygotorulaspora. FEMS Yeast Res. 4:233-245.
68. Kurtzman, C. P. 2011. Discussion of teleomorphic and anamorphic ascomycetous yeasts and yeast-like taxa, p. 293-307. In C. P. Kurtzman, J. W. Fell, and T. Boekhout (ed.), The yeasts, a taxonomic study, 5th ed. Elsevier, Amsterdam, The Netherlands.
69. Le, S., C. Davis, J. B. Konopka, and R. Sternglanz. 1997. Two new S-phasespecific genes from Saccharomyces cerevisiae. Yeast 13:1029-1042.
70. Leatherwood, J., and A. Vas. 2003. Connecting ORC and heterochromatin: why? Cell Cycle 2:573-575.
71. Lue, N. F. 2010. Plasticity of telomere maintenance mechanisms in yeast. Trends Biochem. Sci. 35:8-17.
72. Luo, K., M. A. Vega-Palas, and M. Grunstein. 2002. Rap1-Sir4 binding independent of other Sir, yKu, or histone interactions initiates the assembly of telomeric heterochromatin in yeast. Genes Dev. 16:1528-1539.
73. Lynch, D. B., M. E. Logue, G. Butler, and K. H. Wolfe. 2010. Chromosomal G+ C content evolution in yeasts: systematic interspecies differences, and GC-poor troughs at centromeres. Genome Biol. Evol. 2:572-583.
74. Lynch, M., and V. Katju. 2004. The altered evolutionary trajectories of gene duplicates. Trends Genet. 20:544-549.
75. Lynch, P. J., and L. N. Rusche. 2009. A silencer promotes the assembly of silenced chromatin independently of recruitment. Mol. Cell. Biol. 29:43-56.
76. Lynch, P. J., and L. N. Rusche. 2010. An auxiliary silencer and a boundary element maintain high levels of silencing proteins at HMR in Saccharomyces cerevisiae. Genetics 185:113-127.
77. Ma, B., et al. 2009. High-affinity transporters for NAD+ precursors in Candida glabrata are regulated by Hst1 and induced in response to niacin limitation. Mol. Cell. Biol. 29:4067-4079.
78. Mancio-Silva, L., A. P. Rojas-Meza, M. Vargas, A. Scherf, and R. Hernandez-Rivas. 2008. Differential association of Orc1 and Sir2 proteins to telomeric domains in Plasmodium falciparum. J. Cell Sci. 121:2046-2053.
79. Martino, F., et al. 2009. Reconstitution of yeast silent chromatin: multiple contact sites and O-AADPR binding load SIR complexes onto nucleosomes in vitro. Mol. Cell 33:323-334.
80. Mead, J., et al. 2007. Swapping the gene-specific and regional silencing specificities of the Hst1 and Sir2 histone deacetylases. Mol. Cell. Biol. 27:2466-2475.
81. Miller, M. G., and A. D. Johnson. 2002. White-opaque switching in Candida albicans is controlled by mating-type locus homeodomain proteins and allows efficient mating. Cell 110:293-302.
82. 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. U. S. A. 94:2186-2191.
83. 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.
84. Murayama, A., et al. 2008. Epigenetic control of rDNA loci in response to intracellular energy status. Cell 133:627-639.
85. Murphy, G. A., et al. 2003. The Sir4 C-terminal coiled coil is required for telomeric and mating-type silencing in Saccharomyces cerevisiae. J. Mol. Biol. 334:769-780.
86. Nakayashiki, H. 2005. RNA silencing in fungi: mechanisms and applications. FEBS Lett. 579:5950-5957.
87. Newman, B. L., J. R. Lundblad, Y. Chen, and S. M. Smolik. 2002. A Drosophila homologue of Sir2 modifies position-effect variegation but does not affect life span. Genetics 162:1675-1685.
88. Noma, K., et al. 2004. RITS acts in cis to promote RNA interferencemediated transcriptional and post-transcriptional silencing. Nat. Genet. 36:1174-1180.
89. Onishi, M., G.-G. Liou, J. R. Buchberger, T. Walz, and D. Moazed. 2007. Role of the conserved Sir3-BAH domain in nucleosome binding and silent chromatin assembly. Mol. Cell 28:1015-1028.
90. Pak, D. T., et al. 1997. Association of the origin recognition complex with heterochromatin and HP1 in higher eukaryotes. Cell 91:311-323.
91. Park, Y., J. Hanish, and A. J. Lustig. 1998. Sir3p domains involved in the initiation of telomeric silencing in Saccharomyces cerevisiae. Genetics 150: 977-986.
92. Perez-Martin, J., J. A. Uria, and A. D. Johnson. 1999. Phenotypic switching in Candida albicans is controlled by a SIR2 gene. EMBO J. 18:2580-2592.
93. Prasanth, S. G., K. V. Prasanth, K. Siddiqui, D. L. Spector, and B. Stillman. 2004. Human Orc2 localizes to centrosomes, centromeres and heterochromatin during chromosome inheritance. EMBO J. 23:2651-2663.
94. Ramirez-Zavaleta, C. Y., G. E. Salas-Delgado, A. De Las Penas, and I. Castano. 2010. Subtelomeric silencing of the MTL3 locus of Candida glabrata requires yKu70, yKu80, and Rif1 proteins. Eukaryot. Cell 9:1602-1611.
95. Reedy, J. L., A. M. Floyd, and J. Heitman. 2009. Mechanistic plasticity of sexual reproduction and meiosis in the Candida pathogenic species complex. Curr. Biol. 19:891-899.
96. Rosas-Hernandez, L. L., et al. 2008. yKu70/yKu80 and Rif1 regulate silencing differentially at telomeres in Candida glabrata. Eukaryot. Cell 7:2168-2178.
97. Rusche, L. N., and M. A. Hickman. 2007. Evolution of silencing at the mating-type loci in hemiascomycetes, p. 189-200. In J. Heitman, L. Casselton, and J. Kronstand (ed.), Sex in fungi: molecular determination and evolutionary implications. American Society for Microbiology, Washington, DC.
98. 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.
99. 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.
100. Sampath, V., et al. 2009. Mutational analysis of the Sir3 BAH domain reveals multiple points of interaction with nucleosomes. Mol. Cell. Biol. 29:2532-2545.
101. Sanyal, K., M. Baum, and J. Carbon. 2004. Centromeric DNA sequences in the pathogenic yeast Candida albicans are all different and unique. Proc. Natl. Acad. Sci. U. S. A. 101:11374-11379.
102. Sauve, A. A., C. Wolberger, V. L. Schramm, and J. D. Boeke. 2006. The biochemistry of sirtuins. Annu. Rev. Biochem. 75:435-465.
103. Shankaranarayana, G. D., M. R. Motamedi, D. Moazed, and S. I. Grewal. 2003. Sir2 regulates histone H3 lysine 9 methylation and heterochromatin assembly in fission yeast. Curr. Biol. 13:1240-1246.
104. Sharp, J. A., D. C. Krawitz, K. A. Gardner, C. A. Fox, and P. D. Kaufman. 2003. The budding yeast silencing protein Sir1 is a functional component of centromeric chromatin. Genes Dev. 17:2356-2361.
105. Sjostrand, J. O., A. Kegel, and S. U. Astrom. 2002. Functional diversity of silencers in budding yeasts. Eukaryot. Cell 1:548-557.
106. Souciet, J. L., et al. 2009. Comparative genomics of protoploid Saccharomycetaceae. Genome Res. 19:1696-1709.
107. 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.
108. Triolo, T., and R. Sternglanz. 1996. Role of interactions between the origin recognition complex and SIR1 in transcriptional silencing. Nature 381:251-253.
109. van Hoof, A. 2005. Conserved functions of yeast genes support the duplication, degeneration and complementation model for gene duplication. Genetics 171:1455-1461.
110. Vaquero, A. 2009. The conserved role of sirtuins in chromatin regulation. Int. J. Dev. Biol. 53:303-322.
111. Verdel, A., et al. 2004. RNAi-mediated targeting of heterochromatin by the RITS complex. Science 303:672-676.
112. Wolfe, K. H., and D. C. Shields. 1997. Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387:708-713.
113. Wong, S., G. Butler, and K. H. Wolfe. 2002. Gene order evolution and paleopolyploidy in hemiascomycete yeasts. Proc. Natl. Acad. Sci. U. S. A. 99:9272-9277.
114. Wong, S., M. A. Fares, W. Zimmermann, G. Butler, and K. H. Wolfe. 2003. Evidence from comparative genomics for a complete sexual cycle in the 'asexual' pathogenic yeast Candida glabrata. Genome Biol. 4:R10.
115. Xie, J., et al. 1999. Sum1 and Hst1 repress middle sporulation-specific gene expression during mitosis in Saccharomyces cerevisiae. EMBO J. 18:6448-6454.
116. Zhang, Z., M. K. Hayashi, O. Merkel, B. Stillman, and R. M. Xu. 2002. Structure and function of the BAH-containing domain of Orc1p in epigenetic silencing. EMBO J. 21:4600-4611.
117. Zill, O. A., and J. Rine. 2008. Interspecies variation reveals a conserved repressor of alpha-specific genes in Saccharomyces yeasts. Genes Dev. 22: 1704-1716.
118. Zill, O. A., D. Scannell, L. Teytelman, and J. Rine. 2010. Co-evolution of transcriptional silencing proteins and the DNA elements specifying their assembly. PLoS Biol. 8:e1000550.