Chapter 11 : Evolution of Silencing at the Mating-Type Loci in Hemiascomycetes

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This chapter explores how a unique silencing mechanism evolved in the hemiascomycete class of fungi, which includes the model yeast . It reviews what is known about silencing in species related to and explores the origins and development of the unique Sirmediated silencing mechanism. The phylogenetic relationships of the species discussed in this chapter are illustrated. The whole-genome duplication played an important role in the development of Sirmediated silencing. For clarity, in the remainder of this chapter, gene and protein names are preceded by the initials of the genus and species of the host organism. The chapter also explores the evolution of the Sir proteins and then examines the changing nature of the genomic regions most likely to be silenced: silent mating-type cassettes, telomeres, and centromeres. Beyond the hemiascomycetes, SpSir2p contributes to classical silencing at centromeres, telomeres, and mating-type loci in , where it deacetylates H3-K9, thereby promoting methylation of this lysine and the association of SpSwi6. An interesting example of the evolution of Sir2p is the emergence of a new paralog, Hst1p, which arose in the whole-genome duplication. An examination of the distribution of silencing proteins in the hemiascomycete class of fungi, coupled with experimental studies of silencing in a few species, suggests the following speculative model for the evolution of Sirmediated silencing.

Citation: Laura N, Meleah A. 2007. Evolution of Silencing at the Mating-Type Loci in Hemiascomycetes, p 189-200. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch11
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Figure 11.1

Model for Sir-mediated silencing. 1 through 4, Sir1p through Sir4p; ORC, origin recognition complex; R, Rap1p; A, Abf1p; Ac, acetyl group.

Citation: Laura N, Meleah A. 2007. Evolution of Silencing at the Mating-Type Loci in Hemiascomycetes, p 189-200. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch11
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Image of Figure 11.2
Figure 11.2

Relationship of species discussed. The phylogenetic tree is based on the 25S ribosomal DNA sequences, using Mega3.1 software, under the Maximum Parsimony model (500 replicates).

Citation: Laura N, Meleah A. 2007. Evolution of Silencing at the Mating-Type Loci in Hemiascomycetes, p 189-200. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch11
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1. 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: 931937.
2. 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: 8191.
3. Astrom, S. U., and, J. Rine. 1998. Theme and variation among silencing proteins in Saccharomyces cerevisiae and Kluyveromyces lactis. Genetics 148: 10211029.
4. Blander, G., and, L. Guarente. 2004. The Sir2 family of protein deacetylases. Annu. Rev. Biochem. 73: 417435.
5. Brachmann, C. B.,, J. M. Sherman,, S. E. Devine,, E. E. Cameron,, L. Pillus, and, J. D. Boeke. 1995. The SIR2 gene family, conserved from bacteria to humans, functions in silencing, cell cycle progression, and chromosome stability. Genes Dev. 9: 28882902.
6. Brockert, P. J.,, S. A. Lachke,, T. Srikantha,, C. Pujol,, R. Galask, and, D. R. Soll. 2003. Phenotypic switching and mating type switching of Candida glabrata at sites of colonization. Infect. Immun. 71: 71097118.
7. Butler, G.,, C. Kenny,, A. Fagan,, C. Kurischko,, C. Gaillardin, and K. H. Wolfe. 2004. Evolution of the MAT locus and its Ho endonuclease in yeast species. Proc. Natl. Acad. Sci. USA 101: 16321637.
8. 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: 14561461.
9. 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: 47784781.
10. Castano, I.,, S. J. Pan,, M. Zupancic,, C. Hennequin,, B. Dujon, and, B. P. Cormack. 2005. Telomere length control and transcriptional regulation of subtelomeric adhesins in Candida glabrata. Mol. Microbiol. 55: 12461258.
11. Chang, J. F.,, B. E. Hall,, J. C. Tanny,, D. Moazed,, D. Filman, and, T. Ellenberger. 2003. Structure of the coiled-coil dimerization motif of Sir4 and its interaction with Sir3. Structure 11: 637649.
12. Chen, X. J., and, G. D. Clark-Walker. 1994. sir2 mutants of Kluyveromyces lactis are hypersensitive to DNA-targeting drugs. Mol. Cell. Biol. 14: 45014508.
13. Chi, M. H., and, D. Shore. 1996. SUM1-1, a dominant suppressor of SIR mutations in Saccharomyces cerevisiae, increases transcriptional silencing at telomeres and HM mating-type loci and decreases chromosome stability. Mol. Cell. Biol. 16: 42814294.
14. Choo, K. H. 2001. Domain organization at the centromere and neocentromere. Dev. Cell 1: 165177.
15. Coria,, R., L. Kawasaki,, F. Torres-Quiroz,, L. Ongay-Larios,, E. Sanchez-Paredes,, N. Velazquez-Zavala,, R. NavarroOlmos,, M. Rodriguez-Gonzalez,, R. Aguilar-Corachan, and G. Coello. 2006. The pheromone response pathway of Kluyveromyces lactis. FEMS Yeast Res. 6: 336344.
16. De Las Penas, A.,, S. J. Pan,, I. Castano,, J. Alder,, R. Cregg, and, B. P. Cormack. 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: 22452258.
17. Dietrich, F. S.,, S. Voegeli,, S. Brachat,, A. Lerch,, K. Gates,, S. Steiner,, C. Mohr,, R. Pohlmann,, P. Luedi,, S. Choi,, R. A. Wing,, A. Flavier,, T. D. Gaffney, and, P. Philippsen. 2004. The Ashbya gossypii genome as a tool for mapping the ancient Saccharomyces cerevisiae genome. Science 304: 304307.
18. Dodgson, A. R.,, C. Pujol,, M. A. Pfaller,, D. W. Denning, and, D. R. Soll. 2005. Evidence for recombination in Candida glabrata. Fungal Genet. Biol. 42: 233243.
19. Domergue, R.,, I. Castano,, A. De Las Penas,, M. Zupancic,, V. Lockatell,, J. R. Hebel,, D. Johnson, and, B. P. Cormack. 2005. Nicotinic acid limitation regulates silencing of Candida adhesins during UTI. Science 308: 866870.
20. Dujon, B. 2005. Hemiascomycetous yeasts at the forefront of comparative genomics. Curr. Opin. Genet. Dev. 15: 614620.
21. Dujon,, B. 2006. Yeasts illustrate the molecular mechanisms of eukaryotic genome evolution. Trends Genet. 22: 375387.
22. Dujon, B.,, D. Sherman,, G. Fischer,, P. Durrens,, S. Casaregola,, I. Lafontaine,, J. De Montigny,, C. Marck,, C. Neuveglise, E. Talla,, N. Goffard,, L. Frangeul,, M. Aigle,, V. Anthouard,, A. Babour,, V. Barbe,, S. Barnay,, S. Blanchin,, J. M. Beckerich,, E. Beyne,, C. Bleykasten,, A. Boisrame,, J. Boyer,, L. Cattolico,, F. Confanioleri,, A. De Daruvar,, L. Despons,, E. Fabre,, C. Fairhead,, H. Ferry-Dumazet,, A. Groppi,, F. Hantraye,, C. Hennequin,, N. Jauniaux,, P. Joyet,, R. Kachouri,, A. Kerrest,, R. Koszul,, M. Lemaire,, I. Lesur,, L. Ma,, H. Muller,, J. M. Nicaud,, M. Nikolski,, S. Oztas,, O. Ozier-Kalogeropoulos,, S. Pellenz,, S. Potier,, G. F. Richard,, M. L. Straub,, A. Suleau,, D. Swennen,, F. Tekaia,, M. WesolowskiLouvel,, E. Westhof,, B. Wirth,, M. Zeniou-Meyer,, I. Zivanovic,, M. Bolotin-Fukuhara,, A. Thierry,, C. Bouchier,, B. Caudron,, C. Scarpelli,, C. Gaillardin,, J. Weissenbach,, P. Wincker, and, J. L. Souciet. 2004. Genome evolution in yeasts. Nature 430: 3544.
23. Ekwall, K.,, J. P. Javerzat,, A. Lorentz,, H. Schmidt,, G. Cranston, and, R. Allshire. 1995. The chromodomain protein Swi6: a key component at fission yeast centromeres. Science 269: 14291431.
24. Fabre, E.,, H. Muller,, P. Therizols,, I. Lafontaine,, B. Dujon, and, C. Fairhead. 2005. Comparative genomics in hemiascomycete yeasts: evolution of sex, silencing, and subtelomeres. Mol. Biol. Evol. 22: 856873.
25. 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: 8096.
26. Freeman-Cook, L. L.,, E. B. Gomez,, E. J. Spedale,, J. Marlett,, S. L. Forsburg,, L. Pillus, and, P. Laurenson. 2005. Conserved locus-specific silencing functions of Schizosaccharomyces pombe sir2+. Genetics 169: 12431260.
27. 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: 18121821.
28. 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: 45224535.
29. Gottlieb, S., and, R. E. Esposito. 1989. A new role for a yeast transcriptional silencer gene, SIR2, in regulation of recombination in ribosomal DNA. Cell 56: 771776.
30. Gottschling, D. E.,, O. M. Aparicio,, B. L. Billington, and, V. A. Zakian. 1990. Position effect at S. cerevisiae telomeres: reversible repression of Pol II transcription. Cell 63: 751762.
31. Grewal, S. I., and, J. C. Rice. 2004. Regulation of heterochromatin by histone methylation and small RNAs. Curr. Opin. Cell Biol. 16: 230238.
32. 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: 729738.
33. Hansen, K. R.,, P. T. Ibarra, and, G. Thon. 2006. Evolutionary-conserved telomere-linked helicase genes of fission yeast are repressed by silencing factors, RNAi components and the telomere-binding protein Taz1. Nucleic Acids Res. 34: 7888.
34. 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: 583592.
35. Hedges, S. B. 2002. The origin and evolution of model organisms. Nat. Rev. Genet. 3: 838849.
36. Herman,, A., and H. Roman. 1966. Allele specific determinants of homothallism in Saccharomyces lactis. Genetics 53: 727740.
37. Hoppe, G. J.,, J. C. Tanny,, A. D. Rudner,, S. A. Gerber,, S. Danaie,, S. P. Gygi, and, D. Moazed. 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: 41674180.
38. Iraqui, I.,, S. Garcia-Sanchez,, S. Aubert,, F. Dromer,, J. M. Ghigo,, C. d’Enfert, and G. Janbon. 2005. The Yak1p kinase controls expression of adhesins and biofilm formation in Candida glabrata in a Sir4p-dependent pathway. Mol. Microbiol. 55: 12591271.
39. Jia, S.,, K. Noma, and, S. I. Grewal. 2004. RNAi-independent heterochromatin nucleation by the stress-activated ATF/CREB family proteins. Science 304: 19711976.
40. Kanoh, J.,, M. Sadaie,, T. Urano, and, F. Ishikawa. 2005. Telomere binding protein Taz1 establishes Swi6 heterochromatin independently of RNAi at telomeres. Curr. Biol. 15: 18081819.
41. 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: 378384.
42. 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: 617624.
43. Kim, H. S.,, E. S. Choi,, J. A. Shin,, Y. K. Jang, and, S. D. Park. 2004. Regulation of Swi6/HP1-dependent heterochromatin assembly by cooperation of components of the mitogen-activated protein kinase pathway and a histone deacetylase clr6. J. Biol. Chem. 279: 4285042859.
44. Klar, A. J.,, S. N. Kakar,, J. M. Ivy,, J. B. Hicks,, G. P. Livi, and, L. M. Miglio. 1985. SUM1, an apparent positive regulator of the cryptic mating-type loci in Saccharomyces cerevisiae. Genetics 111: 745758.
45. Kyrion, G.,, K. Liu,, C. Liu, and, A. J. Lustig. 1993. RAP1 and telomere structure regulate telomere position effects in Saccharomyces cerevisiae. Genes Dev. 7: 11461159.
46. Longtine, M. S.,, N. M. Wilson,, M. E. Petracek, and, J. Berman. 1989. A yeast telomere binding activity binds to two related telomere sequence motifs and is indistinguishable from RAP1. Curr. Genet. 16: 225239.
47. 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: 15281539.
48. Lynch, P. J.,, H. B. Fraser,, E. Sevastopoulos,, J. Rine, and, L. N. Rusche. 2005. Sum1p, the origin recognition complex, and the spreading of a promoter-specific repressor in Saccharomyces cerevisiae. Mol. Cell. Biol. 25: 59205932.
49. McCord, R.,, M. Pierce,, J. Xie,, S. Wonkatal,, C. Mickel, and, A. K. Vershon. 2003. Rfm1, a novel tethering factor required to recruit the Hst1 histone deacetylase for repression of middle sporulation genes. Mol. Cell. Biol. 23: 20092016.
50. Mishra, K., and, D. Shore. 1999. Yeast Ku protein plays a direct role in telomeric silencing and counteracts inhibition by rif proteins. Curr. Biol. 9: 11231126.
51. 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: 21862191.
52. Murphy, G. A.,, E. J. Spedale,, S. T. Powell,, L. Pillus,, S. C. Schultz, and, L. Chen. 2003. The Sir4 C-terminal coiled coil is required for telomeric and mating type silencing in Saccharomyces cerevisiae. J. Mol. Biol. 334: 769780.
53. Nakayashiki, H. 2005. RNA silencing in fungi: mechanisms and applications. FEBS Lett. 579: 59505957.
54. 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: 16751685.
55. Noma, K.,, T. Sugiyama,, H. Cam,, A. Verdel,, M. Zofall,, S. Jia,, D. Moazed, and, S. I. Grewal. 2004. RITS acts in cis to promote RNA interference-mediated transcriptional and post-transcriptional silencing. Nat. Genet. 36: 11741180.
56. Pappas, D. L., Jr., R. Frisch, and M. Weinreich. 2004. The NAD(+)-dependent Sir2p histone deacetylase is a negative regulator of chromosomal DNA replication. Genes Dev. 18: 769781.
57. 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: 25802592.
58. Pfaller, M. A.,, R. N. Jones,, S. A. Messer,, M. B. Edmond, and, R. P. Wenzel. 1998. National surveillance of nosocomial blood stream infection due to species of Candida other than Candida albicans: frequency of occurrence and antifungal susceptibility in the SCOPE Program. Diagn. Microbiol. Infect. Dis. 30: 121129.
59. Roy, R.,, B. Meier,, A. D. McAinsh,, H. M. Feldmann, and, S. P. Jackson. 2004. Separation-of-function mutants of yeast Ku80 reveal a Yku80p-Sir4p interaction involved in telomeric silencing. J. Biol. Chem. 279: 8694.
60. 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: 481516.
61. Rusche, L. N.,, A. L. Kirchmaier, and, J. Rine. 2002. Ordered nucleation and spreading of silenced chromatin in Saccharomyces cerevisiae. Mol. Biol. Cell 13: 22072222.
62. Rusche, L. N., and, J. Rine. 2001. Conversion of a gene-specific repressor to a regional silencer. Genes Dev. 15: 955967.
63. 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. USA 101: 1137411379.
64. Selmecki, A.,, A. Forche, and, J. Berman. 2006. Aneuploidy and isochromosome formation in drug-resistant Candida albicans. Science 313: 367370.
65. 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: 12401246.
66. 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: 23562361.
67. Sjostrand, J. O.,, A. Kegel, and, S. U. Astrom. 2002. Functional diversity of silencers in budding yeasts. Eukaryot. Cell 1: 548557.
68. Smith, J. S., and, J. D. Boeke. 1997. An unusual form of transcriptional silencing in yeast ribosomal DNA. Genes Dev. 11: 241254.
69. Smith, J. S.,, E. Caputo, and, J. D. Boeke. 1999. A genetic screen for ribosomal DNA silencing defects identifies multiple DNA replication and chromatin-modulating factors. Mol. Cell. Biol. 19: 31843197.
70. Srikantha, T.,, S. A. Lachke, and, D. R. Soll. 2003. Three mating type-like loci in Candida glabrata. Eukaryot. Cell 2: 328340.
71. Strahl-Bolsinger, S.,, A. Hecht,, K. Luo, and, M. Grunstein. 1997. SIR2 and SIR4 interactions differ in core and extended telomeric heterochromatin in yeast. Genes Dev. 11: 8393.
72. Sutton, A.,, R. C. Heller,, J. Landry,, J. S. Choy,, A. Sirko, and, R. Sternglanz. 2001. A novel form of transcriptional silencing by Sum1-1 requires Hst1 and the origin recognition complex. Mol. Cell. Biol. 21: 35143522.
73. Triolo, T., and, R. Sternglanz. 1996. Role of interactions between the origin recognition complex and SIR1 in transcriptional silencing. Nature 381: 251253.
74. van Hoof, A. 2005. Conserved functions of yeast genes support the duplication, degeneration and complementation model for gene duplication. Genetics 171: 14551461.
75. Verdel, A.,, S. Jia,, S. Gerber,, T. Sugiyama,, S. Gygi,, S. I. Grewal, and, D. Moazed. 2004. RNAi-mediated targeting of heterochromatin by the RITS complex. Science 303: 672676.
76. Wolfe, K. H., and, D. C. Shields. 1997. Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387: 708713.
77. Wong, S.,, G. Butler, and, K. H. Wolfe. 2002. Gene order evolution and paleopolyploidy in hemiascomycete yeasts. Proc. Natl. Acad. Sci. USA 99: 92729277.
78. 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.
79. Xie, J.,, M. Pierce,, V. Gailus-Durner,, M. Wagner,, E. Winter, and, A. K. Vershon. 1999. Sum1 and Hst1 repress middle sporulation-specific gene expression during mitosis in Saccharomyces cerevisiae. EMBO J. 18: 64486454.

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