The histone chaperone ASF1 is essential for sexual development in the filamentous fungus Sordaria macrospora

Molecular Microbiology

Volumn 84, Issue 4, 2012, Pages 748-765

  Gesing, Stefan ^a   Schindler, Daniel ^a   Fränzel, Benjamin ^a   Wolters, Dirk ^a   Nowrousian, Minou ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTI SILENCING FUNCTION 1 PROTEIN; CHAPERONE; EPIDERMAL GROWTH FACTOR; HISTONE H3; HISTONE H4; HYBRID PROTEIN; PROTEIN ASF1; UNCLASSIFIED DRUG;

ANALYTIC METHOD; ARTICLE; ASCOMYCETES; CAC2 GENE; CELL NUCLEUS; CONTROLLED STUDY; DELETION MUTANT; DEVELOPMENTAL GENE; FERTILITY; FRUITING BODY; FUNGAL DEVELOPMENT; FUSARIUM GRAMINEARUM; GENE DELETION; GENE EXPRESSION; GENETIC CODE; GENETIC CONSERVATION; GENETIC IDENTIFICATION; MASS SPECTROMETRY; MICROARRAY ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PHYSICAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PYRONEMA CONFLUENS; RTT106 GENE; SEQUENCE HOMOLOGY; SEXUAL DEVELOPMENT; SORDARIA MACROSPORA; SORDARIALES; TANDEM AFFINITY PURIFICATION; TWO HYBRID SYSTEM; UPREGULATION; WILD TYPE;

CELL NUCLEUS; DNA, FUNGAL; FUNGAL PROTEINS; GENE DELETION; GENES, ESSENTIAL; GENES, FUNGAL; GENETIC COMPLEMENTATION TEST; HISTONES; MASS SPECTROMETRY; MICROARRAY ANALYSIS; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; PROTEIN INTERACTION MAPPING; SEQUENCE ANALYSIS, DNA; SORDARIALES; TWO-HYBRID SYSTEM TECHNIQUES;

ASCOMYCOTA; CONFLUENS; FUNGI; GIBBERELLA ZEAE; PYRONEMA; SORDARIA MACROSPORA;

EID: 84860565364     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2012.08058.x     Document Type: Article

References (115)

1. Adkins, M.W., Howar, S.R., and Tyler, J.K. (2004) Chromatin disassembly mediated by the histone chaperone Asf1 is essential for transcriptional activation of the yeast PHO5 and PHO8 genes. Mol Cell 14: 657-666.
2. Adkins, M.W., Williams, S.K., Linger, J., and Tyler, J.K. (2007) Chromatin disassembly from the PHO5 promoter is essential for the recruitment of the general transcription machinery and coactivators. Mol Cell Biol 27: 6372-6382.
3. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
4. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. (1997) Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
5. Avvakumov, N., Nourani, A., and Cote, J. (2011) Histone chaperones: modulators of chromatin marks. Mol Cell 41: 502-514.
6. Bai, L., and Morozov, A.V. (2010) Gene regulation by nucleosome positioning. Trends Genet 26: 476-483.
7. Bayram, O., Krappmann, S., Ni, M., Bok, J.W., Helmstaedt, K., Valerius, O., etal. (2008) VelB/VeA/LaeA complex coordinates light signal with fungal development and secondary metabolism. Science 320: 1504-1506.
8. Bistis, G.N., Perkins, D.D., and Read, N.D. (2003) Different cell types in Neurospora crassa. Fungal Genet Newsl 50: 17-19.
9. Bloemendal, S., Lord, K.M., Rech, C., Hoff, B., Engh, I., Read, N.D., and Kück, U. (2010) A mutant defective in sexual development produces aseptate ascogonia. Eukaryot Cell 9: 1856-1866.
10. Bloemendal, S., Bernhards, Y., Bartho, K., Dettmann, A., Voigt, O., Teichert, I., etal. (2012) A homolog of the human STRIPAK complex controls sexual development in fungi. Mol Microbiol doi:10.1111/j.1365-2958.2012.08024.x
11. Busch, S., Schwier, E.U., Nahlik, K., Bayram, Ö., Helmstaedt, K., Draht, O.W., etal. (2007) An eight-subunit COP9 signalosome with an intact JAMM motif is required for fungal fruit body formation. Proc Nat Acad Sci USA 104: 8089-8094.
12. Cairns, B.R., Lorch, Y., Li, Y., Zhang, M., Lacomis, L., Erdjument-Bromage, H., etal. (1996) RSC, an essential, abundant chromatin-remodeling complex. Cell 87: 1249-1260.
13. Colot, H.V., Park, G., Turner, G.E., Ringelberg, C., Crew, C.M., Litvinkova, L., etal. (2006) A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc Natl Acad Sci USA 103: 10352-10357.
14. Das, C., Tyler, J.K., and Churchill, M.E. (2010) The histone shuffle: histone chaperones in an energetic dance. Trends Biochem Sci 35: 476-489.
15. Eddy, S.R. (1998) Profile hidden Markov models. Bioinformatics 14: 755-763.
16. Engh, I., Nowrousian, M., and Kück, U. (2007a) Regulation of melanin biosynthesis via the dihydroxynaphtalene pathway is dependent on sexual development in the ascomycete Sordaria macrospora. FEMS Microbiol Lett 275: 62-70.
17. Engh, I., Wurtz, C., Witzel-Schlomp, K., Zhang, H.Y., Hoff, B., Nowrousian, M., etal. (2007b) The WW domain protein PRO40 is required for fungal fertility and associates with Woronin bodies. Eukaryot Cell 6: 831-843.
18. English, C.M., Maluf, N.K., Tripet, B., Churchill, M.E., and Tyler, J.K. (2005) ASF1 binds to a heterodimer of histones H3 and H4: a two-step mechanism for the assembly of the H3-H4 heterotetramer on DNA. Biochemistry 44: 13673-13682.
19. English, C.M., Adkins, M.W., Carson, J.J., Churchill, M.E., and Tyler, J.K. (2006) Structural basis for the histone chaperone activity of Asf1. Cell 127: 495-508.
20. Gingras, A.C., Caballero, M., Zarske, M., Sanchez, A., Hazbun, T.R., Fields, S., etal. (2005) A novel, evolutionarily conserved protein phosphatase complex involved in cisplatin sensitivity. Mol Cell Proteomics 4: 1725-1740.
21. Green, E.M., Antczak, A.J., Bailey, A.O., Franco, A.A., Wu, K.J., Yates, J.R., and Kaufman, P.D. (2005) Replication-independent histone deposition by the HIR complex and Asf1. Curr Biol 15: 2044-2049.
22. Grigsby, I.F., Rutledge, E.M., Morton, C.A., and Finger, F.P. (2009) Functional redundancy of two C. elegans homologs of the histone chaperone Asf1 in germline DNA replication. Dev Biol 329: 64-79.
23. Healy, S., Khan, D.H., and Davie, J.R. (2011) Gene expression regulation through 14-3-3 interactions with histones and HDACs. Discov Med 11: 349-358.
24. Heyd, F., Chen, R., Afshar, K., Saba, I., Lazure, C., Fiolka, K., and Möröy, T. (2011) The p150 subunit of the histone chaperone Caf-1 interacts with the transcriptional repressor Gfi1. Biochim Biophys Acta 1809: 255-261.
25. Hoff, B., Kamerewerd, J., Sigl, C., Mitterbauer, R., Zadra, I., Kurnsteiner, H., and Kuck, U. (2010) Two components of a velvet-like complex control hyphal morphogenesis, conidiophore development, and penicillin biosynthesis in Penicillium chrysogenum. Eukaryot Cell 9: 1236-1250.
26. Huang, S., Zhou, H., Katzmann, D., Hochstrasser, M., Atanasova, E., and Zhang, Z. (2005) Rtt106p is a histone chaperone involved in heterochromatin-mediated silencing. Proc Nat Acad Sci USA 102: 13410-13415.
27. Huang, X.Q., Hardison, R.C., and Miller, W. (1990) A space-efficient algorithm for local similarities. Comput Appl Biosci 6: 373-381.
28. Jacobsen, S., Wittig, M., and Pöggeler, S. (2002) Interaction between mating-type proteins from the homothallic fungus Sordaria macrospora. Curr Genet 41: 150-158.
29. James, P., Halladay, J., and Craig, E.A. (1996) Genomic libraries and a host strain deigned for highly efficient two-hybrid selection in yeast. Genetics 144: 1425-1436.
30. Jerpseth, B., Greener, A., Short, J.M., Viola, J., and Kretz, P.L. (1992) XL1-Blue MRF'E. coli cells: McrA-, McrCB-, McrF-, Mrr-, HsdR- derivative of XL1-Blue cells. Strateg Mol Biol 5: 81-83.
31. Kale, S.P., Milde, L., Trapp, M.K., Frisvad, J.C., Keller, N.P., and Bok, J.W. (2008) Requirement of LaeA for secondary metabolism and sclerotial production in Aspergillus flavus. Fungal Genet Biol 45: 1422-1429.
32. Kalinka, A.T., Varga, K.M., Gerrard, D.T., Preibisch, S., Corcoran, D.L., Jarrells, J., etal. (2010) Gene expression divergence recapitulates the developmental hourglass model. Nature 468: 811-814.
33. Kaufman, P.D., Kobayashi, R., and Stillman, B. (1997) Ultraviolet radiation sensitivity and reduction of telomeric silencing in Saccharomyces cerevisiae cells lacking chromatin assembly factor-I. Genes Dev 11: 345-357.
34. Kim, H., Seol, J., Han, J., Youn, H., and Cho, E. (2007) Histone chaperones regulated histone exchange during transcription. EMBO J 26: 4467-4474.
35. Kim, H.J., Seol, J.H., and Cho, E.J. (2009) Potential role of the histone chaperone, CAF-1, in transcription. BMB Rep 42: 227-231.
36. Klix, V., Nowrousian, M., Ringelberg, C., Loros, J.J., Dunlap, J.C., and Pöggeler, S. (2010) Functional characterization of MAT1-1-specific mating-type genes in the homothallic ascomycete Sordaria macrospora provides new insights into essential and nonessential sexual regulators. Eukaryot Cell 9: 894-905.
37. Krawitz, D.C., Kama, T., and Kaufman, P.D. (2002) Chromatin assembly factor I mutants defective for PCNA binding require Asf1/Hir proteins for silencing. Mol Cell Biol 22: 614-625.
38. Krebs, A., and Tora, L. (2009) Keys to open chromatin for transcription activation: FACT and Asf1. Mol Cell 34: 397-399.
39. Kück, U. (2005) A Sordaria macrospora mutant lacking the leu1 gene shows a developmental arrest during fruiting body formation. Mol Genet Genomics 274: 307-315.
40. Kück, U., Pöggeler, S., Nowrousian, M., Nolting, N., and Engh, I. (2009) Sordaria macrospora, a model system for fungal development. In The Mycota XV. Anke, T., and Weber, D. (eds). Berlin-Heidelberg: Springer Verlag, pp. 17-39.
41. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
42. Lambert, J.P., Fillingham, J., Siahbazi, M., Greenblatt, J., Baetz, K., and Figeys, D. (2010) Defining the budding yeast chromatin-associated interactome. Mol Syst Biol 6: 448.
43. Le, S., Davis, C., Konopka, J.B., and Sternglanz, R. (1997) Two new S-phase-specific genes from Saccharomyces cerevisiae. Yeast 13: 1029-1042.
44. Lorch, Y., Cairns, B.R., Zhang, M., and Kornberg, R.D. (1998) Activated RSC-nucleosome complex and persistently altered form of the nucleosome. Cell 94: 29-34.
45. Lorch, Y., Maier-Davis, B., and Kornberg, R.D. (2006) Chromatin remodeling by nucleosome disassembly in vitro. Proc Natl Acad Sci USA 103: 3090-3093.
46. Lumbsch, H.T. (2000) Phylogeny of filamentous ascomycetes. Naturwissenschaften 87: 335-342.
47. MacKenzie, D.A., Jeenes, D.J., Belshaw, N.J., and Archer, D.B. (1993) Regulation of secreted protein production by filamentous fungi: recent developments and perspectives. J Gen Microbiol 139: 2295-2307.
48. Masloff, S., Pöggeler, S., and Kück, U. (1999) The pro1(+) gene from Sordaria macrospora encodes a C6 zinc finger transcription factor required for fruiting body development. Genetics 152: 191-199.
49. Mayrhofer, S., Weber, J.M., and Pöggeler, S. (2006) Pheromones and pheromone receptors are required for proper sexual development in the homothallic ascomycete Sordaria macrospora. Genetics 172: 1521-1533.
50. Mello, J.A., Sillje, H.H., Roche, D.M., Kirschner, D.B., Nigg, E.A., and Almouzni, G. (2002) Human Asf1 and CAF-1 interact and synergize in a repair-coupled nucleosome assembly pathway. EMBO Rep 3: 329-334.
51. Minard, L.V., Lin, L.J., and Schultz, M.C. (2011a) SWI/SNF and Asf1 independently promote derepression of the DNA damage response genes under conditions of replication stress. PLoS ONE 6: e21633.
52. Minard, L.V., Williams, J.S., Walker, A.C., and Schultz, M.C. (2011b) Transcriptional regulation by Asf1: new mechanistic insights from studies of the DNA damage response to replication stress. J Biol Chem 286: 7082-7092.
53. Moggs, J.G., Grandi, P., Quivy, J.P., Jonsson, Z.O., Hubscher, U., Becker, P.B., and Almouzni, G. (2000) A CAF-1-PCNA-mediated chromatin assembly pathway triggered by sensing DNA damage. Mol Cell Biol 20: 1206-1218.
54. Moore-Landecker, E. (1992) Physiology and biochemistry of ascocarp induction and development. Mycol Res 96: 705-716.
55. Moshkin, Y.M., Armstrong, J.A., Maeda, R.K., Tamkun, J.W., Verrijzer, P., Kennison, J.A., and Karch, F. (2002) Histone chaperone ASF1 cooperates with the Brahma chromatin-remodelling machinery. Genes Dev 16: 2621-2626.
56. Mousson, F., Lautrette, A., Thuret, J.Y., Agez, M., Courbeyrette, R., Amigues, B., etal. (2005) Structural basis for the interaction of Asf1 with histone H3 and its functional implications. Proc Natl Acad Sci USA 102: 5975-5980.
57. Mousson, F., Ochsenbein, F., and Mann, C. (2007) The histone chaperone Asf1 at the crossroads of chromatin and DNA checkpoint pathways. Chromosoma 116: 79-93.
58. Munakata, T., Adachi, N., Yokoyama, N., Kuzuhara, T., and Horikoshi, M. (2000) A human homologue of yeast anti-silencing factor has histone chaperone activity. Genes Cells 5: 221-233.
59. Natsume, R., Eitoku, M., Akai, Y., Sano, N., Horikoshi, M., and Senda, T. (2007) Structure and function of the histone chaperone CIA/ASF1 complexed with histones H3 and H4. Nature 446: 338-341.
60. Neely, K.E., and Workman, J.L. (2002) The complexity of chromatin remodeling and its links to cancer. Biochim Biophys Acta 1603: 19-29.
61. Nowrousian, M. (2007) Of patterns and pathways: microarray technologies for the analysis of filamentous fungi. Fungal Biol Rev 21: 171-178.
62. Nowrousian, M. (2009) A novel polyketide biosynthesis gene cluster is involved in fruiting body morphogenesis in the filamentous fungi Sordaria macrospora and Neurospora crassa. Curr Genet 55: 185-198.
63. Nowrousian, M. (2010) Next-generation sequencing techniques for eukaryotic microorganisms: sequencing-based solutions to biological problems. Eukaryot Cell 9: 1300-1310.
64. Nowrousian, M., and Cebula, P. (2005) The gene for a lectin-like protein is transcriptionally activated during sexual development, but is not essential for fruiting body formation in the filamentous fungus Sordaria macrospora. BMC Microbiol 5: 64.
65. Nowrousian, M., and Kück, U. (2006) Comparative gene expression analysis of fruiting body development in two filamentous fungi. FEMS Microbiol Lett 257: 328-335.
66. Nowrousian, M., Masloff, S., Pöggeler, S., and Kück, U. (1999) Cell differentiation during sexual development of the fungus Sordaria macrospora requires ATP citrate lyase activity. Mol Cell Biol 19: 450-460.
67. Nowrousian, M., Ringelberg, C., Dunlap, J.C., Loros, J.J., and Kück, U. (2005) Cross-species microarray hybridization to identify developmentally regulated genes in the filamentous fungus Sordaria macrospora. Mol Genet Genomics 273: 137-149.
68. Nowrousian, M., Frank, S., Koers, S., Strauch, P., Weitner, T., Ringelberg, C., etal. (2007a) The novel ER membrane protein PRO41 is essential for sexual development in the filamentous fungus Sordaria macrospora. Mol Microbiol 64: 923-937.
69. Nowrousian, M., Piotrowski, M., and Kück, U. (2007b) Multiple layers of temporal and spatial control regulate accumulation of the fruiting body-specific protein APP in Sordaria macrospora and Neurospora crassa. Fungal Genet Biol 44: 602-614.
70. Nowrousian, M., Stajich, J.E., Chu, M., Engh, I., Espagne, E., Halliday, K., etal. (2010) De novo assembly of a 40Mb eukaryotic genome from short sequence reads: Sordaria macrospora, a model organism for fungal morphogenesis. PLoS Genet 6: e1000891.
71. Nowrousian, M., Teichert, I., Masloff, S., and Kück, U. (2012) Whole-genome sequencing of Sordaria macrospora mutants identifies developmental genes. G3 (Bethesda) 2: 261-270.
72. Ochman, H., Gerber, A.S., and Hartl, D.L. (1988) Genetic applications of an inverse polymerase chain reaction. Genetics 120: 621-623.
73. Park, Y.J., and Luger, K. (2008) Histone chaperones in nucleosome eviction and histone exchange. Curr Opin Struct Biol 18: 282-289.
74. Perrin, R.M., Fedorova, N.D., Bok, J.W., Cramer, R.A., Wortman, J.R., Kim, H.S., etal. (2007) Transcriptional regulation of chemical diversity in Aspergillus fumigatus by LaeA. PLoS Pathog 3: e50.
75. Pilyugin, M., Demmers, J., Verrijzer, C.P., Karch, F., and Moshkin, Y.M. (2009) Phosphorylation-mediated control of histone chaperone ASF1 levels by Tousled-like kinases. PLoS ONE 4: e8328.
76. Pöggeler, S., and Kück, U. (2004) A WD40 repeat protein regulates fungal cell differentiation and can be replaced functionally by the mammalian homologue striatin. Eukaryot Cell 3: 232-240.
77. Pöggeler, S., and Kück, U. (2006) Highly efficient generation of signal transduction knockout mutants using a fungal strain deficient in the mammalian ku70 ortholog. Gene 378: 1-10.
78. Pöggeler, S., Nowrousian, M., Jacobsen, S., and Kück, U. (1997a) An efficient procedure to isolate fungal genes from an indexed cosmid library. J Microbiol Methods 29: 49-61.
79. Pöggeler, S., Risch, S., Kück, U., and Osiewacz, H.D. (1997b) Mating-type genes from the homothallic fungus Sordaria macrospora are functionally expressed in a heterothallic ascomycete. Genetics 147: 567-580.
80. Pöggeler, S., Nowrousian, M., and Kück, U. (2006a) Fruiting-body development in ascomycetes. In The Mycota I. Kües, U., and Fischer, R. (eds). Berlin-Heidelberg: Springer Verlag, pp. 325-355.
81. Pöggeler, S., Nowrousian, M., Ringelberg, C., Loros, J.J., Dunlap, J.C., and Kück, U. (2006b) Microarray and real time PCR analyses reveal mating type-dependent gene expression in a homothallic fungus. Mol Genet Genomics 275: 492-503.
82. Qi, W., Kwon, C., and Trail, F. (2006) Microarray analysis of transcript accumulation during perithecium development in the filamentous fungus Gibberella zeae (anamorph Fusarium graminearum). Mol Genet Genomics 276: 87-100.
83. Rigaut, G., Shevchenko, A., Rutz, B., Wilm, M., Mann, M., and Seraphin, B. (1999) A generic protein purification method for protein complex characterization and proteome exploration. Nat Biotechnol 17: 1030-1032.
84. Rose, M., and Botstein, D. (1983) Construction and use of gene fusions to lacZ (beta-galactosidase) that are expressed in yeast. Methods Enzymol 101: 167-180.
85. Ruepp, A., Zollner, A., Maier, D., Albermann, K., Hani, J., Mokrejs, M., etal. (2004) The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acids Res 32: 5539-5545.
86. Rufiange, A., Jacques, P.E., Bhat, W., Robert, F., and Nourani, A. (2007) Genome-wide replication-independent histone H3 exchange occurs predominantly at promoters and implicates H3 K56 acetylation and Asf1. Mol Cell 27: 393-405.
87. Sambrook, J., and Russel, D.W. (2001) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
88. Sanematsu, F., Takami, Y., Barman, H.K., Fukagawa, T., Ono, T., Shibahara, K., and Nakayama, T. (2006) Asf1 is required for viability and chromatin assembly during DNA replication in vertebrate cells. J Biol Chem 281: 13817-13827.
89. Sarikaya Bayram, O., Bayram, O., Valerius, O., Park, H.S., Irniger, S., Gerke, J., etal. (2010) LaeA control of velvet family regulatory proteins for light-dependent development and fungal cell-type specificity. PLoS Genet 6: e1001226.
90. Schär, P., Herrmann, G., Daly, G., and Lindahl, T. (1997) A newly identified DNA ligase of Saccharomyces cerevisiae involved in RAD52-independent repair of DNA double-strand breaks. Genes Dev 11: 1912-1924.
91. Schwartz, B.E., and Ahmad, K. (2005) Transcriptional activation triggers deposition and removal of the histone variant H3.3. Genes Dev 19: 804-814.
92. Silva, A.C., Xu, X., Kim, H.S., Fillingham, J., Kislinger, T., Mennella, T.A., and Keogh, M.C. (2012) The replication-independent H3-H4 chaperones HIR, ASF1, and RTT106 co-operate to maintain promoter fidelity. J Biol Chem 287: 1709-1718.
93. Singer, M.S., Kahana, A., Wolf, A.J., Meisinger, L.L., Peterson, S.E., Goggin, C., etal. (1998) Identification of high-copy disruptors of telomeric silencing in Saccharomyces cerevisiae. Genetics 150: 613-632.
94. Snel, B., van Noort, V., and Huynen, M.A. (2004) Gene co-regulation is highly conserved in the evolution of eukaryotes and prokaryotes. Nucleic Acids Res 32: 4725-4731.
95. Sogo, J.M., Stahl, H., Koller, T., and Knippers, R. (1986) Structure of replicating simian virus 40 minichromosomes. The replication fork, core histone segregation and terminal structures. J Mol Biol 189: 189-204.
96. Stuart, J.M., Segal, E., Koller, D., and Kim, S.K. (2003) A gene-coexpression network for global discovery of conserved genetic modules. Science 302: 249-255.
97. Sunavala-Dossabhoy, G., and De Benedetti, A. (2009) Tousled homolog, TLK1, binds and phosphorylates Rad9; TLK1 acts as a molecular chaperone in DNA repair. DNA Repair (Amst) 8: 87-102.
98. Tagami, H., Ray-Gallet, D., Almouzni, G., and Nakatani, Y. (2004) Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell 116: 51-61.
99. Takahata, S., Yu, Y., and Stillman, D.J. (2009) FACT and Asf1 regulate nucleosome dynamics and coactivator binding at the HO promoter. Mol Cell 34: 405-415.
100. Takami, Y., Ono, T., Fukagawa, T., Shibahara, K., and Nakayama, T. (2007) Essential role of chromatin-assembly factor-1-mediated rapid nucleosome assembly for DNA replication and cell division in vertebrate cells. Mol Biol Cell 18: 129-141.
101. Thompson, J.D., Higgins, D.G., and Gibson, T.J. (1994) clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
102. Tian, C., Kasuga, T., Sachs, M.S., and Glass, N.L. (2007) Transcriptional profiling of cross pathway control in Neurospora crassa and comparative analysis of the Gcn4 and CPC1 regulons. Eukaryot Cell 6: 1018-1029.
103. Treich, I., and Carlson, M. (1997) Interaction of a Swi3 homolog with Sth1 provides evidence for a Swi/Snf-related complex with an essential function in Saccharomyces cerevisiae. Mol Cell Biol 17: 1768-1775.
104. Tyler, J.K., Adams, C.R., Chen, S.R., Kobayashi, R., Kamakaka, R.T., and Kadonaga, J.T. (1999) The RCAF complex mediates chromatin assembly during DNA replication and repair. Nature 402: 555-560.
105. Umehara, T., Chimura, T., Ichikawa, N., and Horikoshi, M. (2002) Polyanionic stretch-deleted histone chaperone Cia1/Asf1p is functional both in vivo and in vitro. Genes Cells 7: 59-73.
106. Weake, V.M., and Workman, J.L. (2010) Inducible gene expression: diverse regulatory mechanisms. Nat Rev Genet 11: 426-437.
107. Wellen, K.E., Hatzivassiliou, G., Sachdeva, U.M., Bui, T.V., Cross, J.R., and Thompson, C.B. (2009) ATP-citrate lyase links cellular metabolism to histone acetylation. Science 324: 1076-1080.
108. Wessels, J.G.H. (1993) Fruiting in the higher fungi. Adv Microb Physiol 34: 147-202.
109. Wiemann, P., Brown, D.W., Kleigrewe, K., Bok, J.W., Keller, N.P., Humpf, H.U., and Tudzynski, B. (2010) FfVel1 and FfLae1, components of a velvet-like complex in Fusarium fujikuroi, affect differentiation, secondary metabolism and virulence. Mol Microbiol 77: 972-994.
110. Williams, S.K., Truong, D., and Tyler, J.K. (2008) Acetylation in the globular core of histone H3 on lysine-56 promotes chromatin disassembly during transcriptional activation. Proc Natl Acad Sci USA 105: 9000-9005.
111. Wolters, D.A., Washburn, M.P., and Yates, J.R., 3rd (2001) An automated multidimensional protein identification technology for shotgun proteomics. Anal Chem 73: 5683-5690.
112. Yahyaoui, W., and Zannis-Hadjopoulos, M. (2009) 14-3-3 proteins function in the initiation and elongation steps of DNA replication in Saccharomyces cerevisiae. J Cell Sci 122: 4419-4426.
113. Yarden, O., and Yanofsky, C. (1991) Chitin synthase 1 plays a major role in cell wall biogenesis in Neurospora crassa. Genes Dev 5: 2420-2430.
114. Zabaronick, S.R., and Tyler, J.K. (2005) The histone chaperone anti-silencing function 1 is a global regulator of transcription independent of passage through S phase. Mol Cell Biol 25: 652-660.
115. Zhu, Y., Weng, M., Yang, Y., Zhang, C., Li, Z., Shen, W.H., and Dong, A. (2011) Arabidopsis homologues of the histone chaperone ASF1 are crucial for chromatin replication and cell proliferation in plant development. Plant J 66: 443-455.