Chromosomal distribution and functional interpretation of epigenetic histone marks in plants

Plant Cytogenetics: Genome Structure and Chromosome Function

Volumn 9, Issue , 2012, Pages 231-253

  Fuchs, Jörg ^a   Schubert, Ingo ^a  

^a LEIBNIZ INSTITUTE OF PLANT GENETICS AND CROP PLANT RESEARCH IPK   (Germany)

Author keywords

Acetylation; Chromatin organization; Euchromatin; Heterochromatin; Histone modification; Immunostaining; Methylation; Phosphorylation

Indexed keywords

EID: 84884418081     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-0-387-70869-0_9     Document Type: Chapter

References (152)

1. Aagaard L, Laible G, Selenko P, Schmid M, Dorn R, Schotta G, Kuhfittig S, Wolf A, Lebersorger A, Singh PB, Reuter G, Jenuwein T (1999) Functional mammalian homologues of the Drosophila PEV-modifier Su(var)3-9 encode centromere-associated proteins which complex with the heterochromatin component M31. EMBO J 18:2-1938
2. Adams RR, Maiato H, Earnshaw WC, Carmena M (2001) Essential roles of Drosophila inner centromere protein (INCENP) and aurora B in histone H3 phosphorylation, metaphase chromosome alignment, kinetochore disjunction, and chromosome segregation. J Cell Biol 153:2-880
3. Adhvaryu KK, Morris SA, Strahl BD, Selker EU (2005) Methylation of histone H3 lysine 36 is required for normal development in Neurospora crassa. Eukaryot Cell 4:2-1464
4. Allfrey VG, Faulkner R, Mirsky AE (1964) Acetylation and methylation of histones and their possible role in the regulation of RNA synthesis. Proc Natl Acad Sci USA 51:2-794
5. Allshire RC, Selker EU (2007) Fungal models for epigenetic research: Schizosaccharomyces pombe and Neurospora crassa. In: Allis CD, Jenuwein T, Reinberg D, Caparros M-L (eds) Epigenetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 101-125
6. Bannister AJ, Zegerman P, Partridge JF, Miska EA, Thomas JO, Allshire RC, Kouzarides T (2001) Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410:2-124
7. Bartee L, Malagnac F, Bender J (2001) Arabidopsis cmt3 chromomethylase mutations block nonCG methylation and silencing of an endogenous gene. Genes Dev 15:2-1758
8. Bedford MT, Richard S (2005) Arginine methylation an emerging regulator of protein function. Mol Cell 18:2-272
9. Belyaev N, Keohane AM, Turner BM (1996) Differential underacetylation of histones H2A, H3 and H4 on the inactive X chromosome in human female cells. Hum. Genet 97:2-578
10. Belyaev ND, Houben A, Baranczewski P, Schubert I (1997) Histone H4 acetylation in plant heterochromatin is altered during the cell cycle. Chromosoma 106:2-197
11. Belyaev ND, Houben A, Baranczewski P, Schubert I (1998) The acetylation patterns of histones H3 and H4 along Vicia faba chromosomes are different. Chromosome Res 6:2-63
12. Bergmüller E, Gehrig PM, Gruissem W (2007) Characterization of post-translational modifications of histone H2B-variants isolated from Arabidopsis thaliana. J Proteome Res 6:2-3668
13. Bird A (2002) DNA methylation patterns and epigenetic memory. Genes Dev 16:2-21
14. Bird AW, Yu DY, Pray-Grant MG, Qiu Q, Harmon KE, Megee PC, Grant PA, Smith MM, Christman MF (2002) Acetylation of histone H4 by Esa1 is required for DNA double-strand break repair. Nature 419:2-415
15. Cao X, Jacobsen SE (2002) Locus-specific control of asymmetric and CpNpG methylation by the DRM and CMT3 methyltransferase genes. Proc Natl Acad Sci USA 99 Suppl 4:16491-16498
16. Carchilan M, Delgado M, Ribeiro T, Costa-Nunes P, Caperta A, Morais-Cecílio L, Jones RN, Viegas W, Houben A (2007) Transcriptionally active heterochromatin in rye B chromosomes. Plant Cell 19:2-1749
17. Chan SW-L, Henderson IR, Jacobsen SE (2005) Gardening the genome: DNA methylation in Arabidopsis thaliana. Nat Rev Genet 6:2-360
18. Cheung WL, Briggs SD, Allis CD (2000) Acetylation and chromosomal functions. Curr Opin Cell Biol 12:2-333
19. Cloos PAC, Christensen J, Agger K, Maiolica A, Rappsilber J, Antal T, Hansen KH, Helin K (2006) The putative oncogene GASC1 demethylates tri- and dimethylated lysine 9 on histone H3. Nature 442:2-311
20. Dacwag CS, Ohkawa Y, Pal S, Sif S, Imbalzano AN (2007) The protein arginine methyltransferase Prmt5 is required for myogenesis because it facilitates ATP-dependent chromatin remodeling. Mol Cell Biol 27:2-394
21. Daujat S, Bauer UM, Shah V, Turner B, Berger S, Kouzarides T (2002) Crosstalk between CARM1 methylation and CBP acetylation on histone H3. Curr Biol 12:2-2097
22. De Santa F, Totaro MG, Prosperini E, Notarbartolo S, Testa G, Natoli G (2007) The histone H3 lysine-27 demethylase Jmjd3 links inflammation to inhibition of polycomb-mediated gene silencing. Cell 130:2-1094
23. Delattre M, Spierer A, Tonka C-H, Spierer P (2000) The genomic silencing of position-effect variegation in Drosophila melanogaster: interaction between the heterochromatin-associated proteins Su(var)3-7 and HP1. J Cell Sci 113 Pt 23:4253-4261
24. Di Stefano L, Ji J-Y, Moon N-S, Herr A, Dyson N (2007) Mutation of Drosophila Lsd1 disrupts H3-K4 methylation, resulting in tissue-specific defects during development. Curr Biol 17:2-812
25. Döbel P, Schubert I, Rieger R (1978) Distribution of heterochromatin in a reconstructed karyotype of Vicia faba as identified by banding- and DNA-late replication patterns. Chromosoma 69:2-209
26. Ebbs ML, Bartee L, Bender J (2005) H3 lysine 9 methylation is maintained on a transcribed inverted repeat by combined action of SUVH6 and SUVH4 methyltransferases. Mol Cell Biol 25:2-10515
27. Ebbs ML, Bender J (2006) Locus-specific control of DNA methylation by the Arabidopsis SUVH5 histone methyltransferase. Plant Cell 18:2-1176
28. Ebert A, Schotta G, Lein S, Kubicek S, Krauss V, Jenuwein T, Reuter G (2004) Su(var) genes regulate the balance between euchromatin and heterochromatin in Drosophila. Genes Dev 18: 2-2983
29. Ebert A, Lein S, Schotta G, Reuter G (2006) Histone modification and the control of heterochromatic gene silencing in Drosophila. Chromosome Res 14:2-392
30. Eissenberg JC, Lee MG, Schneider J, Ilvarsonn A, Shiekhattar R, Shilatifard A (2007) The trithorax-group gene in Drosophila little imaginal discs encodes a trimethylated histone H3 Lys4 demethylase. Nat Struct Mol Biol 14:2-346
31. Finnegan EJ, Kovac KA (2000) Plant DNA methyltransferases. Plant Mol Biol 43:2-201
32. Fischle W, Tseng BS, Dormann HL, Ueberheide BM, Garcia BA, Shabanowitz J, Hunt DF, Funabiki H, Allis CD (2005) Regulation of HP1-chromatin binding by histone H3 methylation and phosphorylation. Nature 438:2-1122
33. Fodor BD, Kubicek S, Yonezawa M, O'Sullivan RJ, Sengupta R, Perez-Burgos L, Opravil S, Mechtler K, Schotta G, Jenuwein T (2006) Jmjd2b antagonizes H3K9 trimethylation at pericentric heterochromatin in mammalian cells. Genes Dev 20:2-1562
34. Freitag M, Hickey PC, Khlafallah TK, Read ND, Selker EU (2004) HP1 is essential for DNA methylation in Neurospora. Mol Cell 13:2-434
35. Friesner JD, Liu B, Culligan K, Britt AB (2005) Ionizing radiation-dependent gamma-H2AX focus formation requires ataxia telangiectasia mutated and ataxia telangiectasia mutated and Rad3-related. Mol Biol Cell 16:2-2576
36. Fuchs J, Jovtchev G, Schubert I (2008) The chromosomal distribution of histone methylation marks in gymnosperms differs from that of angiosperms. Chromosome Res 16:2-898
37. Fuchs J, Pich U, Meister A, Schubert I (1994) Differentiation of field bean heterochromatin by in situ hybridization with a repeated FokI sequence. Chromosome Res 2:2-28
38. Fuchs J, Strehl S, Brandes A, Schweizer D, Schubert I (1998) Molecular-cytogenetic characterization of the Vicia faba genome-heterochromatin differentiation, replication patterns and sequence localization. Chromosome Res 6:2-230
39. Fuchs J, Demidov D, Houben A, Schubert I (2006) Chromosomal histone modification patterns-from conservation to diversity. Trends Plant Sci 11:2-208
40. Gernand D, Demidov D, Houben A (2003) The temporal and spatial pattern of histone H3 phosphorylation at serine 28 and serine 10 is similar in plants but differs between mono- and polycentric chromosomes. Cytogenet Genome Res 101:2-176
41. Goto H, Tomono Y, Ajiro K, Kosako H, Fujita M, Sakurai M, Okawa K, Iwamatsu A, Okigaki T, Takahashi T, Inagaki M (1999) Identification of a novel phosphorylation site on histone H3 coupled with mitotic chromosome condensation. J Biol Chem 274:2-25549
42. Grewal SIS, Moazed D (2003) Heterochromatin and epigenetic control of gene expression. Science 301:2-802
43. Grunstein M (1997) Histone acetylation in chromatin structure and transcription. Nature 389: 2-352
44. Guerra M, Brasileiro-Vidal AC, Arana P, Puertas MJ (2006) Mitotic microtubule development and histone H3 phosphorylation in the holocentric chromosomes of Rhynchospora tenuis (Cyperaceae). Genetica 126:2-41
45. Gurtley LR, Walters RA, Tobey RA (1975) Sequential phosphorylation of histone subfraction in the Chinese hamster cell cycle. J Biol Chem 250:2-3944
46. Hanson KK, Kelley AC, Bienz M (2005) Loss of Drosophila borealin causes polyploidy, delayed apoptosis and abnormal tissue development. Development 132:2-4787
47. Heard E (2005) Delving into the diversity of facultative heterochromatin: the epigenetics of the inactive X chromosome. Curr Opin Genet Dev 15:2-489
48. Hendzel MJ, Wei Y, Mancini MA, Van Hooser A, Ranalli T, Brinkley BR, Bazett-Jones DP, Allis CD (1997) Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106:2-360
49. Hizume K, Yoshimura SH, Kumeta M, Takeyasu K (2007) Structural organization of dynamic chromatin. Subcell Biochem 41:2-28
50. Houben A, Belyaev ND, Turner BM, Schubert I (1996) Differential immunostaining of plant chromosomes by antibodies recognizing acetylated histone H4 variants. Chromosome Res 4:2-194
51. Houben A, Wako T, Furushima-Shimogawara R, Presting G, Künzel G, Schubert I, Fukui K (1999) Short communication: the cell cycle dependent phosphorylation of histone H3 is correlated with the condensation of plant mitotic chromosomes. Plant J 18:2-679
52. Houben A, Demidov D, Gernand D, Meister A, Leach CR, Schubert I (2003) Methylation of his-tone H3 in euchromatin of plant chromosomes depends on basic nuclear DNA content. Plant J 33:2-973
53. Houben A, Demidov D, Rutten T, Scheidtmann KH (2005) Novel phosphorylation of histone H3 at threonine 11 that temporally correlates with condensation of mitotic and meiotic chromosomes in plant cells. Cytogenet Genome Res 109:2-155
54. Houben A, Demidov D, Caperta AD, Karimi R, Agueci F, Vlasenko L (2007) Phosphorylation of histone H3 in plants-a dynamic affair. Biochim Biophys Acta 1769:2-315
55. Ikura T, Ogryzko VV, Grigoriev M, Groisman R, Wang J, Horikoshi M, Scully R, Qin J, Nakatani Y (2000) Involvement of the TIP60 histone acetylase complex in DNA repair and apoptosis. Cell 102:2-473
56. Jackson JP, Lindroth AM, Cao X, Jacobsen SE (2002) Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416:2-560
57. Jackson JP, Johnson L, Jasencakova Z, Zhang X, Perez-Burgos L, Singh PB, Cheng X, Schubert I, Jenuwein T, Jacobsen SE (2004) Dimethylation of histone H3 lysine 9 is a critical mark for DNA methylation and gene silencing in Arabidopsis thaliana. Chromosoma 112:2-315
58. James TC, Elgin SCR (1986) Identification of a nonhistone chromosomal protein associated with heterochromatin in Drosophila melanogaster and its gene. Mol Cell Biol 6:2-3872
59. Jasencakova Z, Meister A, Walter J, Turner BM, Schubert I (2000) Histone H4 acetylation of euchromatin and heterochromatin is cell cycle dependent and correlated with replication rather than with transcription. Plant Cell 12:2-2100
60. Jasencakova Z, Meister A, Schubert I (2001) Chromatin organization and its relation to replication and histone acetylation during the cell cycle in barley. Chromosoma 110:2-92
61. Jasencakova Z, Soppe WJJ, Meister A, Gernand D, Turner BM, Schubert I (2003) Histone modifications in Arabidopsis-high methylation of H3 lysine 9 is dispensable for constitutive heterochromatin. Plant J 33:2-480
62. Jenuwein T, Allis CD (2001) Translating the histone code. Science 293:2-1080
63. Jeppesen P, Mitchell A, Turner B, Perry P (1992) Antibodies to defined histone epitopes reveal variations in chromatin conformation and underacetylation of centric heterochromatin in human metaphase chromosomes. Chromosoma 101:2-332
64. Jeppesen P, Turner BM (1993) The inactive X chromosome in female mammals is distinguished by a lack of histone H4 acetylation, a cytogenetic marker for gene expression. Cell 74: 2-289
65. Jia S, Kobayashi R, Grewal SIS (2005) Ubiquitin ligase component Cu14 associates with Clr4 histone methyltransferase to assemble heterochromatin. Nat Cell Biol 7:2-1013
66. Jiang D, Yang W, He Y, Amasino RM (2007) Arabidopsis relatives of the human lysine specific demethylase1 repress the expression of FWA and FLOWERING LOCUS C and thus promote the floral transition. Plant Cell 19:2-2987
67. Johnson LM, Cao X, Jacobsen SE (2002) Interplay between two epigenetic marks. DNA methylation and histone H3 lysine 9 methylation. Curr Biol 12:2-1367
68. Johnson LM, Mollah S, Garcia BA, Muratore TL, Shabanowitz J, Hunt DF, Jacobsen SE (2004) Mass spectrometry analysis of Arabidopsis histone H3 reveals distinct combinations of post-translational modifications. Nucleic Acids Res 32:2-6518
69. Johnson LM, Bostick M, Zhang X, Kraft E, Henderson I, Callis J, Jacobsen SE (2007) The SRA methyl-cytosine-binding domain links DNA and histone methylation. Curr Biol 17:2-384
70. Kaszás É, Cande WZ (2000) Phosphorylation of histone H3 is correlated with changes in the maintenance of sister chromatid cohesion during meiosis in maize, rather than the condensation of the chromatin. J Cell Sci 113 (Pt 18):3217-3226
71. Kirmizis A, Santos-Rosa H, Penkett CJ, Singer MA, Vermeulen M, Mann M, Bähler J, Green RD, Kouzarides T (2007) Arginine methylation at histone H3R2 controls deposition of H3K4 trim-ethylation. Nature 449:2-932
72. Klose RJ, Yamane K, Bae Y, Zhang D, Erdjument-Bromage H, Tempst P, Wong J, Zhang Y (2006) The transcriptional repressor JHDM3A demethylates trimethyl histone H3 lysine 9 and lysine 36. Nature 442:2-316
73. Klose RJ, Yan Q, Tothova Z, Yamane K, Erdjument-Bromage H, Tempst P, Gilliland DG, Zhang Y, Kaelin WG, Jr (2007) The retinoblastoma binding protein RBP2 is an H3K4 demethylase. Cell 128:2-900
74. Kornberg RD (1974) Chromatin structure: a repeating unit of histones and DNA. Science 184:2-871
75. Kornberg RD, Lorch Y (1999) Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome. Cell 98:2-294
76. Lachner M, O'Carroll D, Rea S, Mechtler K, Jenuwein T (2001) Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410:2-120
77. Lachner M, Sengupta R, Schotta G, Jenuwein T (2004) Trilogies of histone lysine methylation as epigenetic landmarks of the eukaryotic genome. Cold Spring Harb Symp Quant Biol 69: 2-218
78. Lan F, Bayliss PE, Rinn JL, Whetstine JR, Wang JK, Chen S, Iwase S, Alpatov R, Issaeva I, Canaani E, Roberts TM, Chang HY, Shi Y (2007) A histone H3 lysine 27 demethylase regulates animal posterior development. Nature 449:2-694
79. Latham JA, Dent SY (2007) Cross-regulation of histone modifications. Nat Struct Mol Biol 14:2-1024
80. Lee DY, Hayes JJ, Pruss D, Wolffe AP (1993) A positive role for histone acetylation in transcription factor access to nucleosomal DNA. Cell 72:2-84
81. Lee MG, Villa R, Trojer P, Norman J, Yan K-P, Reinberg D, Croce LD, Shiekhattar R (2007a) Demethylation of H3K27 regulates polycomb recruitment and H2A ubiquitination. Science 318:2-450
82. Lee N, Zhang J, Klose RJ, Erdjument-Bromage H, Tempst P, Jones RS, Zhang Y (2007b) The trithorax-group protein Lid is a histone H3 trimethyl-Lys4 demethylase. Nat Struct Mol Biol 14:2-343
83. Libault M, Tessadori F, Germann S, Snijder B, Fransz P, Gaudin V (2005) The Arabidopsis LHP1 protein is a component of euchromatin. Planta 222:2-925
84. Lindroth AM, Cao X, Jackson JP, Zilberman D, McCallum CM, Henikoff S, Jacobsen SE (2001) Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science 292:2-2080
85. Lindroth AM, Shultis D, Jasencakova Z, Fuchs J, Johnson L, Schubert D, Patnaik D, Pradhan S, Goodrich J, Schubert I, Jenuwein T, Khorasanizadeh S, Jacobsen SE (2004) Dual histone H3 methylation marks at lysines 9 and 27 required for interaction with CHROMOMETHYLASE3. EMBO J 23:2-4296
86. Loidl P (2004) A plant dialect of the histone language. Trends Plant Sci 9:2-90
87. Loury R, Sassone-Corsi P (2004) Analysis of histone phosphorylation: coupling intracellular signaling to chromatin remodeling. Methods Enzymol 377:2-212
88. Luger K, Richmond TJ (1998) The histone tails of the nucleosome. Curr Opin Genet Dev 8:2-146
89. Lusser A, Kölle D, Loidl P (2001) Histone acetylation: lessons from the plant kingdom. Trends Plant Sci 6:2-65
90. Malagnac F, Bartee L, Bender J (2002) An Arabidopsis SET domain protein required for maintenance but not establishment of DNA methylation. EMBO J 21:2-6852
91. Manzanero S, Arana P, Puertas MJ, Houben A (2000) The chromosomal distribution of phosphorylated histone H3 differs between plants and animals at meiosis. Chromosoma 109:2-317
92. Marschner S, Meister A, Blattner FR, Houben A (2007) Evolution and function of B chromosome 45 S rDNA sequences in Brachycome dichromosomatica. Genome 50:2-644
93. Mathieu O, Probst AV, Paszkowski J (2005) Distinct regulation of histone H3 methylation at lysines 27 and 9 by CpG methylation in Arabidopsis. EMBO J 24:2-2791
94. Mathieu O, Reinders J, Aikovski M, Smathajitt C, Paszkowski J (2007) Transgenerational stability of the Arabidopsis epigenome is coordinated by CG methylation. Cell 130:2-862
95. McBlane F, Boyes J (2000) Stimulation of V(D)J recombination by histone acetylation. Curr Biol 10:2-486
96. McMurry MT, Krangel MS (2000) A role for histone acetylation in the developmental regulation of VDJ recombination. Science 287:2-458
97. Metzger E, Wissmann M, Yin N, Müller JM, Schneider R, Peters AHFM, Günther T, Buettner R, Schüle R (2005) LSD1 demethylates repressive histone marks to promote androgen-receptor-dependent transcription. Nature 437:2-439
98. Morris SA, Shibata Y, Noma K, Tsukamoto Y, Warren E, Temple B, Grewal SIS, Strahl BD (2005) Histone H3 K36 methylation is associated with transcription elongation in Schizosaccharomyces pombe. Eukaryot Cell 4:2-1454
99. Morris SA, Rao B, Garcia BA, Hake SB, Diaz RL, Shabanowitz J, Hunt DF, Allis CD, Lieb JD, Strahl BD (2007) Identification of histone H3 lysine 36 acetylation as a highly conserved his-tone modification. J Biol Chem 282:2-7640
100. Nakahigashi K, Jasencakova Z, Schubert I, Goto K (2005) The Arabidopsis heterochromatin protein1 homolog (TERMINAL FLOWER2) silences genes within the euchromatic region but not genes positioned in heterochromatin. Plant Cell Physiol 46:2-1756
101. Nakayama J, Rice JC, Strahl BD, Allis CD, Grewal SIS (2001) Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science 292:2-113
102. Naumann K, Fischer A, Hofmann I, Krauss V, Phalke S, Irmler K, Hause G, Aurich A-C, Dorn R, Jenuwein T, Reuter G (2005) Pivotal role of AtSUVH2 in heterochromatic histone methylation and gene silencing in Arabidopsis. EMBO J 24:2-1429
103. Noma K, Allis CD, Grewal SIS (2001) Transitions in distinct histone H3 methylation patterns at the heterochromatin domain boundaries. Science 293:2-1155
104. Nowak SJ, Corces VG (2000) Phosphorylation of histone H3 correlates with transcriptionally active loci. Genes Dev 14:2-3013
105. Okada T, Endo M, Singh MB, Bhalla PL (2005) Analysis of the histone H3 gene family in Arabidopsis and identification of the male-gamete-specific variant AtMGH3. Plant J 44:2-568
106. Peters AHFM, Kubicek S, Mechtler K, O'Sullivan RJ, Derijck AAHA, Perez-Burgos L, Kohlmaier A, Opravil S, Tachibana M, Shinkai Y, Martens JHA, Jenuwein T (2003) Partitioning and plasticity of repressive histone methylation states in mammalian chromatin. Mol Cell 12:2-1589
107. Plath K, Fang J, Mlynarczyk-Evans SK, Cao R, Worringer KA, Wang H, de la Cruz CC, Otte AP, Panning B, Zhang Y (2003) Role of histone H3 lysine 27 methylation in X inactivation. Science 300:2-135
108. Polioudaki H, Markaki Y, Kourmouli N, Dialynas G, Theodoropoulos PA, Singh PB, Georgatos SD (2004) Mitotic phosphorylation of histone H3 at threonine 3. FEBS Lett 560:2-44
109. Preuss U, Landsberg G, Scheidtmann KH (2003) Novel mitosis-specific phosphorylation of his-tone H3 at Thr11 mediated by Dlk/ZIP kinase. Nucleic Acids Res 31:2-885
110. Prigent C, Dimitrov S (2003) Phosphorylation of serine 10 in histone H3, what for? J Cell Sci 116:2-3685
111. Rice JC, Briggs SD, Ueberheide B, Barber CM, Shabanowitz J, Hunt DF, Shinkai Y, Allis CD (2003) Histone methyltransferases direct different degrees of methylation to define distinct chromatin domains. Mol Cell 12:2-1598
112. Richards EJ, Elgin SCR (2002) Epigenetic codes for heterochromatin formation and silencing: rounding up the usual suspects. Cell 108:2-500
113. Rossi V, Locatelli S, Varotto S, Donn G, Pirona R, Henderson DA, Hartings H, Motto M (2007) Maize histone deacetylase hda101 is involved in plant development, gene transcription, and sequence-specific modulation of histone modification of genes and repeats. Plant Cell 19:2-1162
114. Rudolph T, Yonezawa M, Lein S, Heidrich K, Kubicek S, Schäfer C, Phalke S, Walther M, Schmidt A, Jenuwein T, Reuter G (2007) Heterochromatin formation in Drosophila is initiated through active removal of H3K4 methylation by the LSD1 homolog SU(VAR)3-3. Mol Cell 26: 2-115
115. Salvador LM, Park Y, Cottom J, Maizels ET, Jones JCR, Schillace RV, Carr DW, Cheung P, Allis CD, Jameson JL, Hunzicker-Dunn M (2001) Follicle-stimulating hormone stimulates protein kinase A-mediated histone H3 phosphorylation and acetylation leading to select gene activation in ovarian granulosa cells. J Biol Chem 276:2-40155
116. Sanders SL, Portoso M, Mata J, Bähler J, Allshire RC, Kouzarides T (2004) Methylation of histone H4 lysine 20 controls recruitment of Crb2 to sites of DNA damage. Cell 119:2-614
117. Saze H, Mittelsten Scheid O, Paszkowski J (2003) Maintenance of CpG methylation is essential for epigenetic inheritance during plant gametogenesis. Nat Genet 34:2-69
118. Schotta G, Lachner M, Sarma K, Ebert A, Sengupta R, Reuter G, Reinberg D, Jenuwein T (2004) A silencing pathway to induce H3-K9 and H4-K20 trimethylation at constitutive heterochromatin. Genes Dev 18:2-1262
119. Secombe J, Li L, Carlos L, Eisenman RN (2007) The Trithorax group protein Lid is a trimethyl histone H3K4 demethylase required for dMyc-induced cell growth. Genes Dev 21:2-551
120. Shi J, Dawe RK (2006) Partitioning of the maize epigenome by the number of methyl groups on histone H3 lysines 9 and 27. Genetics 173:2-1583
121. Shi Y-J, Matson C, Lan F, Iwase S, Baba T, Shi Y (2005) Regulation of LSD1 histone demethylase activity by its associated factors. Mol Cell 19:2-864
122. Shi Y, Lan F, Matson C, Mulligan P, Whetstine JR, Cole PA, Casero RA, Shi Y (2004) Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119:2-953
123. Silva J, Mak W, Zvetkova I, Appanah R, Nesterova TB, Webster Z, Peters AHFM, Jenuwein T, Otte AP, Brockdorff N (2003) Establishment of histone h3 methylation on the inactive X chromosome requires transient recruitment of Eed-Enx1 polycomb group complexes. Dev Cell 4:2-495
124. Siroky J, Castiglione MR, Vyskot B (1998) DNA methylation patterns of Melandrium album chromosomes. Chromosome Res 6:2-446
125. Soppe WJJ, Jasencakova Z, Houben A, Kakutani T, Meister A, Huang MS, Jacobsen SE, Schubert I, Fransz PF (2002) DNA methylation controls histone H3 lysine 9 methylation and heterochromatin assembly in Arabidopsis. EMBO J 21:2-6559
126. Sridhar VV, Kapoor A, Zhang K, Zhu J, Zhou T, Hasegawa PM, Bressan RA, Zhu J-K (2007) Control of DNA methylation and heterochromatic silencing by histone H2B deubiquitination. Nature 447:2-738
127. Strahl BD, Allis CD (2000) The language of covalent histone modifications. Nature 403:2-45
128. Sun Z-W, Allis CD (2002) Ubiquitination of histone H2B regulates H3 methylation and gene silencing in yeast. Nature 418:2-108
129. Taddei A, Roche D, Sibarita J-B, Turner BM, Almouzni G (1999) Duplication and maintenance of heterochromatin domains. J Cell Biol 147:2-1166
130. Tamaru H, Selker EU (2001) A histone H3 methyltransferase controls DNA methylation in Neurospora crassa. Nature 414:2-283
131. Tamaru H, Zhang X, McMillen D, Singh PB, Nakayama J, Grewal SI, Allis CD, Cheng X, Selker EU (2003) Trimethylated lysine 9 of histone H3 is a mark for DNA methylation in Neurospora crassa. Nat Genet 34:2-79
132. Tariq M, Saze H, Probst AV, Lichota J, Habu Y, Paszkowski J (2003) Erasure of CpG methylation in Arabidopsis alters patterns of histone H3 methylation in heterochromatin. Proc Natl Acad Sci USA 100:2-8827
133. Thiriet C, Hayes JJ (2005) Chromatin in need of a fix: phosphorylation of H2AX connects chromatin to DNA repair. Mol Cell 18:2-622
134. Tsukada Y, Fang J, Erdjument-Bromage H, Warren ME, Borchers CH, Tempst P, Zhang Y (2006) Histone demethylation by a family of JmjC domain-containing proteins. Nature 439:2-816
135. Turck F, Roudier F, Farrona S, Martin-Magniette M-L, Guillaume E, Buisine N, Gagnot S, Martienssen RA, Coupland G, Colot V (2007) Arabidopsis TFL2/LHP1 specifically associates with genes marked by trimethylation of histone H3 lysine 27. PLoS Genet 3:e86
136. Turner BM, Birley AJ, Lavender J (1992) Histone H4 isoforms acetylated at specific lysine residues define individual chromosomes and chromatin domains in Drosophila polytene nuclei. Cell 69:2-384
137. Turner BM (2000) Histone acetylation and an epigenetic code. BioEssays 22:2-845
138. Vongs A, Kakutani T, Martienssen RA, Richards EJ (1993) Arabidopsis thaliana DNA methylation mutants. Science 260:2-1928
139. Vyskot B, Araya A, Veuskens J, Negrutiu I, Mouras A (1993) DNA methylation of sex chromosomes in a dioecious plant, Melandrium album. Mol Gen Genet 239:2-224
140. Vyskot B, Siroky J, Hladilova R, Belyaev ND, Turner BM (1999) Euchromatic domains in plant chromosomes as revealed by H4 histone acetylation and early DNA replication. Genome 42:2-350
141. Wade PA, Pruss D, Wolffe AP (1997) Histone acetylation: chromatin in action. Trends Biochem Sci 22:2-132
142. Wang X, Zhang Y, Ma Q, Zhang Z, Xue Y, Bao S, Chong K (2007) SKB1-mediated symmetric dimethylation of histone H4R3 controls flowering time in Arabidopsis. EMBO J 26:2-1941
143. Whetstine JR, Nottke A, Lan F, Huarte M, Smolikov S, Chen Z, Spooner E, Li E, Zhang G, Colaiacovo M, Shi Y (2006) Reversal of histone lysine trimethylation by the JMJD2 family of histone demethylases. Cell 125:2-481
144. Wilkinson CRM, Bartlett R, Nurse P, Bird AP (1995) The fission yeast gene pmt1+ encodes a DNA methyltransferase homologue. Nucleic Acids Res 23:2-210
145. Xiang Y, Zhu Z, Han G, Lin H, Xu L, Chen CD (2007) JMJD3 is a histone H3K27 demethylase. Cell Res 17:2-857
146. Yamada T, Fischle W, Sugiyama T, Allis CD, Grewal SIS (2005) The nucleation and maintenance of heterochromatin by a histone deacetylase in fission yeast. Mol Cell 20:2-185
147. Yamane K, Toumazou C, Tsukada Y, Erdjument-Bromage H, Tempst P, Wong J, Zhang Y (2006) JHDM2A, a JmjC-containing H3K9 demethylase, facilitates transcription activation by androgen receptor. Cell 125:2-495
148. Zhang X, Li X, Marshall JB, Zhong CX, Dawe RK (2005) Phosphoserines on maize CENTROMERIC HISTONE H3 and histone H3 demarcate the centromere and pericentromere during chromosome segregation. Plant Cell 17:2-583
149. Zhang X, Clarenz O, Cokus S, Bernatavichute YV, Pellegrini M, Goodrich J, Jacobsen SE (2007a) Whole-genome analysis of histone H3 lysine 27 trimethylation in Arabidopsis. PLoS Biol 5:e129
150. Zhang X, Germann S, Blus BJ, Khorasanizadeh S, Gaudin V, Jacobsen SE (2007b) The Arabidopsis LHP1 protein colocalizes with histone H3 Lys27 trimethylation. Nat Struct Mol Biol 14:2-871
151. Zhu P, Zhou W, Wang J, Puc J, Ohgi KA, Erdjument-Bromage H, Tempst P, Glass CK, Rosenfeld MG (2007) A histone H2A deubiquitinase complex coordinating histone acetylation and H1 dissociation in transcriptional regulation. Mol Cell 27:2-621
152. Zilberman D, Gehring M, Tran RK, Ballinger T, Henikoff S (2007) Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat Genet 39:2-69