1932

Abstract

Eukaryotic genomes often contain large quantities of potentially deleterious sequences, such as transposons. One strategy for mitigating this risk is to package such sequences into so-called constitutive heterochromatin, where the dense chromatin environment is thought to inhibit transcription by excluding transcription factors and RNA polymerase. This type of model makes it tempting to think of heterochromatin as an inert region that is isolated from the rest of the nucleus. Recent work on heterochromatin, however, reveals that it is a dynamic environment. Despite its dense packaging, heterochromatin must remain accessible for a host of processes, including DNA replication and repair, and, paradoxically, transcription. In plants, transcripts produced by specialized RNA polymerases are used to target regions of the genome for silencing via DNA methylation. Thus, the maintenance of heterochromatin requires a careful balancing act of access and exclusion, which is achieved through the action of a host of interrelated pathways.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-genet-112414-055048
2015-11-23
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/genet/49/1/annurev-genet-112414-055048.html?itemId=/content/journals/10.1146/annurev-genet-112414-055048&mimeType=html&fmt=ahah

Literature Cited

  1. Abbas T, Shibata E, Park J, Jha S, Karnani N, Dutta A. 1.  2010. CRL4Cdt2 regulates cell proliferation and histone gene expression by targeting PR-Set7/Set8 for degradation. Mol. Cell 40:9–21 [Google Scholar]
  2. Aggarwal BD, Calvi BR. 2.  2004. Chromatin regulates origin activity in Drosophila follicle cells. Nature 430:372–76 [Google Scholar]
  3. Ahmad K, Henikoff S. 3.  2002. Histone H3 variants specify modes of chromatin assembly. PNAS 99:Suppl.) 4:16477–84 [Google Scholar]
  4. Arias EE, Walter JC. 4.  2007. Strength in numbers: preventing rereplication via multiple mechanisms in eukaryotic cells. Gene Dev. 21:497–518 [Google Scholar]
  5. Bank EM, Gruenbaum Y. 5.  2011. The nuclear lamina and heterochromatin: a complex relationship. Biochem. Soc. Trans. 39:1705–9 [Google Scholar]
  6. Baroux C, Pecinka A, Fuchs J, Schubert I, Grossniklaus U. 6.  2007. The triploid endosperm genome of Arabidopsis adopts a peculiar, parental-dosage-dependent chromatin organization. Plant Cell 19:1782–94 [Google Scholar]
  7. Bell O, Schwaiger M, Oakeley EJ, Lienert F, Beisel C. 7.  et al. 2010. Accessibility of the Drosophila genome discriminates PcG repression, H4K16 acetylation and replication timing. Nat. Struct. Mol. Biol 17:894–900 [Google Scholar]
  8. Berezney R, Dubey DD, Huberman JA. 8.  2000. Heterogeneity of eukaryotic replicons, replicon clusters, and replication foci. Chromosoma 108:471–84 [Google Scholar]
  9. Berkovich E, Monnat RJ, Kastan MB. 9.  2007. Roles of ATM and NBS1 in chromatin structure modulation and DNA double-strand break repair. Nat. Cell Biol. 9:683–90 [Google Scholar]
  10. Bernatavichute YV, Zhang X, Cokus S, Pellegrini M, Jacobsen SE. 10.  2008. Genome-wide association of histone H3 lysine nine methylation with CHG DNA methylation in Arabidopsis thaliana. PLOS ONE 3:e3156 [Google Scholar]
  11. Boveri T. 11.  1904. Ergebnisse über die Konstitution der Chromatischen Substanz des Zellkerns Jena, Germ: Gustav Fischer
  12. Brown SW. 12.  1966. Heterochromatin. Science 151:417–25 [Google Scholar]
  13. Burlingame RW, Love WE, Wang BC, Hamlin R, Xuong NH, Moudrianakis EN. 13.  1985. Crystallographic structure of the octameric histone core of the nucleosome at a resolution of 3.3 A. Science 228:546–53 [Google Scholar]
  14. Cadoret JC, Meisch F, Hassan-Zadeh V, Luyten I, Guillet C. 14.  et al. 2008. Genome-wide studies highlight indirect links between human replication origins and gene regulation. PNAS 105:15837–42 [Google Scholar]
  15. Campi M, D'Andrea L, Emiliani J, Casati P. 15.  2012. Participation of chromatin-remodeling proteins in the repair of ultraviolet-B-damaged DNA. Plant Physiol. 158:981–95 [Google Scholar]
  16. Cann KL, Dellaire G. 16.  2011. Heterochromatin and the DNA damage response: the need to relax. Biochem. Cell. Biol. 89:45–60 [Google Scholar]
  17. Cao X, Jacobsen SE. 17.  2002. Locus-specific control of asymmetric and CpNpG methylation by the DRM and CMT3 methyltransferase genes. PNAS 99:Suppl. 4:16491–98 [Google Scholar]
  18. Cao X, Jacobsen SE. 18.  2002. Role of the Arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing. Curr. Biol. 12:1138–44 [Google Scholar]
  19. Castel SE, Martienssen RA. 20.  2013. RNA interference in the nucleus: roles for small RNAs in transcription, epigenetics and beyond. Nat. Rev. Genet. 14:100–12 [Google Scholar]
  20. Cayrou C, Coulombe P, Vigneron A, Stanojcic S, Ganier O. 21.  et al. 2011. Genome-scale analysis of metazoan replication origins reveals their organization in specific but flexible sites defined by conserved features. Genome Res. 21:1438–49 [Google Scholar]
  21. Chiolo I, Minoda A, Colmenares SU, Polyzos A, Costes SV, Karpen GH. 22.  2011. Double-strand breaks in heterochromatin move outside of a dynamic HP1a domain to complete recombinational repair. Cell 144:732–44 [Google Scholar]
  22. Ciska M, Masuda K, Moreno Diaz de la Espina S. 23.  2013. Lamin-like analogues in plants: the characterization of NMCP1 in Allium cepa. J. Exp. Bot. 64:1553–64 [Google Scholar]
  23. Copenhaver GP, Pikaard CS. 24.  1996. RFLP and physical mapping with an rDNA-specific endonuclease reveals that nucleolus organizer regions of Arabidopsis thaliana adjoin the telomeres on chromosomes 2 and 4. Plant J. Cell Mol. Biol. 9:259–72 [Google Scholar]
  24. Costas C, Sanchez MD, Stroud H, Yu Y, Oliveros JC. 25.  et al. 2011. Genome-wide mapping of Arabidopsis thaliana origins of DNA replication and their associated epigenetic marks. Nat. Struct. Mol. Biol 18:395–400 [Google Scholar]
  25. Costas C, Sanchez Mde L, Sequeira-Mendes J, Gutierrez C. 26.  2011. Progress in understanding DNA replication control. Plant Sci 181:203–9 [Google Scholar]
  26. Cvetic C, Walter JC. 27.  2005. Eukaryotic origins of DNA replication: Could you please be more specific?. Semin. Cell Dev. Biol. 16:343–53 [Google Scholar]
  27. Dekker J, Rippe K, Dekker M, Kleckner N. 28.  2002. Capturing chromosome conformation. Science 295:1306–11 [Google Scholar]
  28. Dellaire G, Kepkay R, Bazett-Jones DP. 29.  2009. High resolution imaging of changes in the structure and spatial organization of chromatin, γ-H2A.X and the MRN complex within etoposide-induced DNA repair foci. Cell Cycle 8:3750–69 [Google Scholar]
  29. Dittmer TA, Stacey NJ, Sugimoto-Shirasu K, Richards EJ. 30.  2007. LITTLE NUCLEI genes affecting nuclear morphology in Arabidopsis thaliana. Plant Cell 19:2793–803 [Google Scholar]
  30. Du JM, Zhong XH, Bernatavichute YV, Stroud H, Feng SH. 31.  et al. 2012. Dual binding of chromomethylase domains to H3K9me2-containing nucleosomes directs DNA methylation in plants. Cell 151:167–80 [Google Scholar]
  31. Dutta A. 32.  2007. Chaotic license for genetic instability and cancer. Nat. Genet. 39:10–11 [Google Scholar]
  32. Earley KW, Pontvianne F, Wierzbicki AT, Blevins T, Tucker S. 33.  et al. 2010. Mechanisms of HDA6-mediated rRNA gene silencing: suppression of intergenic Pol II transcription and differential effects on maintenance versus siRNA-directed cytosine methylation. Genes Dev. 24:1119–32 [Google Scholar]
  33. Eaton ML, Prinz JA, MacAlpine HK, Tretyakov G, Kharchenko PV, MacAlpine DM. 34.  2011. Chromatin signatures of the Drosophila replication program. Genome Res. 21:164–74 [Google Scholar]
  34. Edenberg HJ, Huberman JA. 35.  1975. Eukaryotic chromosome replication. Annu. Rev. Genet. 9:245–84 [Google Scholar]
  35. Fadloun A, Eid A, Torres-Padilla ME. 36.  2013. Mechanisms and dynamics of heterochromatin formation during mammalian development: closed paths and open questions. Curr. Top. Dev. Biol. 104:1–45 [Google Scholar]
  36. Falck J, Coates J, Jackson SP. 37.  2005. Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage. Nature 434:605–11 [Google Scholar]
  37. Falk M, Lukasova E, Kozubek S. 38.  2010. Higher-order chromatin structure in DSB induction, repair and misrepair. Mutat. Res. 704:88–100 [Google Scholar]
  38. Farkash-Amar S, Lipson D, Polten A, Goren A, Helmstetter C. 39.  et al. 2008. Global organization of replication time zones of the mouse genome. Genome Res. 18:1562–70 [Google Scholar]
  39. Finnegan EJ, Dennis ES. 40.  1993. Isolation and identification by sequence homology of a putative cytosine methyltransferase from Arabidopsis thaliana. Nucleic Acids Res. 21:2383–88 [Google Scholar]
  40. Fransz P, De Jong JH, Lysak M, Castiglione MR, Schubert I. 41.  2002. Interphase chromosomes in Arabidopsis are organized as well defined chromocenters from which euchromatin loops emanate. PNAS 99:14584–89 [Google Scholar]
  41. Galbraith DW, Harkins KR, Knapp S. 42.  1991. Systemic endopolyploidy in Arabidopsis thaliana. Plant Physiol. 96:985–89 [Google Scholar]
  42. Goodarzi AA, Noon AT, Deckbar D, Ziv Y, Shiloh Y. 43.  et al. 2008. ATM signaling facilitates repair of DNA double-strand breaks associated with heterochromatin. Mol. Cell 31:167–77 [Google Scholar]
  43. Goodrich J, Puangsomlee P, Martin M, Long D, Meyerowitz EM, Coupland G. 44.  1997. A polycomb-group gene regulates homeotic gene expression in Arabidopsis. Nature 386:44–51 [Google Scholar]
  44. Grewal SIS, Moazed D. 45.  2003. Heterochromatin and epigenetic control of gene expression. Science 301:798–802 [Google Scholar]
  45. Haaf T, Schmid M. 46.  1991. Chromosome topology in mammalian interphase nuclei. Exp. Cell Res. 192:325–32 [Google Scholar]
  46. Haag JR, Ream TS, Marasco M, Nicora CD, Norbeck AD. 47.  et al. 2012. In vitro transcription activities of Pol IV, Pol V, and RDR2 reveal coupling of Pol IV and RDR2 for dsRNA synthesis in plant RNA silencing. Mol. Cell 48:811–18 [Google Scholar]
  47. Hartl T, Boswell C, Orr-Weaver TL, Bosco G. 48.  2007. Developmentally regulated histone modifications in Drosophila follicle cells: initiation of gene amplification is associated with histone H3 and H4 hyperacetylation and H1 phosphorylation. Chromosoma 116:197–214 [Google Scholar]
  48. Hayashi MT, Takahashi TS, Nakagawa T, Nakayama J, Masukata H. 49.  2009. The heterochromatin protein Swi6/HP1 activates replication origins at the pericentromeric region and silent mating-type locus. Nat. Cell Biol. 11:357–62 [Google Scholar]
  49. Heidenreich E, Novotny R, Kneidinger B, Holzmann V, Wintersberger U. 50.  2003. Non-homologous end joining as an important mutagenic process in cell cycle-arrested cells. Embo J 22:2274–83 [Google Scholar]
  50. Heitz E. 51.  1928. Das Heterochromatin der Moose. I. Jahrb. Wiss. Bot. 69:762–818 [Google Scholar]
  51. Hennig L, Derkacheva M. 52.  2009. Diversity of polycomb group complexes in plants: same rules, different players?. Trends Genet. 25:414–23 [Google Scholar]
  52. Herr AJ, Jensen MB, Dalmay T, Baulcombe DC. 53.  2005. RNA polymerase IV directs silencing of endogenous DNA. Science 308:118–20 [Google Scholar]
  53. Hiratani I, Leskovar A, Gilbert DM. 54.  2004. Differentiation-induced replication-timing changes are restricted to AT-rich/long interspersed nuclear element (LINE)-rich isochores. PNAS 101:16861–66 [Google Scholar]
  54. Hiratani I, Ryba T, Itoh M, Yokochi T, Schwaiger M. 55.  et al. 2008. Global reorganization of replication domains during embryonic stem cell differentiation. PLOS Biol. 6:e245 [Google Scholar]
  55. Hook SS, Lin JJ, Dutta A. 56.  2007. Mechanisms to control rereplication and implications for cancer. Curr. Opin. Cell Biol. 19:663–71 [Google Scholar]
  56. House NC, Koch MR, Freudenreich CH. 57.  2014. Chromatin modifications and DNA repair: beyond double-strand breaks. Front. Genet. 5:296 [Google Scholar]
  57. Huff JT, Zilberman D. 58.  2014. Dnmt1-independent CG methylation contributes to nucleosome positioning in diverse eukaryotes. Cell 156:1286–97 [Google Scholar]
  58. Hyrien O, Maric C, Mechali M. 59.  1995. Transition in specification of embryonic metazoan DNA-replication origins. Science 270:994–97 [Google Scholar]
  59. Ivanov AV, Peng HZ, Yurchenko V, Yap KL, Negorev DG. 60.  et al. 2007. PHD domain-mediated E3 ligase activity directs intramolecular sumoylation of an adjacent bromodomain required for gene silencing. Mol. Cell 28:823–37 [Google Scholar]
  60. Jaberaboansari A, Nelson GB, Roti JLR, Wheeler KT. 61.  1988. Postirradiation alterations of neuronal chromatin structure. Radiat. Res. 114:94–104 [Google Scholar]
  61. Jackson JP, Lindroth AM, Cao X, Jacobsen SE. 62.  2002. Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416:556–60 [Google Scholar]
  62. Jacob Y, Bergamin E, Donoghue MT, Mongeon V, LeBlanc C. 63.  et al. 2014. Selective methylation of histone H3 variant H3.1 regulates heterochromatin replication. Science 343:1249–53 [Google Scholar]
  63. Jacob Y, Feng S, LeBlanc CA, Bernatavichute YV, Stroud H. 64.  et al. 2009. ATXR5 and ATXR6 are H3K27 monomethyltransferases required for chromatin structure and gene silencing. Nat. Struct. Mol. Biol 16:763–68 [Google Scholar]
  64. Jacob Y, Michaels SD. 65.  2009. H3K27me1 is E(z) in animals, but not in plants. Epigenetics 4:366–69 [Google Scholar]
  65. Jacob Y, Stroud H, LeBlanc C, Feng SH, Zhuo LT. 66.  et al. 2010. Regulation of heterochromatic DNA replication by histone H3 lysine 27 methyltransferases. Nature 466:987–91 [Google Scholar]
  66. Jeddeloh JA, Stokes TL, Richards EJ. 67.  1999. Maintenance of genomic methylation requires a SWI2/SNF2-like protein. Nat. Genet. 22:94–97 [Google Scholar]
  67. Johnson DS, Mortazavi A, Myers RM, Wold B. 68.  2007. Genome-wide mapping of in vivo protein-DNA interactions. Science 316:1497–502 [Google Scholar]
  68. Johnson LM, Bostick M, Zhang XY, Kraft E, Henderson I. 69.  et al. 2007. The SRA methyl-cytosine-binding domain links DNA and histone methylation. Curr. Biol. 17:379–84 [Google Scholar]
  69. Johnson LM, Du J, Hale CJ, Bischof S, Feng S. 70.  et al. 2014. SRA- and SET-domain-containing proteins link RNA polymerase V occupancy to DNA methylation. Nature 507:124–28 [Google Scholar]
  70. Johnson LM, Law JA, Khattar A, Henderson IR, Jacobsen SE. 71.  2008. SRA-domain proteins required for DRM2-mediated de novo DNA methylation. PLOS Genet. 4:e1000280 [Google Scholar]
  71. Kankel MW, Ramsey DE, Stokes TL, Flowers SK, Haag JR. 72.  et al. 2003. Arabidopsis MET1 cytosine methyltransferase mutants. Genetics 163:1109–22 [Google Scholar]
  72. Kawashima T, Berger F. 73.  2014. Epigenetic reprogramming in plant sexual reproduction. Nat. Rev. Genet. 15:613–24 [Google Scholar]
  73. Kossel A. 74.  1911. Über die chemische Beschaffenheit des Zellkerns Münch Med Wschr 585 Stockholm, Swed: P.A. Norstedt
  74. Kuo AJ, Song J, Cheung P, Ishibe-Murakami S, Yamazoe S. 75.  et al. 2012. The BAH domain of ORC1 links H4K20me2 to DNA replication licensing and Meier-Gorlin syndrome. Nature 484:115–19 [Google Scholar]
  75. Kurz EU, Lees-Miller SP. 76.  2004. DNA damage-induced activation of ATM and ATM-dependent signaling pathways. DNA Rep. 3:889–900 [Google Scholar]
  76. Lario LD, Ramirez-Parra E, Gutierrez C, Spampinato CP, Casati P. 77.  2013. ANTI-SILENCING FUNCTION1 proteins are involved in ultraviolet-induced DNA damage repair and are cell cycle regulated by E2F transcription factors in Arabidopsis. Plant Physiol. 162:1164–77 [Google Scholar]
  77. Law JA, Ausin I, Johnson LM, Vashisht AA, Zhu JK. 78.  et al. 2010. A protein complex required for polymerase V transcripts and RNA-directed DNA methylation in Arabidopsis. Curr. Biol. 20:951–56 [Google Scholar]
  78. Law JA, Du J, Hale CJ, Feng S, Krajewski K. 79.  et al. 2013. Polymerase IV occupancy at RNA-directed DNA methylation sites requires SHH1. Nature 498:385–89 [Google Scholar]
  79. Law JA, Jacobsen SE. 80.  2009. Molecular biology. Dynamic DNA methylation. Science 323:1568–69 [Google Scholar]
  80. Law JA, Jacobsen SE. 81.  2010. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat. Rev. Genet. 11:204–20 [Google Scholar]
  81. Law JA, Vashisht AA, Wohlschlegel JA, Jacobsen SE. 82.  2011. SHH1, a homeodomain protein required for DNA methylation, as well as RDR2, RDM4, and chromatin remodeling factors, associate with RNA polymerase IV. PLOS Genet. 7:e1002195 [Google Scholar]
  82. Lee JH, Paull TT. 83.  2005. ATM activation by DNA double-strand breaks through the Mre11-Rad50-Nbs1 complex. Science 308:551–54 [Google Scholar]
  83. Lee TI, Jenner RG, Boyer LA, Guenther MG, Levine SS. 84.  et al. 2006. Control of developmental regulators by polycomb in human embryonic stem cells. Cell 125:301–13 [Google Scholar]
  84. Lewis PW, Beall EL, Fleischer TC, Georlette D, Link AJ, Botchan MR. 85.  2004. Identification of a Drosophila Myb-E2F2/RBF transcriptional repressor complex. Genes Dev. 18:2929–40 [Google Scholar]
  85. Li E, Bestor TH, Jaenisch R. 86.  1992. Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69:915–26 [Google Scholar]
  86. Li X, Lee YK, Jeng JC, Yen Y, Schultz DC. 87.  et al. 2007. Role for KAP1 serine 824 phosphorylation and sumoylation/desumoylation switch in regulating KAP1-mediated transcriptional repression. J. Biol. Chem. 282:36177–89 [Google Scholar]
  87. Liang F, Han MG, Romanienko PJ, Jasin M. 88.  1998. Homology-directed repair is a major double-strand break repair pathway in mammalian cells. PNAS 95:5172–77 [Google Scholar]
  88. Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, Ragoczy T. 89.  et al. 2009. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326:289–93 [Google Scholar]
  89. Lindahl T. 90.  1993. Instability and decay of the primary structure of DNA. Nature 362:709–15 [Google Scholar]
  90. Lindroth AM, Shultis D, Jasencakova Z, Fuchs J, Johnson L. 91.  et al. 2004. Dual histone H3 methylation marks at lysines 9 and 27 required for interaction with CHROMOMETHYLASE3. EMBO J. 23:4146–55 [Google Scholar]
  91. Liu ZW, Shao CR, Zhang CJ, Zhou JX, Zhang SW. 92.  et al. 2014. The SET domain proteins SUVH2 and SUVH9 are required for Pol V occupancy at RNA-directed DNA methylation loci. PLOS Genet. 10:e1003948 [Google Scholar]
  92. Long Q, Rabanal FA, Meng D, Huber CD, Farlow A. 93.  et al. 2013. Massive genomic variation and strong selection in Arabidopsis thaliana lines from Sweden. Nat. Genet. 45:884–90 [Google Scholar]
  93. MacAlpine HK, Gordan R, Powell SK, Hartemink AJ, MacAlpine DM. 94.  2010. Drosophila ORC localizes to open chromatin and marks sites of cohesin complex loading. Genome Res. 20:201–11 [Google Scholar]
  94. Madigan JP, Chotkowski HL, Glaser RL. 95.  2002. DNA double-strand break-induced phosphorylation of Drosophila histone variant H2Av helps prevent radiation-induced apoptosis. Nucleic Acids Res. 30:3698–705 [Google Scholar]
  95. Malagnac F, Bartee L, Bender J. 96.  2002. An Arabidopsis SET domain protein required for maintenance but not establishment of DNA methylation. EMBO J. 21:6842–52 [Google Scholar]
  96. Manuelidis L. 97.  1985. Indications of centromere movement during interphase and differentiation. Ann. N. Y. Acad. Sci. 450:205–21 [Google Scholar]
  97. Martin C, Zhang Y. 98.  2005. The diverse functions of histone lysine methylation. Nat. Rev Mol. Cell Biol. 6:838–49 [Google Scholar]
  98. Mathieu O, Jasencakova Z, Vaillant I, Gendrel AV, Colot V. 99.  et al. 2003. Changes in 5S rDNA chromatin organization and transcription during heterochromatin establishment in Arabidopsis. Plant Cell 15:2929–39 [Google Scholar]
  99. Mathieu O, Probst AV, Paszkowski J. 100.  2005. Distinct regulation of histone H3 methylation at lysines 27 and 9 by CpG methylation in Arabidopsis. EMBO J. 24:2783–91 [Google Scholar]
  100. Mechali M. 101.  2010. Eukaryotic DNA replication origins: many choices for appropriate answers. Nat. Rev. Mol. Cell Biol. 11:728–38 [Google Scholar]
  101. Mehrotra S, Maqbool SB, Kolpakas A, Murnen K, Calvi BR. 102.  2008. Endocycling cells do not apoptose in response to DNA rereplication genotoxic stress. Gene Dev. 22:3158–71 [Google Scholar]
  102. Mehrotra S, McKim KS. 103.  2006. Temporal analysis of meiotic DNA double-strand break formation and repair in Drosophila females. PLOS Genet. 2:1883–97 [Google Scholar]
  103. Miotto B, Struhl K. 104.  2008. HBO1 histone acetylase is a coactivator of the replication licensing factor Cdt1. Gene Dev. 22:2633–38 [Google Scholar]
  104. Miotto B, Struhl K. 105.  2010. HBO1 histone acetylase activity is essential for DNA Replication licensing and inhibited by geminin. Mol. Cell 37:57–66 [Google Scholar]
  105. Moissiard G, Cokus SJ, Cary J, Feng S, Billi AC. 106.  et al. 2012. MORC family ATPases required for heterochromatin condensation and gene silencing. Science 336:1448–51 [Google Scholar]
  106. Mullenders LHF, Vanzeeland AA, Natarajan AT. 107.  1983. Comparison of DNA loop size and super-coiled domain size in human cells. Mutat. Res. 112:245–52 [Google Scholar]
  107. Muller HJ, Painter TS. 108.  1932. The differentiation of the sex chromosomes of Drosophila into genetically active and inert regions. Zeit. Ind. Abst. Vererb.50
  108. Naumann K, Fischer A, Hofmann I, Krauss V, Phalke S. 109.  et al. 2005. Pivotal role of AtSUVH2 in heterochromatic histone methylation and gene silencing in Arabidopsis. EMBO J. 24:1418–29 [Google Scholar]
  109. O'Carroll D, Erhardt S, Pagani M, Barton SC, Surani MA, Jenuwein T. 110.  2001. The polycomb-group gene Ezh2 is required for early mouse development. Mol. Cell. Biol. 21:4330–36 [Google Scholar]
  110. Onodera Y, Haag JR, Ream T, Costa Nunes P, Pontes O, Pikaard CS. 111.  2005. Plant nuclear RNA polymerase IV mediates siRNA and DNA methylation-dependent heterochromatin formation. Cell 120:613–22 [Google Scholar]
  111. Pasquale B. 112.  1908. Sulle cinesi vegetative del “Cynomorium coccineum L.”. N Giorn Bot Ital N Ser. 15:15 [Google Scholar]
  112. Pearson CE, Edamura KN, Cleary JD. 113.  2005. Repeat instability: mechanisms of dynamic mutations. Nat. Rev. Genet. 6:729–42 [Google Scholar]
  113. Peng JC, Karpen GH. 114.  2008. Epigenetic regulation of heterochromatic DNA stability. Curr. Opin. Genet. Dev. 18:204–11 [Google Scholar]
  114. Perry P, Sauer S, Billon N, Richardson WD, Spivakov M. 115.  et al. 2004. A dynamic switch in the replication timing of key regulator genes in embryonic stem cells upon neural induction. Cell Cycle 3:1645–50 [Google Scholar]
  115. Pien S, Grossniklaus U. 116.  2007. Polycomb group and trithorax group proteins in Arabidopsis. Biochim. Biophys. Acta 1769:375–82 [Google Scholar]
  116. Pikaard CS, Mittelsten Scheid O. 117.  2014. Epigenetic regulation in plants. Cold Spring Harb. Perspect. Biol. 6:a019315 [Google Scholar]
  117. Pontes O, Lawrence RJ, Silva M, Preuss S, Costa-Nunes P. 118.  et al. 2007. Postembryonic establishment of megabase-scale gene silencing in nucleolar dominance. PLOS ONE 2:e1157 [Google Scholar]
  118. Pontes O, Li CF, Costa Nunes P, Haag J, Ream T. 119.  et al. 2006. The Arabidopsis chromatin-modifying nuclear siRNA pathway involves a nucleolar RNA processing center. Cell 126:79–92 [Google Scholar]
  119. Pontvianne F, Blevins T, Chandrasekhara C, Feng W, Stroud H. 120.  et al. 2012. Histone methyltransferases regulating rRNA gene dose and dosage control in Arabidopsis. Genes Dev 26:945–57 [Google Scholar]
  120. Pontvianne F, Blevins T, Chandrasekhara C, Mozgova I, Hassel C. 121.  et al. 2013. Subnuclear partitioning of rRNA genes between the nucleolus and nucleoplasm reflects alternative epiallelic states. Genes Dev. 27:1545–50 [Google Scholar]
  121. Price BD, D'Andrea AD. 122.  2013. Chromatin remodeling at DNA double-strand breaks. Cell 152:1344–54 [Google Scholar]
  122. Qi Y, He X, Wang XJ, Kohany O, Jurka J, Hannon GJ. 123.  2006. Distinct catalytic and non-catalytic roles of ARGONAUTE4 in RNA-directed DNA methylation. Nature 443:1008–12 [Google Scholar]
  123. Ramirez-Parra E, Gutierrez C. 124.  2007. E2F regulates FASCIATA1, a chromatin assembly gene whose loss switches on the endocycle and activates gene expression by changing the epigenetic status. Plant Physiol. 144:105–20 [Google Scholar]
  124. Raynaud C, Sozzani R, Glab N, Domenichini S, Perennes C. 125.  et al. 2006. Two cell-cycle regulated SET-domain proteins interact with proliferating cell nuclear antigen (PCNA) in Arabidopsis. Plant J. 47:395–407 [Google Scholar]
  125. Remus D, Diffley JFX. 126.  2009. Eukaryotic DNA replication control: lock and load, then fire. Curr. Opin. Cell Biol. 21:771–77 [Google Scholar]
  126. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM. 127.  1998. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 273:5858–68 [Google Scholar]
  127. Ronemus MJ, Galbiati M, Ticknor C, Chen J, Dellaporta SL. 128.  1996. Demethylation-induced developmental pleiotropy in Arabidopsis. Science 273:654–57 [Google Scholar]
  128. Roti JLR, Wright WD. 129.  1987. Visualization of DNA loops in nucleoids from Hela cells: assays for DNA damage and repair. Cytometry 8:461–67 [Google Scholar]
  129. Rouse J, Jackson SP. 130.  2002. Interfaces between the detection, signaling, and repair of DNA damage. Science 297:547–51 [Google Scholar]
  130. Sakamoto Y, Takagi S. 131.  2013. LITTLE NUCLEI 1 and 4 regulate nuclear morphology in Arabidopsis thaliana. Plant Cell Physiol. 54:622–33 [Google Scholar]
  131. Sanchez MD, Gutierrez C. 132.  2009. Arabidopsis ORC1 is a PHD-containing H3K4me3 effector that regulates transcription. PNAS 106:2065–70 [Google Scholar]
  132. Schoft VK, Chumak N, Mosiolek M, Slusarz L, Komnenovic V. 133.  et al. 2009. Induction of RNA-directed DNA methylation upon decondensation of constitutive heterochromatin. EMBO Rep. 10:1015–21 [Google Scholar]
  133. Schubeler D, Scalzo D, Kooperberg C, van Steensel B, Delrow J, Groudine M. 134.  2002. Genome-wide DNA replication profile for Drosophila melanogaster: a link between transcription and replication timing. Nat. Genet. 32:438–42 [Google Scholar]
  134. Schwaiger M, Stadler MB, Bell O, Kohler H, Oakeley EJ, Schubeler D. 135.  2009. Chromatin state marks cell-type- and gender-specific replication of the Drosophila genome. Gene Dev. 23:589–601 [Google Scholar]
  135. Schwartz YB, Kahn TG, Nix DA, Li XY, Bourgon R. 136.  et al. 2006. Genome-wide analysis of polycomb targets in Drosophila melanogaster. Nat. Genet. 38:700–5 [Google Scholar]
  136. Shahbazian MD, Grunstein M. 137.  2007. Functions of site-specific histone acetylation and deacetylation. Annu. Rev. Biochem. 76:75–100 [Google Scholar]
  137. She W, Baroux C. 138.  2014. Chromatin dynamics during plant sexual reproduction. Front. Plant Sci. 5:354 [Google Scholar]
  138. She W, Grimanelli D, Rutowicz K, Whitehead MW, Puzio M. 139.  et al. 2013. Chromatin reprogramming during the somatic-to-reproductive cell fate transition in plants. Development 140:4008–19 [Google Scholar]
  139. Shechter D, Costanzo V, Gautier J. 140.  2004. Regulation of DNA replication by ATR: signaling in response to DNA intermediates. DNA Rep. 3:901–8 [Google Scholar]
  140. Shinomiya T, Ina S. 141.  1991. Analysis of chromosomal replicons in early embryos of Drosophila melanogaster by two-dimensional gel electrophoresis. Nucleic Acids Res. 19:3935–41 [Google Scholar]
  141. Shirahige K, Iwasaki T, Rashid MB, Ogasawara N, Yoshikawa H. 142.  1993. Location and characterization of autonomously replicating sequences from chromosome VI of Saccharomyces cerevisiae. Mol. Cell Biol. 13:5043–56 [Google Scholar]
  142. Slotkin RK, Vaughn M, Borges F, Tanurdzic M, Becker JD. 143.  et al. 2009. Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136:461–72 [Google Scholar]
  143. Smith LM, Pontes O, Searle I, Yelina N, Yousafzai FK. 144.  et al. 2007. An SNF2 protein associated with nuclear RNA silencing and the spread of a silencing signal between cells in Arabidopsis. Plant Cell 19:1507–21 [Google Scholar]
  144. Sonoda E, Hochegger H, Saberi A, Taniguchi Y, Takeda S. 145.  2006. Differential usage of non-homologous end-joining and homologous recombination in double strand break repair. DNA Rep. 5:1021–29 [Google Scholar]
  145. Soppe WJJ, Jasencakova Z, Houben A, Kakutani T, Meister A. 146.  et al. 2002. DNA methylation controls histone H3 lysine 9 methylation and heterochromatin assembly in Arabidopsis. EMBO J. 21:6549–59 [Google Scholar]
  146. Sutton WS. 147.  1903. The chromosomes in heredity. Biol. Bull. 4:231–50 [Google Scholar]
  147. Symeonidou IE, Taraviras S, Lygerou Z. 148.  2012. Control over DNA replication in time and space. FEBS Lett. 586:2803–12 [Google Scholar]
  148. Takeda S, Tadele Z, Hofmann I, Probst AV, Angelis KJ. 149.  et al. 2004. BRU1, a novel link between responses to DNA damage and epigenetic gene silencing in Arabidopsis. Genes Dev. 18:782–93 [Google Scholar]
  149. Tan M, Luo H, Lee S, Jin F, Yang JS. 150.  et al. 2011. Identification of 67 histone marks and histone lysine crotonylation as a new type of histone modification. Cell 146:1016–28 [Google Scholar]
  150. Tardat M, Brustel J, Kirsh O, Lefevbre C, Callanan M. 151.  et al. 2010. The histone H4 Lys 20 methyltransferase PR-Set7 regulates replication origins in mammalian cells. Nat. Cell Biol. 12:1086–93 [Google Scholar]
  151. Tardat M, Murr R, Herceg Z, Sardet C, Julien E. 152.  2007. PR-Set7-dependent lysine methylation ensures genome replication and stability through S phase. J. Cell Biol. 179:1413–26 [Google Scholar]
  152. Tolhuis B, Muijrers I, de Wit E, Teunissen H, Talhout W. 153.  et al. 2006. Genome-wide profiling of PRC1 and PRC2 polycomb chromatin binding in Drosophila melanogaster. Nat. Genet. 38:694–99 [Google Scholar]
  153. Torres-Rosell J, Sunjevaric I, De Piccoli G, Sacher M, Eckert-Boulet N. 154.  et al. 2007. The Smc5-Smc6 complex and SUMO modification of Rad52 regulates recombinational repair at the ribosomal gene locus. Nat. Cell Biol. 9:923–31 [Google Scholar]
  154. Tucker S, Vitins A, Pikaard CS. 155.  2010. Nucleolar dominance and ribosomal RNA gene silencing. Curr. Opin. Cell Biol. 22:351–56 [Google Scholar]
  155. Wang H, Dittmer TA, Richards EJ. 156.  2013. Arabidopsis CROWDED NUCLEI (CRWN) proteins are required for nuclear size control and heterochromatin organization. BMC Plant Biol. 13:200 [Google Scholar]
  156. Wierzbicki AT, Haag JR, Pikaard CS. 157.  2008. Noncoding transcription by RNA polymerase Pol IVb/Pol V mediates transcriptional silencing of overlapping and adjacent genes. Cell 135:635–48 [Google Scholar]
  157. Woodfine K, Fiegler H, Beare DM, Collins JE, McCann OT. 158.  et al. 2004. Replication timing of the human genome. Hum. Mol. Genet. 13:191–202 [Google Scholar]
  158. Wyman C, Kanaar R. 159.  2006. DNA double-strand break repair: all's well that ends well. Annu. Rev. Genet. 40:363–83 [Google Scholar]
  159. Xie Z, Johansen LK, Gustafson AM, Kasschau KD, Lellis AD. 160.  et al. 2004. Genetic and functional diversification of small RNA pathways in plants. PLOS Biol. 2:E104 [Google Scholar]
  160. Yang H, Lu P, Wang Y, Ma H. 161.  2011. The transcriptome landscape of Arabidopsis male meiocytes from high-throughput sequencing: the complexity and evolution of the meiotic process. Plant J. Cell Mol. Biol. 65:503–16 [Google Scholar]
  161. Yelagandula R, Stroud H, Holec S, Zhou K, Feng S. 162.  et al. 2014. The histone variant H2A. W defines heterochromatin and promotes chromatin condensation in Arabidopsis. Cell 158:98–109 [Google Scholar]
  162. You ZS, Chahwan C, Bailis J, Hunter T, Russell P. 163.  2005. ATM activation and its recruitment to damaged DNA require binding to the C terminus of Nbs1. Mol. Cell. Biol. 25:5363–79 [Google Scholar]
  163. Zemach A, Kim MY, Hsieh PH, Coleman-Derr D, Eshed-Williams L. 164.  et al. 2013. The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell 153:193–205 [Google Scholar]
  164. Zhang H, Ma ZY, Zeng L, Tanaka K, Zhang CJ. 165.  et al. 2013. DTF1 is a core component of RNA-directed DNA methylation and may assist in the recruitment of Pol IV. PNAS 110:8290–95 [Google Scholar]
  165. Zhang H, Zhu JK. 166.  2012. Active DNA demethylation in plants and animals. Cold Spring Harb. Symp. Quant. Biol. 77:161–73 [Google Scholar]
  166. Zhang XY, Clarenz O, Cokus S, Bernatavichute YV, Pellegrini M. 167.  et al. 2007. Whole-genome analysis of histone H3 lysine 27 trimethylation in Arabidopsis. PLOS Biol. 5:1026–35 [Google Scholar]
  167. Zhao Y, Chen X. 168.  2014. Noncoding RNAs and DNA methylation in plants. Natl. Sci. Rev. 1:219–29 [Google Scholar]
  168. Zhong X, Hale CJ, Law JA, Johnson LM, Feng S. 169.  et al. 2012. DDR complex facilitates global association of RNA polymerase V to promoters and evolutionarily young transposons. Nat. Struct. Mol. Biol. 19:870–75 [Google Scholar]
  169. Zhou BBS, Elledge SJ. 170.  2000. The DNA damage response: putting checkpoints in perspective. Nature 408:433–39 [Google Scholar]
  170. Zhu W, Dutta A. 171.  2006. An ATR- and BRCA1-mediated Fanconi anemia pathway is required for activating the G2/M checkpoint and DNA damage repair upon rereplication. Mol. Cell Biol. 26:4601–11 [Google Scholar]
  171. Zilberman D, Coleman-Derr D, Ballinger T, Henikoff S. 172.  2008. Histone H2A.Z and DNA methylation are mutually antagonistic chromatin marks. Nature 456:125–29 [Google Scholar]
  172. Ziv Y, Bielopolski D, Galanty Y, Lukas C, Taya Y. 173.  et al. 2006. Chromatin relaxation in response to DNA double-strand breaks is modulated by a novel ATM and KAP-1 dependent pathway. Nat. Cell Biol. 8:870–76 [Google Scholar]
  173. Zou L, Elledge SJ. 174.  2003. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300:1542–48 [Google Scholar]
/content/journals/10.1146/annurev-genet-112414-055048
Loading
/content/journals/10.1146/annurev-genet-112414-055048
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error