Chromatin is a macromolecular complex where DNA associates with histone proteins and a variety of non-histone proteins. Among the 4 histone types present in nucleosomes, histone H3 is encoded by a large number of genes in most eukaryotic species and is the histone that contains the largest variety of potential post-translational modifications in the N-terminal amino acid residues. In addition to centromeric histone H3, 2 major types of histone H3 exist, namely the canonical H3.1 and the variant H3.3. In this article, we review the most recent observations on the distinctive features of plant H3 proteins in terms of their expression and dynamics during the cell cycle and at various developmental stages. We also include a discussion on the histone H3 chaperones that actively participate in H3 deposition, in particular CAF-1, HIRA and ASF1, and on the putative plant homologs of human ATRX and DEK chaperones. Accumulating evidence confirms that the balanced deposition of H3.1 and H3.3 is of primary relevance for cell differentiation during plant organogenesis.

Keywords:
Arabidopsis, Cell cycle, Chromatin, DNA replication, Epigenetics, Gene expression, Histone H3, Plant
1.
Ach RA, Taranto P, Gruissem W: A conserved family of WD-40 proteins binds to the retinoblastoma protein in both plants and animals. Plant Cell 9:1595-1606 (1997).
2.
Ahmad K, Henikoff S: The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol Cell 9:1191-1200 (2002).
3.
Ausin I, Alonso-Blanco C, Jarillo JA, Ruiz-Garcia L, Martinez-Zapater JM: Regulation of flowering time by FVE, a retinoblastoma-associated protein. Nat Genet 36:162-166 (2004).
4.
Banaszynski LA, Wen D, Dewell S, Whitcomb SJ, Lin M, et al: Hira-dependent histone H3.3 deposition facilitates PRC2 recruitment at developmental loci in ES cells. Cell 155:107-120 (2013).
5.
Bonnefoy E, Orsi GA, Couble P, Loppin B: The essential role of Drosophila HIRA for de novo assembly of paternal chromatin at fertilization. PLoS Genet 3:1991-2006 (2007).
6.
Bouveret R, Schönrock N, Gruissem W, Hennig L: Regulation of flowering time by ArabidopsisMSI1. Development 133:1693-1702 (2006).
7.
Breuer C, Morohashi K, Kawamura A, Takahashi N, Ishida T, et al: Transcriptional repression of the APC/C activator CCS52A1 contributes to the active termination of cell growth. EMBO J 31:4488-4501 (2012).
8.
Carrera P, Moshkin YM, Gronke S, Sillje HH, Nigg EA, et al: Tousled-like kinase functions with the chromatin assembly pathway regulating nuclear divisions. Genes Dev 17:2578-2590 (2003).
9.
Cayrou C, Coulombe P, Vigneron A, Stanojcic S, Ganier O, et al: Genome-scale analysis of metazoan replication origins reveals their organization in specific but flexible sites defined by conserved features. Genome Res 21:1438-1449 (2011).
10.
Cooper JL, Henikoff S: Adaptive evolution of the histone fold domain in centromeric histones. Mol Biol Evol 21:1712-1718 (2004).
11.
Costas C, Sanchez MP, Stroud H, Yu Y, Oliveros JC, et al: Genome-wide mapping of Arabidopsis thaliana origins of DNA replication and their associated epigenetic marks. Nat Struct Mol Biol 18:395-400 (2011).
12.
De Rop V, Padeganeh A, Maddox PS: CENP-A: the key player behind centromere identity, propagation, and kinetochore assembly. Chromosoma 121:527-538 (2012).
13.
De Veylder L, Larkin JC, Schnittger A: Molecular control and function of endoreplication in development and physiology. Trends Plant Sci 16:624-634 (2011).
14.
Dubin M, Fuchs J, Graf R, Schubert I, Nellen W: Dynamics of a novel centromeric histone variant CenH3 reveals the evolutionary ancestral timing of centromere biogenesis. Nucleic Acids Res 38:7526-7537 (2010).
15.
Edgar BA, Zielke N, Gutierrez C: Endocycles: a recurrent evolutionary innovation for post-mitotic cell growth. Nat Rev Mol Cell Biol 15:197-210 (2014).
16.
Ehsan H, Reichheld JP, Durfee T, Roe JL: TOUSLED kinase activity oscillates during the cell cycle and interacts with chromatin regulators. Plant Physiol 2004;134:1488-1499.
17.
Exner V, Taranto P, Schönrock N, Gruissem W, Hennig L: Chromatin assembly factor CAF-1 is required for cellular differentiation during plant development. Development 133:4163-4172 (2006).
18.
Exner V, Gruissem W, Hennig L: Control of trichome branching by chromatin assembly factor-1. BMC Plant Biol 8:54 (2008).
19.
Fransz P, ten Hoopen R, Tessadori F: Composition and formation of heterochromatin in Arabidopsis thaliana. Chromosome Res 14:71-82 (2006).
20.
Fuchs J, Demidov D, Houben A, Schubert I: Chromosomal histone modification patterns - from conservation to diversity. Trends Plant Sci 11:199-208 (2006).
21.
Gao J, Zhu Y, Zhou W, Molinier J, Dong A, Shen WH: NAP1 family histone chaperones are required for somatic homologous recombination in Arabidopsis. Plant Cell 24:1437-1447 (2012).
22.
Goldberg AD, Banaszynski LA, Noh KM, Lewis PW, Elsaesser SJ, et al: Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell 140:678-691 (2010).
23.
Heckmann S, Lermontova I, Berckmans B, De Veylder L, Baumlein H, Schubert I: The E2F transcription factor family regulates CENH3 expression in Arabidopsis thaliana. Plant J 68:646-656 (2011).
24.
Hennig L, Derkacheva M: Diversity of Polycomb group complexes in plants: same rules, different players? Trends Genet 25:414-423 (2009).
25.
Hennig L, Taranto P, Walser M, Schönrock N, Gruissem W: Arabidopsis MSI1 is required for epigenetic maintenance of reproductive development. Development 130:2555-2565 (2003).
26.
Heun P, Erhardt S, Blower MD, Weiss S, Skora AD, Karpen GH: Mislocalization of the Drosophila centromere-specific histone CID promotes formation of functional ectopic kinetochores. Dev Cell 10:303-315 (2006).
27.
Hödl M, Basler K: Transcription in the absence of histone H3.3. Curr Biol 19:1221-1226 (2009).
28.
Hoek M, Stillman B: Chromatin assembly factor 1 is essential and couples chromatin assembly to DNA replication in vivo. Proc Natl Acad Sci USA 100:12183-12188 (2003).
29.
Hülskamp M, Schnittger A, Folkers U: Pattern formation and cell differentiation: trichomes in Arabidopsis as a genetic model system. Int Rev Cytol 186:147-178 (1999).
30.
Ingouff M, Berger F: Histone3 variants in plants. Chromosoma 119:27-33 (2010).
31.
Ingouff M, Hamamura Y, Gourgues M, Higashiyama T, Berger F: Distinct dynamics of HISTONE3 variants between the two fertilization products in plants. Curr Biol 17:1032-1037 (2007).
32.
Ingouff M, Rademacher S, Holec S, Soljic L, Xin N, et al: Zygotic resetting of the HISTONE 3 variant repertoire participates in epigenetic reprogramming in Arabidopsis. Curr Biol 20:2137-2143 (2010).
33.
Jansen LE, Black BE, Foltz DR, Cleveland DW: Propagation of centromeric chromatin requires exit from mitosis. J Cell Biol 176:795-805 (2007).
34.
Jaske K, Mokros P, Mozgova I, Fojtova M, Fajkus J: A telomerase-independent component of telomere loss in chromatin assembly factor 1 mutants of Arabidopsis thaliana. Chromosoma 122:285-293 (2013).
35.
Jin C, Zang C, Wei G, Cui K, Peng W, et al: H3.3/H2A.Z double variant-containing nucleosomes mark ‘nucleosome-free regions' of active promoters and other regulatory regions. Nat Genet 41:941-945 (2009).
36.
Kaya H, Shibahara KI, Taoka KI, Iwabuchi M, Stillman B, Araki T: FASCIATA genes for chromatin assembly factor-1 in Arabidopsis maintain the cellular organization of apical meristems. Cell 104:131-142 (2001).
37.
Kirik A, Pecinka A, Wendeler E, Reiss B: The chromatin assembly factor subunit FASCIATA1 is involved in homologous recombination in plants. Plant Cell 18:2431-2442 (2006).
38.
Köhler C, Hennig L, Spillane C, Pien S, Gruissem W, Grossniklaus U: The Polycomb-group protein MEDEA regulates seed development by controlling expression of the MADS-box gene PHERES1. Genes Dev 17:1540-1553 (2003).
39.
Kossel A: Ueber einen peptonartigen Bestandtheil des Zellkerns. Zschr Physiol Chem 8:511 (1884).
40.
Kosugi S, Ohashi Y: E2F sites that can interact with E2F proteins cloned from rice are required for meristematic tissue-specific expression of rice and tobacco proliferating cell nuclear antigen promoters. Plant J 29:45-59 (2002).
41.
Kouzarides T: Chromatin modifications and their function. Cell 128:693-705 (2007).
42.
Kuzmichev A, Nishioka K, Erdjument-Bromage H, Tempst P, Reinberg D: Histone methyltransferase activity associated with a human multiprotein complex containing the Enhancer of Zeste protein. Genes Dev 16:2893-2905 (2002).
43.
Lario LD, Ramirez-Parra E, Gutierrez C, Spampinato CP, Casati P: 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 162:1164-1177 (2013).
44.
Le S, Davis C, Konopka JB, Sternglanz R: Two new S-phase-specific genes from Saccharomyces cerevisiae. Yeast 13:1029-1042 (1997).
45.
Lermontova I, Schubert V, Fuchs J, Klatte S, Macas J, Schubert I: Loading of Arabidopsis centromeric histone CENH3 occurs mainly during G2 and requires the presence of the histone fold domain. Plant Cell 18:2443-2451 (2006).
46.
Lermontova I, Fuchs J, Schubert V, Schubert I: Loading time of the centromeric histone H3 variant differs between plants and animals. Chromosoma 116:507-510 (2007).
47.
Lermontova I, Koroleva O, Rutten T, Fuchs J, Schubert V, et al: Knockdown of CENH3 in Arabidopsis reduces mitotic divisions and causes sterility by disturbed meiotic chromosome segregation. Plant J 68:40-50 (2011a).
48.
Lermontova I, Rutten T, Schubert I: Deposition, turnover, and release of CENH3 at Arabidopsis centromeres. Chromosoma 120:633-640 (2011b).
49.
Lermontova I, Kuhlmann M, Friedel S, Rutten T, Heckmann S, et al: Arabidopsis KINETOCHORE NULL2 is an upstream component for centromeric histone H3 variant cenH3 deposition at centromeres. Plant Cell 25:3389-3404 (2013).
50.
Lewis PW, Elsaesser SJ, Noh KM, Stadler SC, Allis CD: Daxx is an H3.3-specific histone chaperone and cooperates with ATRX in replication-independent chromatin assembly at telomeres. Proc Natl Acad Sci USA 107:14075-14080 (2010).
51.
Liu Q, Gong Z: The coupling of epigenome replication with DNA replication. Curr Opin Plant Biol 14:187-194 (2011).
52.
Lombraña R, Almeida R, Revuelta I, Madeira S, Herranz G, et al: High-resolution analysis of DNA synthesis start sites and nucleosome architecture at efficient mammalian replication origins. EMBO J 32:2631-2644 (2013).
53.
Malik HS, Henikoff S: Phylogenomics of the nucleosome. Nat Struct Biol 10:882-891 (2003).
54.
Manzano C, Ramirez-Parra E, Casimiro I, Otero S, Desvoyes B, et al: Auxin and epigenetic regulation of SKP2B, an F-box that represses lateral root formation. Plant Physiol 160:749-762 (2012).
55.
March-Diaz R, Reyes JC: The beauty of being a variant: H2A.Z and the SWR1 complex in plants. Mol Plant 2:565-577 (2009).
56.
Margueron R, Reinberg D: Chromatin structure and the inheritance of epigenetic information. Nat Rev Genet 11:285-296 (2010).
57.
Mechali M, Yoshida K, Coulombe P, Pasero P: Genetic and epigenetic determinants of DNA replication origins, position and activation. Curr Opin Genet Dev 23:124-131 (2013).
58.
Mendiburo MJ, Padeken J, Fulop S, Schepers A, Heun P: Drosophila CENH3 is sufficient for centromere formation. Science 334:686-690 (2011).
59.
Mito Y, Henikoff JG, Henikoff S: Genome-scale profiling of histone H3.3 replacement patterns. Nat Genet 37:1090-1097 (2005).
60.
Moraes IC, Lermontova I, Schubert I: Recognition of A. thaliana centromeres by heterologous CENH3 requires high similarity to the endogenous protein. Plant Mol Biol 75:253-261 (2011).
61.
Mozgova I, Mokros P, Fajkus J: Dysfunction of chromatin assembly factor 1 induces shortening of telomeres and loss of 45S rDNA in Arabidopsis thaliana. Plant Cell 22:2768-2780 (2010).
62.
Nabatiyan A, Krude T: Silencing of chromatin assembly factor 1 in human cells leads to cell death and loss of chromatin assembly during DNA synthesis. Mol Cell Biol 24:2853-2862 (2004).
63.
Nagaki K, Murata M: Characterization of CENH3 and centromere-associated DNA sequences in sugarcane. Chromosome Res 13:195-203 (2005).
64.
Nagaki K, Yamamoto M, Yamaji N, Mukai Y, Murata M: Chromosome dynamics visualized with an anti-centromeric histone H3 antibody in Allium. PLoS One 7:e51315 (2012).
65.
Nakayama T, Nishioka K, Dong YX, Shimojima T, Hirose S: Drosophila GAGA factor directs histone H3.3 replacement that prevents the heterochromatin spreading. Genes Dev 21:552-561 (2007).
66.
Okada T, Endo M, Singh MB, Bhalla PL: Analysis of the histone H3 gene family in Arabidopsis and identification of the male-gamete-specific variant AtMGH3. Plant J 44:557-568 (2005).
67.
Ono T, Kaya H, Takeda S, Abe M, Ogawa Y, et al: Chromatin assembly factor 1 ensures the stable maintenance of silent chromatin states in Arabidopsis. Genes Cells 11:153-162 (2006).
68.
Phelps-Durr TL, Thomas J, Vahab P, Timmermans MC: Maize rough sheath2 and its Arabidopsis orthologue ASYMMETRIC LEAVES1 interact with HIRA, a predicted histone chaperone, to maintain knox gene silencing and determinacy during organogenesis. Plant Cell 17:2886-2898 (2005).
69.
Polo SE, Almouzni G: Chromatin assembly: a basic recipe with various flavours. Curr Opin Genet Dev 16:104-111 (2006).
70.
Ramirez-Parra E, Gutierrez C: E2F regulates FASCIATA1, a chromatin assembly gene whose loss switches on the endocycle and activates gene expression by changing the epigenetic status. Plant Physiol 144:105-120 (2007a).
71.
Ramirez-Parra E, Gutierrez C: The many faces of chromatin assembly factor 1. Trends Plant Sci 12:570-576 (2007b).
72.
Ravi M, Kwong PN, Menorca RM, Valencia JT, Ramahi JS, et al: The rapidly evolving centromere-specific histone has stringent functional requirements in Arabidopsis thaliana. Genetics 186:461-471 (2010).
73.
Ray-Gallet D, Quivy JP, Scamps C, Martini EM, Lipinski M, Almouzni G: HIRA is critical for a nucleosome assembly pathway independent of DNA synthesis. Mol Cell 9:1091-1100 (2002).
74.
Reyes JC: Chromatin modifiers that control plant development. Curr Opin Plant Biol 9:21-27 (2006).
75.
Ridgway P, Almouzni G: CAF-1 and the inheritance of chromatin states: at the crossroads of DNA replication and repair. J Cell Sci 113:2647-2658 (2000).
76.
Roberts C, Sutherland HF, Farmer H, Kimber W, Halford S, et al: Targeted mutagenesis of the Hira gene results in gastrulation defects and patterning abnormalities of mesoendodermal derivatives prior to early embryonic lethality. Mol Cell Biol 22:2318-2328 (2002).
77.
Sakai A, Schwartz BE, Goldstein S, Ahmad K: Transcriptional and developmental functions of the H3.3 histone variant in Drosophila. Curr Biol 19:1816-1820 (2009).
78.
Sanchez Mde L, Gutierrez C: Novel insights into the plant histone code: lessons from ORC1. Epigenetics 4:205-208 (2009).
79.
Sanchez Mde L, Costas C, Sequeira-Mendes J, Gutierrez C: Regulating DNA replication in plants. Cold Spring Harb Perspect Biol 4:a010140 (2012).
80.
Sanei M, Pickering R, Kumke K, Nasuda S, Houben A: Loss of centromeric histone H3 (CENH3) from centromeres precedes uniparental chromosome elimination in interspecific barley hybrids. Proc Natl Acad Sci USA 108:E498-505 (2011).
81.
Schönrock N, Exner V, Probst A, Gruissem W, Hennig L: Functional genomic analysis of CAF-1 mutants in Arabidopsis thaliana. J Biol Chem 281:9560-9568 (2006).
82.
Schuh M, Lehner CF, Heidmann S: Incorporation of Drosophila CID/CENP-A and CENP-C into centromeres during early embryonic anaphase. Curr Biol 17:237-243 (2007).
83.
Sherwood PW, Tsang SV, Osley MA: Characterization of HIR1 and HIR2, two genes required for regulation of histone gene transcription in Saccharomyces cerevisiae. Mol Cell Biol 13:28-38 (1993).
84.
Shi L, Wang J, Hong F, Spector DL, Fang Y: Four amino acids guide the assembly or disassembly of Arabidopsis histone H3.3-containing nucleosomes. Proc Natl Acad Sci USA 108:10574-10578 (2011).
85.
Sillje HH, Nigg EA: Identification of human Asf1 chromatin assembly factors as substrates of tousled-like kinases. Curr Biol 11:1068-1073 (2001).
86.
Slotkin RK, Vaughn M, Borges F, Tanurdzic M, Becker JD, et al: Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136:461-472 (2009).
87.
Smith S, Stillman B: Purification and characterization of CAF-I, a human cell factor required for chromatin assembly during DNA replication in vitro. Cell 58:15-25 (1989).
88.
Song Y, Seol JH, Yang JH, Kim HJ, Han JW, et al: Dissecting the roles of the histone chaperones reveals the evolutionary conserved mechanism of transcription-coupled deposition of H3.3. Nucleic Acids Res 41:5199-5209 (2013).
89.
Stedman E, Stedman E: The chemical nature and functions of the components of the cell nuclei. Cold Spring Harb Symp Quant Biol 12:224-236 (1947).
90.
Stevens R, Mariconti L, Rossignol P, Perennes C, Cella R, Bergounioux C: Two E2F sites in the Arabidopsis MCM3 promoter have different roles in cell cycle activation and meristematic expression. J Biol Chem 277:32978-32984 (2002).
91.
Stroud H, Otero S, Desvoyes B, Ramirez-Parra E, Jacobsen SE, Gutierrez C: Genome-wide analysis of histone H3.1 and H3.3 variants in Arabidopsis thaliana. Proc Natl Acad Sci USA 109:5370-5375 (2012).
92.
Stroud H, Greenberg MV, Feng S, Bernatavichute YV, Jacobsen SE: Comprehensive analysis of silencing mutants reveals complex regulation of the Arabidopsis methylome. Cell 152:352-364 (2013).
93.
Szenker E, Lacoste N, Almouzni G: A developmental requirement for HIRA-dependent H3.3 deposition revealed at gastrulation in Xenopus. Cell Rep 1:730-740 (2012).
94.
Tagami H, Ray-Gallet D, Almouzni G, Nakatani Y: Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell 116:51-61 (2004).
95.
Takeda S, Tadele Z, Hofmann I, Probst AV, Angelis KJ, et al: BRU1, a novel link between responses to DNA damage and epigenetic gene silencing in Arabidopsis. Genes Dev 18:782-793 (2004).
96.
Talbert PB, Henikoff S: Histone variants - ancient wrap artists of the epigenome. Nat Rev Mol Cell Biol 11:264-275 (2010).
97.
Talbert PB, Masuelli R, Tyagi AP, Comai L, Henikoff S: Centromeric localization and adaptive evolution of an Arabidopsis histone H3 variant. Plant Cell 14:1053-1066 (2002).
98.
Teo CH, Lermontova I, Houben A, Mette MF, Schubert I: De novo generation of plant centromeres at tandem repeats. Chromosoma 122:233-241 (2013).
99.
Vaquero-Sedas MI, Vega-Palas MA: Differential association of Arabidopsis telomeres and centromeres with histone H3 variants. Sci Rep 3:1202 (2013).
100.
Waterborg JH, Robertson AJ: Common features of analogous replacement histone H3 genes in animals and plants. J Mol Evol 43:194-206 (1996).
101.
Weber M, Schubeler D: Genomic patterns of DNA methylation: targets and function of an epigenetic mark. Curr Opin Cell Biol 19:273-280 (2007).
102.
Wollmann H, Holec S, Alden K, Clarke ND, Jacques PE, Berger F: Dynamic deposition of histone variant H3.3 accompanies developmental remodeling of the Arabidopsis transcriptome. PLoS Genet 8:e1002658 (2012).
103.
Wong LH, Ren H, Williams E, McGhie J, Ahn S, et al: Histone H3.3 incorporation provides a unique and functionally essential telomeric chromatin in embryonic stem cells. Genome Res 19:404-414 (2009).
104.
Wu SC, Gyorgyey J, Dudits D: Polyadenylated H3 histone transcripts and H3 histone variants in alfalfa. Nucleic Acids Res 17:3057-3063 (1989).
105.
Xu J, Yanagisawa Y, Tsankov AM, Hart C, Aoki K, et al: Genome-wide identification and characterization of replication origins by deep sequencing. Genome Biol 13:R27 (2012).
106.
Ye X, Franco AA, Santos H, Nelson DM, Kaufman PD, Adams PD: Defective S phase chromatin assembly causes DNA damage, activation of the S phase checkpoint, and S phase arrest. Mol Cell 11:341-351 (2003).
107.
Zhu Y, Weng M, Yang Y, Zhang C, Li Z, et al: Arabidopsis homologues of the histone chaperone ASF1 are crucial for chromatin replication and cell proliferation in plant development. Plant J 66:443-455 (2011).
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