Regulatory Function of Histone Modifications in Controlling Rice Gene Expression and Plant Growth
© Springer Science + Business Media, LLC 2010
Received: 6 April 2010
Accepted: 6 July 2010
Published: 29 July 2010
Histone modifications play pivotal roles in chromatin remodeling and gene regulation. Rice genome possesses multiple genes encoding different classes of histone modification enzymes. Specific histone modification patterns in rice are associated with either heterochromatic or euchromatic regions or related to gene expression. Functional studies of several rice genes encoding histone deacetylases and histone methyltransferases and demethylases reveal specific regulators involved in transposon repression, development regulation, and responses to environmental conditions. Functional interplay between rice histone modification regulators in gene regulation and transposon silencing and their implication in rice epigenetic variation are discussed.
KeywordsChromatin Histone acetylation Methylation Histone deacetylase Histone methyltransferase Histone demethylase jmjC SUVH SIR2 Epigenetic regulation Stress inducible
In eukaryotes, the genomic DNA is tightly compacted into a complex structure known as chromatin. To control genome activities, the accessibility of chromatin is dynamically regulated during growth and development. The massive changes in gene expression that occur during developmental transitions rely at least in part on epigenetic processes such as chromatin remodeling to establish specific states for gene expression. In addition, plants are sessile organisms that have to adapt to their living environments. It is therefore essential for plants to develop rapid responses to changes in environmental conditions for their adaptation and survival. Rapid changes of chromatin structure play a central role in regulating gene expression in response to environmental cues. During the last decade, many plant DNA-binding transcription factors involved in developmental and inducible gene regulations have been identified. However, how these factors activate or repress transcription in a specific chromatin context is not clearly known. Chromatin structure and remodeling are basic components of genetic and epigenetic regulations of genome expression (Horn and Peterson 2002). Nucleosome is the basic structure of chromatin and is composed of 4 types of core histones. Covalent modifications of the N-terminal tails of the core histones play pivotal roles in chromatin remodeling and in gene regulation (Millar and Grunstein 2006). Histone modifications include acetylation, methylation, phosphorylation, ubiquitinylation, and others. Most of the modifications are on the lysine, arginine, or serine residues of H3 or H4. Specific patterns of histone modifications determine active or repressed states of the cognate chromatin (Berger 2007). Different chromatin structures define distinct epigenomes which is reflected by specific gene expression pattern of different cell types and responses to different environmental conditions. Histone modification and recognition genes are found to play important roles in many different aspects of developmental, cellular and genetic processes in Arabidopsis. Functional study of rice histone modification and recognition is emerging. Here, we review recent data of rice histone modification regulation and its function in rice gene expression and plant growth and development. Since there is no much information on histone phosphorylation and ubiquitination in rice, the review will focus on the regulatory mechanism of histone acetylation and methylation.
Histone acetylation in the regulation of rice gene expression
Among histone modifications, histone lysine acetylation appears to be a dynamic reversible switch for inter-conversion between permissive and repressive transcriptional states of chromatin domains. Strong acetylation of histones induces relaxation of chromatin structure and is associated with transcriptional activation, whereas weak acetylation leads to chromatin compaction and gene repression (Berger 2007). N-terminal lysine residues of histone H3 (K9, K14, K18 and K23) and H4 (K5, K8, K12, K16 and K20) are found to be acetylation/deacetylation targets in Arabidopsis (Earley et al. 2007; Zhang et al. 2007a). The dynamic modulation of histone acetylation in plants is shown to be important for plants to adapt their growth and development to environment changes such as light, temperature, biotic, and abiotic stresses (Chen and Tian 2007; Servet et al. 2010). In rice, acetylation of H3K9 and H4K12 is elevated in genes located in euchromatic regions (Yin et al. 2008), suggesting that these markers may be associated with active genes. Dynamic and reversible changes in histone H3 acetylation and H3K4 methylation occur at submergence-inducible genes in rice (Tsuji et al. 2006). When submerged, the rice ADH1 (alcohol dehydrogenase 1) and PDC1 (pyruvate decarboxylase 1) genes are activated in two phases: the first activation occurs after 2 h of submergence, the second after 12 h. The first induction seems to be associated with tri-methylation of histone H3K4 on the 5′- and 3′-coding regions, while the second induction is correlated with increased histone H3 acetylation throughout ADH1 and PDC1 genes. The methylation and acetylation levels return to the initial levels after re-aeration. These data nicely demonstrate the dynamic and reversible changes of histone H3K4 methylation and H3 acetylation in responses to environmental changes in rice. In addition, histone H3K9 acetylation is required for the expression of RICE FLOWERING LOCUS T 1 (RFT1/FT-L3) that is the closest homologue of Heading date 3a (Hd3a) encoding a mobile flowering signal and promote floral transition under short-day conditions (Komiya et al. 2008), showing a role of histone acetylation in the regulation of rice developmental transitions.
Function of histone deacetylases genes in rice
It has been shown that over-expression of OsHDAC1 (HDA702) leads to increased growth rate and altered architecture in transgenic rice (Jang et al. 2003). It is recently shown that OsHDAC1 epigenetically represses the OsNAC6 gene that controls rice seedling root growth (Chung et al. 2009a). OsHDAC1 interacts with the OsNAC6 gene promoter and deacetylates histone H3K9, K14 and K18 and H4K5, K12 and K16. However, over-expression of several other rice HDAC genes does not produce any visible phenotype. In contrast, down-regulation of a few HDAC genes affects different developmental aspects (Hu et al. 2009). Although the mechanism by which HDAC are involved in rice development regulation is unclear, those rice genes seem to have divergent developmental functions compared to closely related homologues in Arabidopsis.
Histone methylation and histone lysine methyltransferases in rice
Histone lysine methylation is an important epigenetic modification with both activating and repressive roles in gene expression. Histone lysine residues can be mono-, di-, or trimethylated, where each distinct methyl state may have different biological functions (Bannister and Kouzarides 2004). For instance, di- and trimethylation of H3K9 (H3K9me2, H3K9me3) and trimethylation of H3K27 (H3K27me3) negatively correlate with gene expression, whereas trimethylation of H3K4 (H3K4me3), as mentioned above, positively correlate with the expression of target genes (Pfluger and Wagner 2007; Fig. 1). These differently methylated histone lysine residues are recognized by different chromatin protein modules that induce distinct chromatin structures. For instance, H3K9me2 is shown to be associated with Heterchromatin Protein1 in animal cells (reviewed in Vermaak and Malik 2009), while H3K27me3 is associated with Polycomb group (PcG) repressive complexes in both plant and animal cells (reviewed in Hennig and Derkacheva 2009).
Results from immunostaining and chromatin immunoprecipitation (ChIP) coupled with DNA microarray (chip) (ChIP-chip) analysis in Arabidopsis suggest that methylation of H3K9 and H3K27 is important for chromatin structure and gene regulation. H3K9me2 is found to be enriched in heterochromatic repetitive sequence regions, while H3K9me3 and H3K27me3 are distributed in the 5′ ends of genes in euchromatic regions (Lippman et al. 2004; Turck et al. 2007; Zhang et al. 2007b). The distribution of H3K9me3 and H3K27me3 does not overlap, suggesting that they may respond to different cellular signals or be involved in distinct regulatory pathways. Analysis of H3K4 methylation of two entire chromosomes in rice revealed that half of protein-coding genes have di- and/or trimethylated H3K4 (Li et al. 2008). Rice genes with predominantly H3K4me3 are actively transcribed, whereas genes with predominantly H3K4me2 were transcribed at moderate levels (Li et al. 2008).
Drosophila Su(var)3-9 protein was the first identified histone lysine methyltransferase specific for H3K9 (Rea et al. 2000). Multiple Su(var)3-9 methyltransferases have been identified in mammals and are shown to play an important role in chromatin function and development (Sims et al. 2003). In line with the genomic characteristics, plant genome encodes many SUVH genes (Baumbusch et al. 2001; Fig. 3). This may be because a large fraction of the genome is repetitive sequences and extensive heterochromatic silencing processes require different SUVH functions. For instance, Arabidopsis genome contains ten SUVH genes, of which KYP (also known as SUVH4), SUVH5 and SUVH6 are shown to undergo H3K9 methylation in a locus-specific manner (Ebbs et al. 2005; Ebbs and Bender 2006; Jackson et al. 2004). The three Arabidopsis SUVH proteins display mono- or dimethyltransferase activity of histone H3K9 (Ebbs and Bender 2006; Jackson et al. 2004). Rice genome encodes 12 SUVH genes (Fig. 3). One of rice SUVH genes, namely SDG714, is found to be involved in H3K9me2 and DNA methylation of Tos17, a copia-like retrotransposon (Ding et al. 2007). A systematic study of rice SUVH genes revealed that different members display distinct function in histone H3K9 methylation, DNA methylation, and transposon silencing (Qin et al. 2010). For instance, down-regulation of most of the rice SUVH members does not induce obvious morphological phenotype, while SDG728 RNAi plants produce deformed seed shape. In addition, both H3K9me2 and H3K9me3 are decreased in the SDG728 RNAi plants, while down-regulation of other rice SUVH genes (e.g., SDG713) only affects H3K9me2. The expression of Tos17 and a Ty1-copia element is activated in RNAi plants of a few SUVH genes (e.g., SDG703, SDG713 and SDG728), but not affected by down-regulation of other SUVH. The activation of Tos17 is correlated with a clear decrease of H3K9me3 on Tos17 in SDG728 RNAi plants, suggesting that H3K9me3 may be an important component of retrotransposon silencing.
As described above, down-regulation of the rice HDAC gene SRT701 leads to transcriptional activation of many transposons (Huang et al. 2007). Down-regulation of SRT701 not only augments H3K9ac but also decreases H3K9me2. As acetylated H3K9 needs to be deacetylated by HDAC before methylation, these data suggest that SRT701 and SUVH genes function within a similar pathway to regulate transposon silencing in rice. Therefore, in addition to DNA methylation that is known to be an important component of transposon and retrotransposnon silencing in plants, histone modification seems to also play a primary role in retrotransposon repression in rice (Fig. 2). Furthermore, SUVH genes (i.e., SDG714, SDG727, and SDG710) are found to have an antagonistic function to the histone H3K9 demethylase gene JMJ706 in regulating H3K9 methylation and panicle development (Qin et al. 2010).
In addition to the SET domain, plant SUVH proteins contain a plant-specific YDG (named after the three conserved amino acids)/SRA (SET- and Ring Finger-associated) domain. The YDG/SRA domain of KYP/SUVH4 is shown to bind directly to methylated DNA (Johnson et al. 2007), suggesting that DNA methylation and H3K9me2 are correlated in Arabidopsis (Soppe et al. 2002; Tariq et al. 2003). Inactivation of rice SDG714 affected DNA methylation on the Tos17 locus, suggesting that rice SUVH function may be also linked to DNA methylation involved in retrotransposon silencing.
Arabidopsis INCREASED EXPRESSION OF BONSAI METHYLATION1 (IBM1; also known as AtJmj15 or JMJ25, At3g07610), represses genic cytosine methylation, possibly through demethylation of H3K9 (Saze et al. 2008). JMJ706, a rice member of the JMJD2 group of jmjC genes, is shown to encode a heterochromatin-associated protein (Sun and Zhou, 2008). In vitro histone demthylation assays and analysis of T-DNA insertion mutants revealed that JMJ706 is involved in H3K9 demethylation required for the expression of a subset of regulatory genes for rice panicle development. However, the mutation of JMJ706 seems not to affect DNA methylation in tandem repeats (Sun 2009). Minor changes in DNA methylation on the retrotransposon Tos17 is observed. Therefore, different plant jmjC proteins involved in H3K9 demethylation may have distinct function in chromatin regulation.
As mentioned above, inactivation of three SUVH genes by amiRNA in the jmj706 mutant background restore partially the panicle phenotype of jmj706 and histone H3K9 methylation. This group of SUVH methyltransferase genes and JMJ706 appear to be involved in different regulatory pathways, but simultaneous inactivation could compensate for each other. This indicates that interaction between the two antagonistic families of enzymes is collectively involved to maintain histone H3K9 methylation homeostasis that is important for rice development.
H3K27me3 are found to be distributed in the 5′ ends of genes in euchromatic regions in Arabidopsis (Turck et al. 2007; Zhang et al. 2007b). Whether H3K27me3 has a similar distribution on rice genome remains to be determined. The repression of many important plant developmental key genes is mediated by H3K27 methylation involving PcG protein complexes. For instance, SET domain-containing PcG proteins CLF and SWN are required for H3K27me3-mediated silencing of important developmental regulatory genes such as the floral organ homeotic gene AGAMOUS during vegetative growth, the meristem regulator SHOOTMERISTEMLESS (STM) in seedlings and the seed development gene PHERES in vegetative tissues (reviewed in Pien and Grossniklaus 2007). The establishment and the maintenance of the repression of the flowering repressor FLC is also mediated by H3K27 methylation. This suggests that H3K27me-mediated gene silencing may be mainly involved in developmental decision in plants. However, activities involved in the demethylation of H3K27me3 remain to be identified in plants.
Conclusions and perspectives
Current knowledge on the function of histone modification regulation and recognition suggests that there are both conservation and difference between plants and other eukaryotic systems in chromatin mechanism of gene regulation. The sessile lifestyle of plants requires increased developmental plasticity. Histone modification and recognition are essential for programming and reprogramming of plant developmental processes and for rapid responses to environmental cues. Plant genomes contain a large portion of repetitive sequences, the repression of which involves both DNA methylation and histone modifications. In addition, plants have large families of genes involved in histone modifications. Studying specific functions of the individual family members will be needed to understand the complexity of regulation of histone modification and epigenomic dynamics during plant developmental transitions and in responses to environmental conditions. Identifying functional interaction between histone modification regulators and other chromatin or signaling factors (such as chromatin remodeling factors, DNA-binding transcription factors) will be required to provide a mechanistic view on how histone modification integrates cell signals to regulate chromatin structures. Identifying the mechanism of recognition and reading of different histone modification markers constitutes another challenge of chromatin signaling for gene regulation. Rice as a cereal has specific development and growth specificities. Studying the mechanism of establishment, maintenance, and erasure of specific rice epigenomes will be essential to unravel the epigenetic mechanism of rice gene regulation. Progresses in this field in rice will have a great impact on the understanding of genetic and epigenetic basis of cereal growth and adaptation to environmental conditions such as water, light, temperature, soil, and pathogens. It is suggested that interaction between plant genomes of different origins during crosses may generate specific epigenetic mechanisms of gene regulation such as allelic inactivation and genomic imprinting (Ishikawa and Kinoshita 2009). Epigenomes related to rice hybrid vigor have been recently reported (He et al. 2010). Importantly, it is recently shown that parent plants with little genomic DNA sequence variations, but contrasting epigenetic modification (i.e., DNA methylation) can generate a panel of epigenetic recombinant inbred lines showing variation and high heritability over many generations for several important traits in Arabidopsis (Johannes et al. 2009; Reinders et al. 2009). It remains to know whether variations in chromatin modification (both histone modification and DNA methylation) will be useful as a resource to create novel epigenetic variations controlling important agronomical traits that could be exploited for rice breeding.
- Aufsatz W, Mette MF, van der Winden J, Matzke M, Matzke AJ. HDA6, a putative histone deacetylase needed to enhance DNA methylation induced by double-stranded RNA. Embo J. 2002;21:6832–41.PubMedPubMed CentralView ArticleGoogle Scholar
- Bannister AJ, Kouzarides T. Histone methylation: recognizing the methyl mark. Methods Enzymol. 2004;376:269–88.PubMedView ArticleGoogle Scholar
- Baumbusch LO, Thorstensen T, Krauss V, Fischer A, Naumann K, Assalkhou R, et al. The Arabidopsis thaliana genome contains at least 29 active genes encoding SET domain proteins that can be assigned to four evolutionarily conserved classes. Nucleic Acids Res. 2001;29:4319–33.PubMedPubMed CentralView ArticleGoogle Scholar
- Berger SL. The complex language of chromatin regulation during transcription. Nature. 2007;447:407–12.PubMedView ArticleGoogle Scholar
- Chen ZJ, Tian L. Roles of dynamic and reversible histone acetylation in plant development and polyploidy. Biochim Biophys Acta. 2007;1769:295–307.PubMedPubMed CentralView ArticleGoogle Scholar
- Chung PJ, Kim YS, Jeong JS, Park SH, Nahm BH, Kim JK. The histone deacetylase OsHDAC1 epigenetically regulates the OsNAC6 gene that controls seedling root growth in rice. Plant J. 2009a;59:764–76.PubMedView ArticleGoogle Scholar
- Chung PJ, Kim YS, Park SH, Nahm BH, Kim JK. Subcellular localization of rice histone deacetylases in organelles. FEBS Lett. 2009b;583:2249–54.PubMedView ArticleGoogle Scholar
- Cloos PA, Christensen J, Agger K, Helin K. Erasing the methyl mark: histone demethylases at the center of cellular differentiation and disease. Genes Dev. 2008;22:1115–40.PubMedPubMed CentralView ArticleGoogle Scholar
- Ding Y, Wang X, Su L, Zhai J, Cao S, Zhang D, et al. SDG714, a histone H3K9 methyltransferase, is involved in Tos17 DNA methylation and transposition in rice. Plant Cell. 2007;19:9–22.PubMedPubMed CentralView ArticleGoogle Scholar
- Earley KW, Shook MS, Brower-Toland B, Hicks L, Pikaard CS. In vitro specificities of Arabidopsis co-activator histone acetyltransferases: implications for histone hyperacetylation in gene activation. Plant J. 2007;52:615–26.PubMedView ArticleGoogle Scholar
- Ebbs ML, Bender J. Locus-specific control of DNA methylation by the Arabidopsis SUVH5 histone methyltransferase. Plant Cell. 2006;18:1166–76.PubMedPubMed CentralView ArticleGoogle Scholar
- Ebbs ML, Bartee L, Bender J. H3 lysine 9 methylation is maintained on a transcribed inverted repeat by combined action of SUVH6 and SUVH4 methyltransferases. Mol Cell Biol. 2005;25:10507–15.PubMedPubMed CentralView ArticleGoogle Scholar
- Finkel T, Deng CX, Mostoslavsky R. Recent progress in the biology and physiology of sirtuins. Nature. 2009;460:587–91.PubMedPubMed CentralView ArticleGoogle Scholar
- He G, Zhu X, Elling AA, Chen L, Wang X, Guo L, et al. Global epigenetic and transcriptional trends among two rice subspecies and their reciprocal hybrids. Plant Cell. 2010;22:17–33.PubMedPubMed CentralView ArticleGoogle Scholar
- Hennig L, Derkacheva M. Diversity of polycomb group complexes in plants: same rules, different players? Trends Genet. 2009;25:414–23.PubMedView ArticleGoogle Scholar
- Horn PJ, Peterson CL. Molecular biology. Chromatin higher order folding—wrapping up transcription. Science. 2002;297:1824–7.PubMedView ArticleGoogle Scholar
- Hu Y, Qin F, Huang L, Sun Q, Li C, Zhao Y, et al. Rice histone deacetylase genes display specific expression patterns and developmental functions. Biochem Biophys Res Commun. 2009;388:266–71.PubMedView ArticleGoogle Scholar
- Huang L, Sun Q, Qin F, Li C, Zhao Y, Zhou DX. Down-regulation of a SILENT INFORMATION REGULATOR2-related histone deacetylase gene, OsSRT1, induces DNA fragmentation and cell death in rice. Plant Physiol. 2007;144:1508–19.PubMedPubMed CentralView ArticleGoogle Scholar
- Ishikawa R, Kinoshita T. Epigenetic programming: the challenge to species hybridization. Mol Plant. 2009;2:589–99.PubMedView ArticleGoogle Scholar
- Jackson JP, Johnson L, Jasencakova Z, Zhang X, PerezBurgos L, Singh PB, et al. Dimethylation of histone H3 lysine 9 is a critical mark for DNA methylation and gene silencing in Arabidopsis thaliana. Chromosoma. 2004;112:308–15.PubMedView ArticleGoogle Scholar
- Jacob Y, Feng S, LeBlanc CA, Bernatavichute YV, Stroud H, Cokus S, et al. ATXR5 and ATXR6 are H3K27 monomethyltransferases required for chromatin structure and gene silencing. Nat Struct Mol Biol. 2009;16:763–8.PubMedPubMed CentralView ArticleGoogle Scholar
- Jang IC, Pahk YM, Song SI, Kwon HJ, Nahm BH, Kim JK. Structure and expression of the rice class-I type histone deacetylase genes OsHDAC1-3: OsHDAC1 overexpression in transgenic plants leads to increased growth rate and altered architecture. Plant J. 2003;33:531–41.PubMedView ArticleGoogle Scholar
- Jeong JH, Song HR, Ko JH, Jeong YM, Kwon YE, Seol JH, et al. Repression of FLOWERING LOCUS T chromatin by functionally redundant histone H3 lysine 4 demethylases in Arabidopsis. PLoS One. 2009;4:e8033.PubMedPubMed CentralView ArticleGoogle Scholar
- Jiang D, Yang W, He Y, Amasino RM. 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. 2007;19:2975–87.PubMedPubMed CentralView ArticleGoogle Scholar
- Johannes F, Porcher E, Teixeira FK, Saliba-Colombani V, Simon M, Agier N, et al. Assessing the impact of transgenerational epigenetic variation on complex traits. PLoS Genet. 2009;5:e1000530.PubMedPubMed CentralView ArticleGoogle Scholar
- Johnson LM, Bostick M, Zhang X, Kraft E, Henderson I, Callis J, et al. The SRA methyl-cytosine-binding domain links DNA and histone methylation. Curr Biol. 2007;17:379–84.PubMedPubMed CentralView ArticleGoogle Scholar
- Klose RJ, Kallin EM, Zhang Y. JmjC-domain-containing proteins and histone demethylation. Nat Rev Genet. 2006;7:715–27.PubMedView ArticleGoogle Scholar
- Komiya R, Ikegami A, Tamaki S, Yokoi S, Shimamoto K. Hd3a and RFT1 are essential for flowering in rice. Development. 2008;135:767–74.PubMedView ArticleGoogle Scholar
- Li X, Wang X, He K, Ma Y, Su N, He H, et al. High-resolution mapping of epigenetic modifications of the rice genome uncovers interplay between DNA methylation, histone methylation, and gene expression. Plant Cell. 2008;20:259–76.PubMedPubMed CentralView ArticleGoogle Scholar
- Lippman Z, Gendrel AV, Black M, Vaughn MW, Dedhia N, McCombie WR, et al. Role of transposable elements in heterochromatin and epigenetic control. Nature. 2004;430:471–6.PubMedView ArticleGoogle Scholar
- Luo M, Platten D, Chaudhury A, Peacock WJ, Dennis ES. Expression, imprinting, and evolution of rice homologs of the polycomb group genes. Mol Plant. 2009;2:711–23.PubMedView ArticleGoogle Scholar
- Lusser A, Brosch G, Loidl A, Haas H, Loidl P. Identification of maize histone deacetylase HD2 as an acidic nucleolar phosphoprotein. Science. 1997;277:88–91.PubMedView ArticleGoogle Scholar
- Millar CB, Grunstein M. Genome-wide patterns of histone modifications in yeast. Nat Rev Mol Cell Biol. 2006;7:657–66.PubMedView ArticleGoogle Scholar
- Pandey R, Muller A, Napoli CA, Selinger DA, Pikaard CS, Richards EJ, et al. Analysis of histone acetyltransferase and histone deacetylase families of Arabidopsis thaliana suggests functional diversification of chromatin modification among multicellular eukaryotes. Nucleic Acids Res. 2002;30:5036–55.PubMedPubMed CentralView ArticleGoogle Scholar
- Pfluger J, Wagner D. Histone modifications and dynamic regulation of genome accessibility in plants. Curr Opin Plant Biol. 2007;10:645–52.PubMedPubMed CentralView ArticleGoogle Scholar
- Pien S, Grossniklaus U. Polycomb group and trithorax group proteins in Arabidopsis. Biochim Biophys Acta. 2007;1769:375–82.PubMedView ArticleGoogle Scholar
- Pien S, Fleury D, Mylne JS, Crevillen P, Inze D, Avramova Z, et al. ARABIDOPSIS TRITHORAX1 dynamically regulates FLOWERING LOCUS C activation via histone 3 lysine 4 trimethylation. Plant Cell. 2008;20:580–8.PubMedPubMed CentralView ArticleGoogle Scholar
- Pontes O, Lawrence RJ, Silva M, Preuss S, Costa-Nunes P, Earley K, et al. Postembryonic establishment of megabase-scale gene silencing in nucleolar dominance. PLoS One. 2007;2:e1157.PubMedPubMed CentralView ArticleGoogle Scholar
- Qin F, Sun Q, Huang L, Chen X, Zhou D-X. Rice SUVH Histone Methyltransferase Genes Display Specific Functions in Chromatin Modification and Retrotransposon Repression. Mol Plant. 2010 (in press)Google Scholar
- Rea S, Eisenhaber F, O’Carroll D, Strahl BD, Sun ZW, Schmid M, et al. Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature. 2000;406:593–9.PubMedView ArticleGoogle Scholar
- Reinders J, Wulff BB, Mirouze M, Mari-Ordonez A, Dapp M, Rozhon W, et al. Compromised stability of DNA methylation and transposon immobilization in mosaic Arabidopsis epigenomes. Genes Dev. 2009;23:939–50.PubMedPubMed CentralView ArticleGoogle Scholar
- Saleh A, Alvarez-Venegas R, Avramova Z. Dynamic and stable histone H3 methylation patterns at the Arabidopsis FLC and AP1 loci. Gene. 2008;423:43–7.PubMedView ArticleGoogle Scholar
- Saze H, Shiraishi A, Miura A, Kakutani T. Control of genic DNA methylation by a jmjC domain-containing protein in Arabidopsis thaliana. Science. 2008;319:462–5.PubMedView ArticleGoogle Scholar
- Searle IR, Pontes O, Melnyk CW, Smith LM, Baulcombe DC. JMJ14, a JmjC domain protein, is required for RNA silencing and cell-to-cell movement of an RNA silencing signal in Arabidopsis. Genes Dev. 2010;24:986–91.PubMedPubMed CentralView ArticleGoogle Scholar
- Servet C, Conde e Silva N, Zhou D-X. Histone acetyltransferase AtGCN5/HAG1 is a versatile regulator of developmental and inducible gene expression in Arabidopsis. Mol Plant. 2010 (in press)Google Scholar
- Shi Y, Lan F, Matson C, Mulligan P, Whetstine JR, Cole PA, et al. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell. 2004;119:941–53.PubMedView ArticleGoogle Scholar
- Sims 3rd RJ, Nishioka K, Reinberg D. Histone lysine methylation: a signature for chromatin function. Trends Genet. 2003;19:629–39.PubMedView ArticleGoogle Scholar
- Soppe WJ, Jasencakova Z, Houben A, Kakutani T, Meister A, Huang MS, et al. DNA methylation controls histone H3 lysine 9 methylation and heterochromatin assembly in Arabidopsis. Embo J. 2002;21:6549–59.PubMedPubMed CentralView ArticleGoogle Scholar
- Sun Q, Zhou DX. Rice jmjC domain-containing gene JMJ706 encodes H3K9 demethylase required for floral organ development. Proc Natl Acad Sci U S A. 2008;105:13679–84.PubMedPubMed CentralView ArticleGoogle Scholar
- Sun QR. Rice histone modification enzyme studies. PhD Thesis, Huazhong Agricultural University, Wuhan, China; 2009.Google Scholar
- Tamada Y, Yun JY, Woo SC, Amasino RM. ARABIDOPSIS TRITHORAX-RELATED7 is required for methylation of lysine 4 of histone H3 and for transcriptional activation of FLOWERING LOCUS C. Plant Cell. 2009;21:3257–69.PubMedPubMed CentralView ArticleGoogle Scholar
- Tariq M, Saze H, Probst AV, Lichota J, Habu Y, Paszkowski J. Erasure of CpG methylation in Arabidopsis alters patterns of histone H3 methylation in heterochromatin. Proc Natl Acad Sci U S A. 2003;100:8823–7.PubMedPubMed CentralView ArticleGoogle Scholar
- Tian L, Chen ZJ. Blocking histone deacetylation in Arabidopsis induces pleiotropic effects on plant gene regulation and development. Proc Natl Acad Sci U S A. 2001;98:200–5.PubMedPubMed CentralView ArticleGoogle Scholar
- Trewick SC, McLaughlin PJ, Allshire RC. Methylation: lost in hydroxylation? EMBO Rep. 2005;6:315–20.PubMedPubMed CentralView ArticleGoogle Scholar
- Tsuji H, Saika H, Tsutsumi N, Hirai A, Nakazono M. Dynamic and reversible changes in histone H3-Lys4 methylation and H3 acetylation occurring at submergence-inducible genes in rice. Plant Cell Physiol. 2006;47:995–1003.PubMedView ArticleGoogle Scholar
- Turck F, Roudier F, Farrona S, Martin-Magniette ML, Guillaume E, Buisine N, et al. Arabidopsis TFL2/LHP1 specifically associates with genes marked by trimethylation of histone H3 lysine 27. PLoS Genet. 2007;3:e86.PubMedPubMed CentralView ArticleGoogle Scholar
- Vermaak D, Malik HS. Multiple roles for heterochromatin protein 1 genes in Drosophila. Annu Rev Genet. 2009;43:467–92.PubMedView ArticleGoogle Scholar
- Wu K, Malik K, Tian L, Brown D, Miki B. Functional analysis of a RPD3 histone deacetylase homologue in Arabidopsis thaliana. Plant Mol Biol. 2000;44:167–76.PubMedView ArticleGoogle Scholar
- Xu CR, Liu C, Wang YL, Li LC, Chen WQ, Xu ZH, et al. Histone acetylation affects expression of cellular patterning genes in the Arabidopsis root epidermis. Proc Natl Acad Sci U S A. 2005;102:14469–74.PubMedPubMed CentralView ArticleGoogle Scholar
- Yang W, Jiang D, Jiang J, He Y. A plant-specific histone H3 lysine-4 demethylase represses the floral transition in Arabidopsis. Plant J. 2010;62:663–73.PubMedView ArticleGoogle Scholar
- Yin BL, Guo L, Zhang DF, Terzaghi W, Wang XF, Liu TT, et al. Integration of cytological features with molecular and epigenetic properties of rice chromosome 4. Mol Plant. 2008;1:816–29.PubMedView ArticleGoogle Scholar
- Zhang K, Sridhar VV, Zhu J, Kapoor A, Zhu JK. Distinctive core histone post-translational modification patterns in Arabidopsis thaliana. PLoS One. 2007a;2:e1210.PubMedPubMed CentralView ArticleGoogle Scholar
- Zhang X, Germann S, Blus BJ, Khorasanizadeh S, Gaudin V, Jacobsen SE. The Arabidopsis LHP1 protein colocalizes with histone H3 Lys27 trimethylation. Nat Struct Mol Biol. 2007b;14:869–71.PubMedView ArticleGoogle Scholar
- Zhou DX. Regulatory mechanism of histone epigenetic modifications in plants. Epigenetics. 2009;4:15–8.PubMedView ArticleGoogle Scholar