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ABSTRACT: During recent years rice genome-wide epigenomic information such as DNA methylation and histone modifications, which are important for genome activity has been accumulated. The function of a number of rice epigenetic regulators has been studied, many of which are found to be involved in a diverse range of developmental and stress-responsive pathways. Analysis of epigenetic variations among different rice varieties indicates that epigenetic modification may lead to inheritable phenotypic variation. Characterizing phenotypic consequences of rice epigenomic variations and the underlining chromatin mechanism and identifying epialleles related to important agronomic traits may provide novel strategies to enhance agronomically favorable traits and grain productivity in rice.
Current opinion in plant biology 04/2013; · 10.33 Impact Factor
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ABSTRACT: Histone lysine methylation is an important epigenetic modification in regulating chromatin structure and gene expression. Histone H3 lysine 4 methylation (H3K4me), which can be in a mono-, di-, or trimethylated state, has been shown to play an important role in gene expression involved in plant developmental control and stress adaptation. However, the resetting mechanism of this epigenetic modification is not yet fully understood. In this work, we identified a JmjC domain-containing protein, JMJ703, as a histone lysine demethylase that specifically reverses all three forms of H3K4me in rice. Loss-of-function mutation of the gene affected stem elongation and plant growth, which may be related to increased expression of cytokinin oxidase genes in the mutant. Analysis of crystal structure of the catalytic core domain (c-JMJ703) of the protein revealed a general structural similarity with mammalian and yeast JMJD2 proteins that are H3K9 and H3K36 demethylases. However, several specific features were observed in the structure of c-JMJ703. Key residues that interact with cofactors Fe(II) and N-oxalylglycine and the methylated H3K4 substrate peptide were identified and were shown to be essential for the demethylase activity in vivo. Several key residues are specifically conserved in known H3K4 demethylases, suggesting that they may be involved in the specificity for H3K4 demethylation.
PLoS Genetics 01/2013; 9(1):e1003239. · 8.69 Impact Factor
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ABSTRACT: Flowering time is tightly controlled by several regulatory pathways including photoperiod, vernalization in which epigenetic processes are involved. In this work, we have found that the Arabidopsis histone deacetylase gene HDA9 is involved in flowering time control. Mutation of the gene led to an early flowering phenotype in short day grown plants while without effect in long days. Analysis of flowering time regulatory gene expression revealed that hda9 mutations highly induced the expression of AGL19, but had no effect on CO, SOC1 or FLC. Chromatin immunoprecipitation assays indicated that the mutations led to a clear increase of histone H3K9 and H3K27 acetylation on the AGL19 gene in short days. AGL19 promotes flowering in a way independent of the CO and FLC pathways and has been shown to be repressed by polycomb group repressive complex2 (PRC2) EMF2 but activated by vernalization. The induced levels of AGL19 expression and histone acetylation by the hda9 mutations were comparable to that of the gene under long day conditions, indicating that AGL19 is regulated also by day length and that HDA9 is involved in short day repression of AGL19 by promoting histone H3 deacetylation, which may be related to the PRC2 EMF2 complex.
Biochemical and Biophysical Research Communications 12/2012; · 2.48 Impact Factor
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ABSTRACT: Epigenomes including genome-wide histone modification and DNA methylation profiles are important for genome activity and for defining gene expression patterns of plant development and responses to various environmental conditions. Rice is the most important crop plant and serves as a model for cereal genomics. Rice epigenomic landscape is emerging and the function of chromatin modification regulators in gene expression, transposon repression and plant development is being characterized. Epigenomic variation that gives rise to stable or transgenerational heritable epialleles related to variation of important agronomical traits or stress responses is being characterized in rice. Implication of epigenomic variation in rice heterosis is being exploited.
Journal of Genetics and Genomics 07/2012; 39(7):307-15. · 1.88 Impact Factor
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ABSTRACT: Histone lysine methylation is an important component of the epigenetic system demarcating transcriptionally active and inactive chromatin domains. It is of primary importance in understanding how different histone lysine methylation marks and a specific combination of them are read and interpreted by chromatin proteins to regulate gene expression. In this paper, we report that the rice CHD3 protein CHR729 that was required for many aspects of plant development can interact with dimethylated histone H3 lysine 4 (H3K4me2, a mark associated with moderately expressed or repressed genes) and with trimethylated histone H3 lysine 27 (H3K27me3, a mark associated with repressed genes), respectively, through the chromodomains and the plant homeodomain (PHD) finger of the protein. A mutation or down-regulation of the gene provoked a decrease of H3K27me3 and H3K4me3 (a mark associated with active genes). Genome-wide analysis revealed that H3K27me3 and H3K4me3, respectively, were lost from about 56 and 23% of marked loci, which correspond mostly to under-expressed or repressed genes. In the mutant, a higher-than-expected proportion of down-regulated genes lost H3K4me3, among which many encode DNA-binding transcription factors. These results suggest that the rice CHD3 protein is a bifunctional chromatin regulator able to recognize and modulate H3K4 and H3K27 methylation over repressed or tissue-specific genes, which may be associated with regulation of a gene transcription program of plant development.
Proceedings of the National Academy of Sciences 03/2012; 109(15):5773-8. · 9.68 Impact Factor
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ABSTRACT: Histone methylation plays an important role in epigenetic regulation of gene expression. Reversible methylation/demethylation of several histone lysine residues is mediated by distinct histone methyltransferases and histone demethylases. Jumonji proteins have been characterized to be involved in histone demethylation. Plant Jumonji homologues are found to have important functions in epigenetic processes, gene expression and plant development and to play an essential role in interplay between histone modifications and DNA methylation. This article is part of a Special Issue entitled: Epigenetic Control of cellular and developmental processes in plants.
Biochimica et Biophysica Acta 03/2011; 1809(8):421-6. · 4.66 Impact Factor
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ABSTRACT: Hybrids between different inbred varieties display novel patterns of gene expression resulted from parental variation in allelic nucleotide sequences. To study the function of chromatin regulators in hybrid gene expression, the histone deacetylase gene OsHDT1 whose expression displayed a circadian rhythm was over-expressed or inactivated by RNAi in an elite rice parent. Increased OsHDT1 expression did not affect plant growth in the parent but led to early flowering in the hybrid. Nonadditive up-regulation of key flowering time genes was found to be related to flowering time of the hybrid. Over-expression of OsHDT1 repressed the nonadditive expression of the key flowering repressors in the hybrid (i.e. OsGI and Hd1) inducing early flowering. Analysis of histone acetylation suggested that OsHDT1 over-expression might promote deacetylation on OsGI and Hd1 chromatin during the peak expression phase. High throughput differential gene expression analysis revealed that altered OsHDT1 levels affected nonadditive expression of many genes in the hybrid. These data demonstrate that nonadditive gene expression was involved in flowering time control in the hybrid rice and that OsHDT1 level was important for nonadditive or differential expression of many genes including the flowering time genes, suggesting that OsHDT1 may be involved in epigenetic control of parental genome interaction for differential gene expression.
PLoS ONE 01/2011; 6(7):e21789. · 4.09 Impact Factor
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ABSTRACT: Ethylene signaling pathway leads to rapid gene activation by two hierarchies of transcription factors with EIN3/EIL proteins as primary ones and ERF proteins as secondary ones. The role of chromatin modifications during the rapid gene activation is not known. In this work we studied trimethylated histone H3 lysine 4 (H3K4me3) and lysine 27 (H3K27me3), two opposite histone methylation marks for gene activity, during the induction course of three ethylene-responsive genes (ERF1, AtERF14 and ChiB). We found that the three genes displayed different histone modification profiles before induction. After induction, H3K4me3 was increased in the 5' region and the gene body of ERF1, while H3K27me3 was decreased in the promoter of AtERF14. But the modification changes were later than the gene activation. Analysis of other rapidly inducible ERF genes confirmed the observation. In addition, histone H2A.Z occupancy on the three genes and the association of the H3K27me3-binding protein LHP1 with AtERF14 and ChiB were not affected by the inductive signal. However, the mutation of genes encoding H2A.Z and LHP1 attenuated and enhanced respectively the induction of target genes and altered H3K4me3. These results indicate that the induction of ethylene-responsive genes does not require immediate modulation of H3K4me3 and H3K27me3 and dissociation of LHP1 and H2A.Z from the targets, and suggest that the chromatin structure of the genes before induction is committed for transcriptional activation and that H3K4me3 is not required for ethylene-responsive gene activation, but may serve as a mark for gene activity.
PLoS ONE 01/2011; 6(11):e28224. · 4.09 Impact Factor
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ABSTRACT: Histone lysine methylation plays an important role in heterochromatin formation and reprogramming of gene expression. SET-domain-containing proteins are shown to have histone lysine methyltransferase activities. A large number of SET-domain genes are identified in plant genomes. The function of most SET-domain genes is not known. In this work, we studied the 12 rice (Oryza sativa) homologs of Su(var)3-9, the histone H3 lysine 9 (H3K9) methyltransferase identified in Drosophila. Several rice SUVHs (i.e. SDG714, SDG727, and SDG710) were found to have an antagonistic function to the histone H3K9 demethylase JMJ706, as down-regulation of these genes could partially complement the jmj706 phenotype and reduced histone H3K9 methylation. Down-regulation of a rice Su(var)3-9 homolog (SUVH), namely SDG728, decreased H3K9 methylation and altered seed morphology. Overexpression of the gene increased H3K9 methylation. SDG728 and other SUVH genes were found to be involved in the repression of retrotransposons such as Tos17 and a Ty1-copia element. Analysis of histone methylation suggested that SDG728-mediated H3K9 methylation may play an important role in retrotransposon repression.
Molecular plant 07/2010; 3(4):773-82. · 5.55 Impact Factor
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ABSTRACT: Histone acetylation/deacetylation is a dynamic process and plays an important role in gene regulation. Histone acetylation homeostasis is regulated by antagonist actions of histone acetyltransferases (HAT) and deacetylases (HDAC). Plant genome encodes multiple HATs and HDACs. The Arabidopsis HAT gene AtGCN5/HAG1plays an essential role in many plant development processes, such as meristem function, cell differentiation, leaf and floral organogenesis, and responses to environmental conditions such as light and cold, indicating an important role of this HAT in the regulation of both long-term developmental switches and short-term inducible gene expression. AtGCN5 targets to a large number of promoters and is required for acetylation of several histone H3 lysine residues. Recruitment of AtGCN5 to target promoters is likely to be mediated by direct or indirect interaction with DNA-binding transcription factors and/or by interaction with acetylated histone lysine residues on the targets. Interplay between AtGCN5 and other HAT and HDAC is demonstrated to control specific regulatory pathways. Analysis of the role of AtGCN5 in light-inducible gene expression suggests a function of AtGCN5 in preparing chromatin commitment for priming inducible gene activation in plants.
Molecular plant 05/2010; 3(4):670-7. · 5.55 Impact Factor
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ABSTRACT: Histone deacetylases (HDAC) are important in plant gene expression. Here we show that the expression of rice HDAC genes is both tissue/organ-specific, and most of them are responsive to drought or salt stresses. Over-expression of several rice HDACs did not produce any visible phenotype, whereas down-regulation of a few HDAC genes affected different developmental aspects. Specifically, down-regulation of HDA703 by amiRNA reduced rice peduncle elongation and fertility, while inactivation of a closely related homolog HDA710 by RNAi affected vegetative growth. HDA704 RNAi altered plant height and flag leaf morphology. Down-regulation of HDT702 led to the production of narrowed leaves and stems. These data suggest that rice HDAC genes may have divergent developmental functions compared with closely related homologs in Arabidopsis.
Biochemical and Biophysical Research Communications 09/2009; 388(2):266-71. · 2.48 Impact Factor
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ABSTRACT: MicroRNAs (miRNA) that guide sequence-specific posttranscriptional gene silencing play an important role in gene expression required for both developmental processes and responses to environmental conditions in plants. However, little is known about the transcriptional and posttranscriptional regulation of miRNA expression. Histone acetylation plays an important role in chromatin remodeling and is required for gene activation. By analyzing the accumulation of subset of miRNAs and the corresponding primary miRNAs in mutants of Arabidopsis, we show that histone acetyltransferase GCN5 (General control non-repressed protein5) has a general repressive effect on miRNA production, while it is required for the expression of a subset of (e.g. stress-inducible) MIRNA genes. The general negative function of GCN5 in miRNA production is likely achieved through an indirect repression of the miRNA machinery genes such as DICER LIKE1 (DCL1), SERRATE (SE), HYPONASTIC LEAVES1 (HYL1) and ARGONAUTE1 (AGO1). Chromatin immunoprecipitation assays revealed that GCN5 targets to a subset of MIRNA genes and is required for acetylation of histone H3 lysine 14 at these loci. Moreover, inhibition of histone deacetylation by trichostatin A treatment or in histone deacetylase gene mutants impaired the accumulation of certain miRNAs. These data together suggest that Arabidopsis GCN5 interferes with the miRNA pathway at both the transcriptional and posttranscriptional levels and histone acetylation/deacetylation is an epigenetic mechanism involved in the regulation of miRNA production.
Cell Research 06/2009; 19(7):899-909. · 8.19 Impact Factor
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ABSTRACT: In rice (Oryza sativa), the shoot-borne crown roots are the major root type and are initiated at lower stem nodes as part of normal plant development. However, the regulatory mechanism of crown root development is poorly understood. In this work, we show that a WUSCHEL-related Homeobox (WOX) gene, WOX11, is involved in the activation of crown root emergence and growth. WOX11 was found to be expressed in emerging crown roots and later in cell division regions of the root meristem. The expression could be induced by exogenous auxin or cytokinin. Loss-of-function mutation or downregulation of the gene reduced the number and the growth rate of crown roots, whereas overexpression of the gene induced precocious crown root growth and dramatically increased the root biomass by producing crown roots at the upper stem nodes and the base of florets. The expressions of auxin- and cytokinin-responsive genes were affected in WOX11 overexpression and RNA interference transgenic plants. Further analysis showed that WOX11 directly repressed RR2, a type-A cytokinin-responsive regulator gene that was found to be expressed in crown root primordia. The results suggest that WOX11 may be an integrator of auxin and cytokinin signaling that feeds into RR2 to regulate cell proliferation during crown root development.
The Plant Cell 04/2009; 21(3):736-48. · 8.99 Impact Factor
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Dao-Xiu Zhou
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ABSTRACT: Histone H3 lysine 9 and lysine 27 are two important targets for epigenetic modifications in plants. H3K9 methylation is either associated with heterochromatin formation or gene repression, while H3K27 methylation profile is likely to be involved in gene expression required for developmental decisions. Although a number of modification enzymes are being identified, the mode of action and functional interplay between the histone modification enzymes and other chromatin pathways remain largely unknown. Studying the regulatory mechanism of histone H3K9 and H3K27 modification would provide important clues to reveal the molecular basis of establishment, inheritance and erasure of epigenetic information during plant cell division and differentiation.
Epigenetics: official journal of the DNA Methylation Society 02/2009; 4(1):15-8. · 4.58 Impact Factor
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ABSTRACT: Histone acetyltransferases (HATs) play critical roles in the regulation of chromatin structure and gene expression. Arabidopsis genome contains 12 HAT genes, but the biological functions of many of them are still unknown. In this work, we studied the evolutionary relationship and cellular functions of the two Arabidopsis HAT genes homologous to the MYST family members.
An extensive phylogenetic analysis of 105 MYST proteins revealed that they can be divided into 5 classes, each of which contains a specific combination of protein modules. The two Arabidopsis MYST proteins, HAM1 and HAM2, belong to a "green clade", clearly separated from other families of HATs. Using a reverse genetic approach, we show that HAM1 and HAM2 are a functionally redundant pair of genes, as single Arabidopsis ham1 and ham2 mutants displayed a wild-type phenotype, while no double mutant seedling could be recovered. Genetic analysis and cytological study revealed that ham1ham2 double mutation induced severe defects in the formation of male and female gametophyte, resulting in an arrest of mitotic cell cycle at early stages of gametogenesis. RT-PCR experiments and the analysis of transgenic plants expressing the GUS reporter gene under the HAM1 or the HAM2 promoter showed that both genes displayed an overlapping expression pattern, mainly in growing organs such as shoots and flower buds.
The work presented here reveals novel properties for MYST HATs in Arabidopsis. In addition to providing an evolutionary relationship of this large protein family, we show the evidence of a link between MYST and gamete formation as previously suggested in mammalian cells. A possible function of the Arabidopsis MYST protein-mediated histone acetylation during cell division is suggested.
BMC Plant Biology 12/2008; 8:121. · 3.45 Impact Factor
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Moussa Benhamed,
Marie-Laure Martin-Magniette,
Ludivine Taconnat,
Frédérique Bitton,
Caroline Servet,
Rebecca De Clercq,
Björn De Meyer,
Caroline Buysschaert,
Stéphane Rombauts,
Raimundo Villarroel,
Sébastien Aubourg,
Jim Beynon,
Rishikesh P Bhalerao,
George Coupland,
Wilhelm Gruissem,
Frank L H Menke,
Bernd Weisshaar,
Jean-Pierre Renou, Dao-Xiu Zhou,
Pierre Hilson
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ABSTRACT: We have assembled approximately 20 000 Arabidopsis thaliana promoter regions, compatible with functional studies that require cloning and with microarray applications. The promoter fragments can be captured as modular entry clones (MultiSite Gateway format) via site-specific recombinational cloning, and transferred into vectors of choice to investigate transcriptional networks. The fragments can also be amplified by PCR and printed on glass arrays. In combination with immunoprecipitation of protein-DNA complexes (ChIP-chip), these arrays enable characterization of binding sites for chromatin-associated proteins or the extent of chromatin modifications at genome scale. The Arabidopsis histone acetyltransferase GCN5 associated with 40% of the tested promoters. At most sites, binding did not depend on the integrity of the GCN5 bromodomain. However, the presence of the bromodomain was necessary for binding to 11% of the promoter regions, and correlated with acetylation of lysine 14 of histone H3 in these promoters. Combined analysis of ChIP-chip and transcriptomic data indicated that binding of GCN5 does not strictly correlate with gene activation. GCN5 has previously been shown to be required for light-regulated gene expression and growth, and we found that GCN5 targets were enriched in early light-responsive genes. Thus, in addition to its transcriptional activation function, GCN5 may play an important role in priming activation of inducible genes under non-induced conditions.
The Plant Journal 11/2008; 56(3):493-504. · 6.16 Impact Factor
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Moussa Benhamed,
Marie-Laure Martin-Magniette,
Ludivine Taconnat,
Frédérique Bitton,
Caroline Servet,
Rebecca De Clercq,
Björn De Meyer,
Caroline Buysschaert,
Stéphane Rombauts,
Raimundo Villarroel,
Sébastien Aubourg,
Jim Beynon,
Rishikesh P. Bhalerao,
George Coupland,
Wilhelm Gruissem,
Frank L.H. Menke,
Bernd Weisshaar,
Jean-Pierre Renou, Dao-Xiu Zhou,
Pierre Hilson
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ABSTRACT: We have assembled approximately 20 000 Arabidopsis thaliana promoter regions, compatible with functional studies that require cloning and with microarray applications. The promoter fragments can be captured as modular entry clones (MultiSite Gateway format) via site-specific recombinational cloning, and transferred into vectors of choice to investigate transcriptional networks. The fragments can also be amplified by PCR and printed on glass arrays. In combination with immunoprecipitation of protein–DNA complexes (ChIP–chip), these arrays enable characterization of binding sites for chromatin-associated proteins or the extent of chromatin modifications at genome scale. The Arabidopsis histone acetyltransferase GCN5 associated with 40% of the tested promoters. At most sites, binding did not depend on the integrity of the GCN5 bromodomain. However, the presence of the bromodomain was necessary for binding to 11% of the promoter regions, and correlated with acetylation of lysine 14 of histone H3 in these promoters. Combined analysis of ChIP–chip and transcriptomic data indicated that binding of GCN5 does not strictly correlate with gene activation. GCN5 has previously been shown to be required for light-regulated gene expression and growth, and we found that GCN5 targets were enriched in early light-responsive genes. Thus, in addition to its transcriptional activation function, GCN5 may play an important role in priming activation of inducible genes under non-induced conditions.
The Plant Journal 10/2008; 56(3):493 - 504. · 6.16 Impact Factor
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ABSTRACT: Histone lysine methylation is an important epigenetic modification with both activating and repressive roles in gene expression. Jumonji C (jmjC) domain-containing proteins have been shown to reverse histone methylation in nonplant model systems. Here, we show that plant Jumonji C proteins have both conserved and specific features compared with mammalian homologues. In particular, the rice JMJD2 family jmjC gene JMJ706 is shown to encode a heterochromatin-enriched protein. The JMJ706 protein specifically reverses di- and trimethylations of lysine 9 of histone H3 (H3K9) in vitro. Loss-of-function mutations of the gene lead to increased di- and trimethylations of H3K9 and affect the spikelet development, including altered floral morphology and organ number. Gene expression and histone modification analysis indicates that JMJ706 regulates a subset of flower development regulatory genes. Taken together, our data suggest that rice JMJ706 encodes a heterochromatin-associated H3K9 demethylase involved in the regulation of flower development in rice.
Proceedings of the National Academy of Sciences 10/2008; 105(36):13679-84. · 9.68 Impact Factor
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ABSTRACT: The homeodomain-leucine zipper (HD-Zip) putative transcription factor genes are divided into 4 families. In this work, we studied the function of a rice HD-Zip I gene, H OME O BO X4 (Oshox4). Oshox4 transcripts were detected in leaf and floral organ primordia but excluded from the shoot apical meristem and the protein was nuclear localized. Over-expression of Oshox4 in rice induced a semi-dwarf phenotype that could not be complemented by applied GA3. The over-expression plants accumulated elevated levels of bioactive GA, while the GA catabolic gene GA2ox3 was upregulated in the transgenic plants. In addition, over-expression of Oshox4 blocked GA-dependent alpha-amylase production. However, down-regulation of Oshox4 in RNAi transgenic plants induced no phenotypic alteration. Interestingly, the expression of YAB1 that is involved in the negative feedback regulation of the GA biosynthesis was upregulated in the Oshox4 over-expressing plants. One-hybrid assays showed that Oshox4 could interact with YAB1 promoter in yeast. In addition, Oshox4 expression was upregulated by GA. These data together suggest that Oshox4 may be involved in the negative regulation of GA signalling and may play a role to fine tune GA responses in rice.
Plant Molecular Biology 03/2008; 66(3):289-301. · 4.15 Impact Factor
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ABSTRACT: The objective of this study was to identify rice gene promoters that are specifically induced by feeding of the striped stemborer (Chilo suppressalis). Two PCR-selected cDNA subtractive libraries were constructed from the rice variety Minghui 63. Up- and down-regulated cDNAs induced by C. suppressalis feeding were arrayed on nylon membranes. After array hybridization and Northern blot analysis, a cDNA (B1-A04) encoding a putative subtilisin/chymotrypsin inhibitor was found to be rapidly and highly induced by C. suppressalis feeding, compared with mechanical wounding. The putative promoter region, spanning from -1,569 to +446 relative to the transcriptional initiation site was isolated, fused to the GUS gene (beta-glucuronidase reporter gene) and introduced by Agrobacterium-mediated transformation to rice. In non-infested plants, the GUS activity driven by this promoter fragment was detected in culms and panicles, but not in leaves and sheaths. At 6 h after insect feeding, GUS activity was significantly induced in sheaths and culms, but not in leaves. GUS activity and native B1-A04 gene were not induced by JA and ABA treatment. A serial deletion analysis revealed two regions (-1,569 to -1,166 and -1,166 to -582) that negatively regulate the gene expression in sheaths of non-infested plants but not in insect-infested plants. An electrophoretic mobility shift assay (EMSA) identified 7 DNA fragments with various binding activities with nuclear proteins from mechanically wounded, insect-infested and untreated plants, and their possible roles in gene regulation were speculated. This promoter fragment should have utility in development of insect resistant transgenic crops.
Plant Molecular Biology 12/2007; 65(4):519-30. · 4.15 Impact Factor
