Arabidopsis HDA6 Regulates Locus-Directed Heterochromatin Silencing in Cooperation with MET1

Heterochromatin silencing is pivotal for genome stability in eukaryotes. In Arabidopsis, a plant-specific mechanism called RNA–directed DNA methylation (RdDM) is involved in heterochromatin silencing. Histone deacetylase HDA6 has been identified as a component of such machineries; however, its endogenous targets and the silencing mechanisms have not been analyzed globally. In this study, we investigated the silencing mechanism mediated by HDA6. Genome-wide transcript profiling revealed that the loci silenced by HDA6 carried sequences corresponding to the RDR2-dependent 24-nt siRNAs, however their transcript levels were mostly unaffected in the rdr2 mutant. Strikingly, we observed significant overlap of genes silenced by HDA6 to those by the CG DNA methyltransferase MET1. Furthermore, regardless of dependence on RdDM pathway, HDA6 deficiency resulted in loss of heterochromatic epigenetic marks and aberrant enrichment for euchromatic marks at HDA6 direct targets, along with ectopic expression of these loci. Acetylation levels increased significantly in the hda6 mutant at all of the lysine residues in the H3 and H4 N-tails, except H4K16. Interestingly, we observed two different CG methylation statuses in the hda6 mutant. CG methylation was sustained in the hda6 mutant at some HDA6 target loci that were surrounded by flanking DNA–methylated regions. In contrast, complete loss of CG methylation occurred in the hda6 mutant at the HDA6 target loci that were isolated from flanking DNA methylation. Regardless of CG methylation status, CHG and CHH methylation were lost and transcriptional derepression occurred in the hda6 mutant. Furthermore, we show that HDA6 binds only to its target loci, not the flanking methylated DNA, indicating the profound target specificity of HDA6. We propose that HDA6 regulates locus-directed heterochromatin silencing in cooperation with MET1, possibly recruiting MET1 to specific loci, thus forming the foundation of silent chromatin structure for subsequent non-CG methylation

Epigenetic regulation of gene responsiveness in Arabidopsis

The regulation of chromatin structure is inevitable for proper transcriptional response in eukaryotes. Recent reports in Arabidopsis have suggested that gene responsiveness is modulated by particular chromatin status. One such feature is H2A.Z, a histone variant conserved among eukaryotes. In Arabidopsis, H2A.Z is enriched within gene bodies of transcriptionally variable genes, which is in contrast to genic DNA methylation found within constitutive genes. In the absence of H2A.Z, the genes normally harboring H2A.Z within gene bodies are transcriptionally misregulated, while DNA methylation is unaffected. Therefore, H2A.Z may promote variability of gene expression without affecting genic DNA methylation. Another epigenetic information that could be important for gene responsiveness is trimethylation of histone H3 lysine 4 (H3K4me3). The level of H3K4me3 increases when stress responsive genes are transcriptionally activated, and it decreases after recovery from the stress. Even after the recovery, however, H3K4me3 is kept at some atypical levels, suggesting possible role of H3K4me3 for a stress memory. In this review, we summarize and discuss the growing evidences connecting chromatin features and gene responsiveness

Simple and universal function of acetic acid to overcome the drought crisis

Abstract Acetic acid is a simple and universal compound found in various organisms. Recently, acetic acid was found to play an essential role in conferring tolerance to water deficit stress in plants. This novel mechanism of drought stress tolerance mediated by acetic acid via networks involving phytohormones, genes, and chromatin regulation has great potential for solving the global food crisis and preventing desertification caused by global warming. We highlight the functions of acetic acid in conferring tolerance to water deficit stress

The Cold Signaling Attenuator HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENE1 Activates FLOWERING LOCUS C Transcription via Chromatin Remodeling under Short-Term Cold Stress in Arabidopsis

Exposure to short-term cold stress delays flowering by activating the floral repressor FLOWERING LOCUS C (FLC) in Arabidopsis thaliana. The cold signaling attenuator HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENE1 (HOS1) negatively regulates cold responses. Notably, HOS1-deficient mutants exhibit early flowering, and FLC expression is suppressed in the mutants. However, it remains unknown how HOS1 regulates FLC expression. Here, we show that HOS1 induces FLC expression by antagonizing the actions of FVE and its interacting partner histone deacetylase 6 (HDA6) under short-term cold stress. HOS1 binds to FLC chromatin in an FVE-dependent manner, and FVE is essential for the HOS1-mediated activation of FLC transcription. HOS1 also interacts with HDA6 and inhibits the binding of HDA6 to FLC chromatin. Intermittent cold treatments induce FLC expression by activating HOS1, which attenuates the activity of HDA6 in silencing FLC chromatin, and the effects of intermittent cold are diminished in hos1 and fve mutants. These observations indicate that HOS1 acts as a chromatin remodeling factor for FLC regulation under short-term cold stress

Genome-Wide Negative Feedback Drives Transgenerational DNA Methylation Dynamics in Arabidopsis

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H3K27me3 demethylases alter HSP22 and HSP17.6C expression in response to recurring heat in Arabidopsis

Acclimation to high temperature increases tolerance of heat shock in plants. Here the authors show that JUMONJI H3K27me3 demethylases are needed for heat acclimation in Arabidopsis and act at loci encoding HEAT SHOCK PROTEINS to facilitate induction upon heat stress

Effects of disrupted heterochromatin in the <i>DDM1</i> wild type background examined at single base resolution.

<p>(A) Methylation level was compared for each transcription unit in CG, CHG, and CHH contexts. The format is as shown in <a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1005154#pgen.1005154.g002" target="_blank">Fig 2A</a>. A globally hypomethylated epiRIL (epiRIL98: plant #3 in Fig <a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1005154#pgen.1005154.g007" target="_blank">7A</a> and <a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1005154#pgen.1005154.g007" target="_blank">7B</a> and plant #2 in Fig <a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1005154#pgen.1005154.g007" target="_blank">7E</a> and <a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1005154#pgen.1005154.g007" target="_blank">7F</a>) and two epiRILs with lower level of hypomethylation (epiRIL260 and epiRIL480) are shown. Global hypomethylation indexes of epiRIL98, epiRIL260, and epiRIL480 are 0.38, 0.04, and 0.09, respectively. “WT” data are from the parental wild-type Col plant used to generate the epiRILs. (B) CHG methylation levels in the genes that were not methylated in WT but methylated in epiRIL98 (methylation level < 0.1 in WT and ≥ 0.1 in epiRIL98: n = 232). For these transcription units, distributions of the methylation levels were compared among the parental WT, the parental 4G <i>ddm1</i> plant, and the epiRIL98. (C-D) Ectopic CHG methylation in epiRIL98 compared to wild type. Each gene was assigned to the inferred haplotypes in epiRIL98: WT-like (C) or <i>ddm1</i>-like (D). The ectopic methylation could be detected in genes of the WT-like haplotype. Examples of such genes are shown in <a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1005154#pgen.1005154.s027" target="_blank">S25 Fig</a>.</p