H3K9 demethylation-mediated transcriptional activation is required for male meiosis in Arabidopsis thaliana
Ontology highlight
ABSTRACT:
ORGANISM(S): Arabidopsis thaliana
PROVIDER: GSE186532 | GEO | 2022/12/31
REPOSITORIES: GEO
Similar Datasets
Project description:Heterochromatin constitutes a fundamental aspect of genomes that is crucial for maintaining genome stability. In flowering plants, maintenance of heterochromatin relies on a positive feedback loop involving the histone 3 lysine nine methyltransferase (H3K9), KRYPTONITE (KYP), and the DNA methyltransferase, CHROMOMETHYLASE3 (CMT3). An H3K9 demethylase, INCREASED IN BONSAI METHYLATION 1 (IBM1), has evolved to modulate the activity of KYP-CMT3 within transcribed genes. The absence of IBM1 activity results in aberrant methylation of gene bodies, which is deleterious. This study demonstrates extensive genetic and gene expression variations in KYP, CMT3, and IBM1 within and between flowering plant species. IBM1 activity in Arabidopsis thaliana is uniquely regulated by the abundance of H3K9me2 in a repetitive sequence within an intron preceding the histone demethylase domain. This mechanism enables IBM1 to monitor global levels of H3K9me2. We discovered that the methylated intron is prevalent across flowering plants, however, its underlying sequence exhibits dynamic evolution. Its absence in species lacking gene body DNA methylation suggests its primary role in sensing H3K9me2 and preventing its integration into these constitutively expressed genes. Furthermore, our investigation uncovered Arabidopsis thaliana accessions resembling weak ibm1 mutants, several Brassicaceae species with reduced IBM1 expression, and a potential IBM1 deletion. Evolution towards reduced IBM1 activity in some flowering plants could explain the frequent natural occurrence of diminished or lost CMT3 activity, as cmt3 mutants in A. thaliana mitigate the deleterious effects of IBM1.
2024-05-10 | GSE252913 | GEO
Project description:Methylation of histone H3 at lysine 9 (H3K9) is a hallmark of heterochromatin that plays crucial roles in chromatin-dependent gene silencing and maintenance of genome stability by repressing repetitive DNA elements and recruiting downstream factors essential for faithful chromosome segregation. Fundamental principles of these processes have been elucidated in the fission yeast Schizosaccharomyces pombe (S. pombe), in which Clr4, the homologue of mammalian SUV39H, is the sole H3K9 methyltransferase. Although H3K9 methylation has been intensely studied in mitotic cells, occurrence and regulation during sexual differentiation remain largely unknown. Whether distinct H3 methylation states are relevant for gametogenesis is also not known. Here, using diploid S. pombe cells, we map H3K9 methylation genome-wide during the meiotic program and show that constitutive heterochromatin temporarily loses H3K9me2 and becomes H3K9me3 when cells exit mitosis and commit to the meiotic life cycle. Cells lacking the ability to tri-methylate H3K9 exhibit severe meiotic chromosome segregation defects, which does not occur in mitotic cells. Artificially increasing the affinity of the fission yeast heterochromatin protein 1 (HP1) homologue Swi6 towards H3K9me2 rescues chromosome segregation in the absence of H3K9me3. Thus, the H3K9me2 to H3K9me3 switch during early meiosis serves to retain Swi6 at centromeres, which is necessary for cohesin recruitment and kinetochore assembly. Finally, we show that the H3K9 methylation switch is regulated by differential phosphorylation of Clr4 by the cyclin-dependent kinase (CDK) Cdk1. Our results reveal how a highly conserved master regulator of the cell cycle regulates the specificity of the H3K9 methyltransferase and thereby controls the ratio of H3K9me2 to H3K9me3 to prevent unwanted gene silencing and to ensure faithful meiotic chromosome segregation. High degree of conservation of the proteins involved in our study and CDK-dependent phosphorylation of the mammalian SUV39H1 homologue suggest broad conservation of the mechanisms described here.
2022-10-17 | GSE182250 | GEO
Project description:We report the H3K9me2 distribution profile with ChIP sequencing of postnatal male germ cells. Histone modification levels are dynamically controlled during mammalian spermatogenesis. We found that H3K9 demethylases, Jmjd1a and Jmjd1b catalyze H3K9 demethylation in prospermatogonia. Combined loss of Jmjd1 enzymes disturbed prospermatogonia to spermatogonia transition in mice. To examine a role of Jmjd1 in prospermatogonia to spermatogonia transition, we performed RNA-seq and ChIP-seq analyses using postnatal germ cells at P3 and P7.
2020-06-08 | GSE148054 | GEO
Project description:In order to gain a more global view of the activity of histone demethylases we report here studies of the two fission yeast SWIRM and polyamine oxidase domain homologues of mammalian LSD1. Consistent with previous work (Nicolas et al., 2006) we find that the two S. pombe proteins, which we name Swm1 and Swm2 (after SWIRM1 and SWIRM2), associate together in a complex. We find that this complex specifically demethylates lysine 9 in histone H3 (H3K9) to up- and down-regulate expression of different genes. Using chromatin-immunoprecipitation, to isolate fragments of chromatin containing either H3K4me2 or H3K9me2, and DNA microarray analysis (ChIP-chip), we have studied genome-wide changes in patterns of histone methylation, and their correlation with gene expression, upon deletion of the swm1+ gene. Using hyper-geometric probability comparisons we uncover links between lysine specific demethylases, the histone deacetylase Clr6, and the chromatin remodeller Hrp1. Keywords: chip on chip Genome-wide studies of histone demethylation catalysed by the fission yeast SWIRM and polyamine oxidase domain homologues of mammalian LSD1
2010-05-27 | E-GEOD-6224 | biostudies-arrayexpress
Project description:In diverse eukaryotes, constitutively silent sequences, such as transposons and repeats, are marked by methylation at histone H3 lysine 9 (H3K9me). Despites the conservation and importance in the genome integrity, mechanisms to exclude H3K9m from active genes remained largely unexplored. Here we show in Arabidopsis that the exclusion depends on a histone demethylase gene, IBM1 (increase in BONSAI methylation); loss-of-function ibm1 mutation caused ectopic H3K9me in thousands of genes, which accompanies genic DNA methylation at non-CG sites. The ibm1-induced genic H3K9me depended on both histone methylase KYP/SUVH4 and DNA methylase CMT3, suggesting interdependence of two epigenetic marks – H3K9me and non-CG methylation. Notably, IBM1 enhanced loss of H3K9m in transcriptionally de-repressed sequences. Furthermore, disruption of transcription in genes induced ectopic non-CG methylation, mimicking the loss of IBM1 function. We propose that active chromatin is stabilized by the autocatalytic loop of transcription and H3K9 demethylation. This process counteracts accumulation of silent epigenetic marks, H3K9me and non-CG methylation, which is also autocatalytic. Leaves of 4-week-old plants were fixed as described previously (Saze et al, 2008). Chromatin immunoprecipitation (ChIP) was performed as described previously (Kimura et al, 2008), using antibody against H3K9me2 (CMA307, Kimura et al, 2008, PMID: 18227620). Non-immunoprecipitated DNA (input DNA) and ChIP samples were amplified, labeled, and hybridized to microarray according to the manufacturer’s instruction (Protocols for Chromatin Immunoprecipitation and Amplification, NimbleGen). Input DNA and ChIP DNA were differentially labeled with Cy3 and Cy5, respectively, and competitively hybridized to a microarray chip. We used NimbleGen 2.1M HD2 array covering entire genome of A. thaliana.
2010-09-21 | E-GEOD-22953 | biostudies-arrayexpress
Project description:Histone methylation patterns regulate gene expression and are highly dynamic during development. The erasure of histone methylation is carried out by histone demethylase enzymes. We had previously shown that vitamin C enhances the activity of Tet enzymes in embryonic stem (ES) cells, leading to DNA demethylation and activation of germline genes. We report here that vitamin C induces a remarkably specific demethylation of histone H3 lysine 9 dimethylation (H3K9me2) in ES cells. Vitamin C treatment reduces global levels of H3K9me2, but not other histone methylation marks analyzed, as measured by Western blot, immunofluorescence and mass spectrometry. Vitamin C leads to widespread loss of H3K9me2 at large chromosomal domains as well as gene promoters and repeat elements. Vitamin C-induced loss of H3K9me2 occurs rapidly within 24 hours and is reversible. Importantly, we found that the histone demethylases Kdm3a and Kdm3b are required for vitamin C-induced demethylation of H3K9me2. Moreover, we show that vitamin C-induced Kdm3a/b-mediated H3K9me2 demethylation and Tet-mediated DNA demethylation are independent processes. Lastly, we document Kdm3a/b are partially required for the up-regulation of germline genes by vitamin C. These results reveal a specific role for vitamin C in histone demethylation in ES cells, and document that DNA methylation and H3K9me2 cooperate to silence germline genes in pluripotent cells.
2017-06-30 | GSE84009 | GEO
Project description:The arginine or lysine methylation status of histones dynamically changes during many essential cellular processes, particularly during embryonic and hematopoietic stem cell development. The enzymes demethylate methyllysine residues have been well defined, but the enzymes demethylate the methylarginine residues during different cellular processes are unknown. In current study, we demonstrate that JMJD1B is a lysine demethylase for H3K9me2 and an arginine demethylase for H4R3me2s. To reveal the biological significance of JMJD1B as an arginine demethylase, we isolate hematopoietic stem/progenitor cells (HSPC) from wild-type and JMJD1B knockout (JKO) bone marrow. We then conduct ChIP-seq on H4R3me2s and H3K9me2 histone markers and perform RNA-seq to determine the global gene expression profiles. We have observed global demethylation of H4R3me2s at the gene body but not the intergenic regions in hematopoietic stem/progenitor cells. H4R3me2s demethylation at the gene body region is directly correlated with gene expression in these cells. Furthermore, knockout of JMJD1B causes defects in removing the H4R3me2s epigenetic marker, leading to down-regulation of genes important for blood cells differentiation and development. Altogether, our current study demonstrates that arginine demethylases exist in cellular systems and that JMJD1B demethylates H4R3me2s for proper epigenetic programming during development.
2018-03-14 | GSE94966 | GEO
Project description:Ray2013 - Meiotic initiation in S. cerevisiae
A mathematical representation of early meiotic events, particularly feedback mechanisms at the system level and phosphorylation of signalling molecules for regulating protein activities, is described here
This model is described in the article:
Dynamic modeling of yeast meiotic initiation.
Ray D, Su Y, Ye P.
BMC Syst Biol. 2013 May 1;7:37
Abstract:
BACKGROUND:
Meiosis is the sexual reproduction process common to eukaryotes. The diploid yeast Saccharomyces cerevisiae undergoes meiosis in sporulation medium to form four haploid spores. Initiation of the process is tightly controlled by intricate networks of positive and negative feedback loops. Intriguingly, expression of early meiotic proteins occurs within a narrow time window. Further, sporulation efficiency is strikingly different for yeast strains with distinct mutations or genetic backgrounds. To investigate signal transduction pathways that regulate transient protein expression and sporulation efficiency, we develop a mathematical model using ordinary differential equations. The model describes early meiotic events, particularly feedback mechanisms at the system level and phosphorylation of signaling molecules for regulating protein activities.
RESULTS:
The mathematical model is capable of simulating the orderly and transient dynamics of meiotic proteins including Ime1, the master regulator of meiotic initiation, and Ime2, a kinase encoded by an early gene. The model is validated by quantitative sporulation phenotypes of single-gene knockouts. Thus, we can use the model to make novel predictions on the cooperation between proteins in the signaling pathway. Virtual perturbations on feedback loops suggest that both positive and negative feedback loops are required to terminate expression of early meiotic proteins. Bifurcation analyses on feedback loops indicate that multiple feedback loops are coordinated to modulate sporulation efficiency. In particular, positive auto-regulation of Ime2 produces a bistable system with a normal meiotic state and a more efficient meiotic state.
CONCLUSIONS:
By systematically scanning through feedback loops in the mathematical model, we demonstrate that, in yeast, the decisions to terminate protein expression and to sporulate at different efficiencies stem from feedback signals toward the master regulator Ime1 and the early meiotic protein Ime2. We argue that the architecture of meiotic initiation pathway generates a robust mechanism that assures a rapid and complete transition into meiosis. This type of systems-level regulation is a commonly used mechanism controlling developmental programs in yeast and other organisms. Our mathematical model uncovers key regulations that can be manipulated to enhance sporulation efficiency, an important first step in the development of new strategies for producing gametes with high quality and quantity.
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2024-09-02 | BIOMD0000000626 | BioModels
Project description:In diverse eukaryotes, constitutively silent sequences, such as transposons and repeats, are marked by methylation at histone H3 lysine 9 (H3K9me). Despites the conservation and importance in the genome integrity, mechanisms to exclude H3K9m from active genes remained largely unexplored. Here we show in Arabidopsis that the exclusion depends on a histone demethylase gene, IBM1 (increase in BONSAI methylation); loss-of-function ibm1 mutation caused ectopic H3K9me in thousands of genes, which accompanies genic DNA methylation at non-CG sites. The ibm1-induced genic H3K9me depended on both histone methylase KYP/SUVH4 and DNA methylase CMT3, suggesting interdependence of two epigenetic marks – H3K9me and non-CG methylation. Notably, IBM1 enhanced loss of H3K9m in transcriptionally de-repressed sequences. Furthermore, disruption of transcription in genes induced ectopic non-CG methylation, mimicking the loss of IBM1 function. We propose that active chromatin is stabilized by the autocatalytic loop of transcription and H3K9 demethylation. This process counteracts accumulation of silent epigenetic marks, H3K9me and non-CG methylation, which is also autocatalytic.
2010-09-21 | GSE22953 | GEO
Project description:To explore whether iron is required for BCR-induced H3K9 demethylation during B cell activation, we performed ChIP-seq to check the H3K9me2 modification in control (iron-normal) and iron-deficient B cells
2019-05-24 | GSE131716 | GEO