Epigenomics in an extraterrestrial environment: organ-specific alteration of DNA methylation and gene expression elicited by spaceflight in Arabidopsis thaliana

Abstract Motivation The COP9 signalosome is a highly conserved multi-protein complex consisting of eight subunits, which influences key developmental pathways through its regulation of protein stability and transcription. In Arabidopsis thaliana, mutations in the COP9 signalosome exhibit a number of diverse pleiotropic phenotypes. Total or partial loss of COP9 signalosome function in Arabidopsis leads to misregulation of a number of genes involved in DNA methylation, suggesting that part of the pleiotropic phenotype is due to global effects on DNA methylation. Results We determined and analyzed the methylomes and transcriptomes of both partial- and total-loss-of-function Arabidopsis mutants of the COP9 signalosome. Our results support the hypothesis that the COP9 signalosome has a global genome-wide effect on methylation and that this effect is at least partially encoded in the DNA. Our analyses suggest that COP9 signalosome-dependent methylation is related to gene expression regulation in various ways. Differentially methylated regions tend to be closer in the 3D conformation of the genome to differentially expressed genes. These results suggest that the COP9 signalosome has a more comprehensive effect on gene expression than thought before, and this is partially related to regulation of methylation. The high level of COP9 signalosome conservation among eukaryotes may also suggest that COP9 signalosome regulates methylation not only in plants but also in other eukaryotes, including humans. Supplementary information Supplementary data are available at Bioinformatics online.

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Gene chip analysis of Arabidopsis thaliana genomic DNA methylation and gene expression in response to carbendazim

Biotechnology Letters ◽

10.1007/s10529-015-1789-1 ◽

2015 ◽

Vol 37 (6) ◽

pp. 1297-1307 ◽

Cited By ~ 3

Author(s):

Zhongai Li ◽

Zicheng Wang ◽

Suoping Li

Keyword(s):

Gene Expression ◽

Dna Methylation ◽

Arabidopsis Thaliana ◽

Genomic Dna ◽

Gene Chip ◽

Chip Analysis

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The plant mobile domain proteins MAIN and MAIL1 interact with the phosphatase PP7L to regulate gene expression and silence transposable elements in Arabidopsis thaliana

10.1101/710905 ◽

2019 ◽

Author(s):

Melody Nicolau ◽

Nathalie Picault ◽

Julie Descombin ◽

Yasaman Jami-Alahmadi ◽

Suhua Feng ◽

...

Keyword(s):

Gene Expression ◽

Dna Methylation ◽

Arabidopsis Thaliana ◽

Transposable Elements ◽

Genome Stability ◽

Phylogenetic Analyses ◽

Dna Repeats ◽

Functional Protein ◽

Developmental Processes ◽

Phosphoprotein Phosphatase

ABSTRACTTransposable elements (TEs) are DNA repeats that must remain silenced to ensure cell integrity. Several epigenetic pathways including DNA methylation and histone modifications are involved in the silencing of TEs, and in the regulation of gene expression. In Arabidopsis thaliana, the TE-derived plant mobile domain (PMD) proteins have been involved in TE silencing, genome stability, and control of developmental processes. Using a forward genetic screen, we found that the PMD protein MAINTENANCE OF MERISTEMS (MAIN) acts synergistically and redundantly with DNA methylation to silence TEs. We found that MAIN and its close homolog MAIN-LIKE 1 (MAIL1) interact together, as well as with the phosphoprotein phosphatase (PPP) PP7-like (PP7L). Remarkably, main, mail1, pp7l single and mail1 pp7l double mutants display similar developmental phenotypes, and share common subsets of upregulated TEs and misregulated genes. Finally, phylogenetic analyses of PMD and PP7-type PPP domains among the Eudicot lineage suggest neo-association processes between the two protein domains to potentially generate new protein function. We propose that, through this interaction, the PMD and PPP domains may constitute a functional protein module required for the proper expression of a common set of genes, and for silencing of TEs.AUTHOR SUMMARYThe plant mobile domain (PMD) is a protein domain of unknown function that is widely spread in the angiosperm plants. Although most PMDs are associated with repeated DNA sequences called transposable elements (TEs), plants have domesticated the PMD to produce genic versions that play important roles within the cell. In Arabidopsis thaliana, MAINTENANCE OF MERISTEMS (MAIN) and MAIN-LIKE 1 (MAIL1) are genic PMDs that are involved in genome stability, developmental processes, and silencing of TEs. The mechanisms involving MAIN and MAIL1 in these cellular processes remain elusive. Here, we show that MAIN, MAIL1 and the phosphoprotein phosphatase (PPP) named PP7-like (PP7L) interact to form a protein complex that is required for the proper expression of genes, and the silencing of TEs. Phylogenetic analyses revealed that PMD and PP7-type PPP domains are evolutionary connected, and several plant species express proteins carrying both PMD and PPP domains. We propose that interaction of PMD and PPP domains would create a functional protein module involved in mechanisms regulating gene expression and repressing TEs.

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Maternal folic acid supplementation modulates DNA methylation and gene expression in the rat offspring in a gestation period-dependent and organ-specific manner

The Journal of Nutritional Biochemistry ◽

10.1016/j.jnutbio.2016.03.018 ◽

2016 ◽

Vol 33 ◽

pp. 103-110 ◽

Cited By ~ 31

Author(s):

Anna Ly ◽

Lisa Ishiguro ◽

Denise Kim ◽

David Im ◽

Sung-Eun Kim ◽

...

Keyword(s):

Gene Expression ◽

Dna Methylation ◽

Folic Acid ◽

Folic Acid Supplementation ◽

Gestation Period ◽

Acid Supplementation ◽

Rat Offspring ◽

Specific Manner ◽

Organ Specific

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A DNA methylation reader complex that enhances gene transcription

Science ◽

10.1126/science.aar7854 ◽

2018 ◽

Vol 362 (6419) ◽

pp. 1182-1186 ◽

Cited By ~ 53

Author(s):

C. Jake Harris ◽

Marion Scheibe ◽

Somsakul Pop Wongpalee ◽

Wanlu Liu ◽

Evan M. Cornett ◽

...

Keyword(s):

Gene Expression ◽

Dna Methylation ◽

Arabidopsis Thaliana ◽

Gene Transcription ◽

Methylated Dna ◽

Transposon Insertion ◽

Activate Gene

DNA methylation generally functions as a repressive transcriptional signal, but it is also known to activate gene expression. In either case, the downstream factors remain largely unknown. By using comparative interactomics, we isolated proteins in Arabidopsis thaliana that associate with methylated DNA. Two SU(VAR)3-9 homologs, the transcriptional antisilencing factor SUVH1, and SUVH3, were among the methyl reader candidates. SUVH1 and SUVH3 bound methylated DNA in vitro, were associated with euchromatic methylation in vivo, and formed a complex with two DNAJ domain-containing homologs, DNAJ1 and DNAJ2. Ectopic recruitment of DNAJ1 enhanced gene transcription in plants, yeast, and mammals. Thus, the SUVH proteins bind to methylated DNA and recruit the DNAJ proteins to enhance proximal gene expression, thereby counteracting the repressive effects of transposon insertion near genes.

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Position-dependent effects of cytosine methylation on FWA expression in Arabidopsis thaliana

10.1101/774281 ◽

2019 ◽

Cited By ~ 2

Author(s):

Thanvi Srikant ◽

Anjar Wibowo ◽

Rebecca Schwab ◽

Detlef Weigel

Keyword(s):

Gene Expression ◽

Dna Methylation ◽

Arabidopsis Thaliana ◽

Transcription Start Site ◽

Cytosine Methylation ◽

Epigenetic Modification ◽

Start Site ◽

Differentially Methylated Regions ◽

Transcription Start ◽

Repeat Elements

ABSTRACTGene expression can be modulated by epigenetic modifications to chromatin, and variants of the same locus distinguished by fixed, heritable epigenetic differences are known as epialleles. DNA methylation at cytosines is a prominent epigenetic modification, particularly in plant genomes, that can modulate gene expression. There are several examples where epialleles are associated with differentially methylated regions that affect the expression of overlapping or close-by genes. However, there are also many differentially methylated regions that have not been assigned a biological function despite their proximity to genes. We investigated the positional importance of DNA methylation at the FWA (FLOWERING WAGENINGEN) locus in Arabidopsis thaliana, a paradigm for stable epialleles. We show that cytosine methylation can be established not only over the well-characterized SINE-derived repeat elements that overlap with the transcription start site, but also in more distal promoter regions. FWA silencing, however, is most effective when methylation covers the transcription start site.

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In plants distal regulatory sequences overlap with unmethylated rather than low-methylated regions, in contrast to mammals

10.1101/2020.03.24.005678 ◽

2020 ◽

Author(s):

Rurika Oka ◽

Mattijs Bliek ◽

Huub C.J. Hoefsloot ◽

Maike Stam

Keyword(s):

Gene Expression ◽

Dna Methylation ◽

Arabidopsis Thaliana ◽

Transcriptional Repression ◽

Genome Stability ◽

Regulation Of Gene Expression ◽

Regulatory Sequences ◽

Regulatory Regions ◽

Plant Genomes ◽

Underlying Mechanisms

AbstractBackgroundDNA methylation is an important factor in the regulation of gene expression and genome stability. High DNA methylation levels are associated with transcriptional repression. In mammalian systems, unmethylated, low methylated and fully methylated regions (UMRs, LMRs, and FMRs, respectively) can be distinguished. UMRs are associated with proximal regulatory regions, while LMRs are associated with distal regulatory regions. Although DNA methylation is mainly limited to the CG context in mammals, while it occurs in CG, CHG and CHH contexts in plants, UMRs and LMRs were expected to occupy similar genomic sequences in both mammals and plants.ResultsThis study investigated major model and crop plants such as Arabidopsis thaliana, tomato (Solanum lycopersicum), rice (Oryza sativa) and maize (Zea mays), and shows that plant genomes can also be subdivided in UMRs, LMRs and FMRs, but that LMRs are mainly present in the CHG context rather than the CG context. Strikingly, the identified CHG LMRs were enriched in transposable elements rather than regulatory regions. Maize candidate regulatory regions overlapped with UMRs. LMRs were enriched for heterochromatic histone modifications and depleted for DNase accessibility and H3K9 acetylation. CHG LMRs form a distinct, abundant cluster of loci, indicating they have a different role than FMRs.ConclusionsBoth mammalian and plant genomes can be segmented in three distinct classes of loci, UMRs, LMRs and FMRs, indicating similar underlying mechanisms. Unlike in mammals, distal regulatory sequences in plants appear to overlap with UMRs instead of LMRs. Our data indicate that LMRs in plants have a different function than those in mammals.

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On the Origin and Evolutionary Consequences of Gene Body DNA Methylation

10.1101/045542 ◽

2016 ◽

Cited By ~ 3

Author(s):

Adam J. Bewick ◽

Lexiang Ji ◽

Chad E. Niederhuth ◽

Eva-Maria Willing ◽

Brigitte T. Hofmeister ◽

...

Keyword(s):

Gene Expression ◽

Dna Methylation ◽

Arabidopsis Thaliana ◽

Dna Methyltransferases ◽

Gene Body ◽

Evolutionary Time ◽

Gene Body Methylation ◽

Eutrema Salsugineum ◽

And Function ◽

Evolutionary Consequences

AbstractIn plants, CG DNA methylation is prevalent in the transcribed regions of many constitutively expressed genes (“gene body methylation; gbM”), but the origin and function of gbM remain unknown. Here we report the discovery that Eutrema salsugineum has lost gbM from its genome, the first known instance for an angiosperm. Of all known DNA methyltransferases, only CHROMOMETHYLASE 3 (CMT3) is missing from E. salsugineum. Identification of an additional angiosperm, Conringia planisiliqua, which independently lost CMT3 and gbM supports that CMT3 is required for the establishment of gbM. Detailed analyses of gene expression, the histone variant H2A.Z and various histone modifications in E. salsugineum and in Arabidopsis thaliana epiRILs found no evidence in support of any role for gbM in regulating transcription or affecting the composition and modifications of chromatin over evolutionary time scales.

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Promoter and Terminator Optimization for DNA Methylation Targeting in Arabidopsis

Epigenomes ◽

10.3390/epigenomes4020009 ◽

2020 ◽

Vol 4 (2) ◽

pp. 9

Author(s):

Jason Gardiner ◽

Jenny M. Zhao ◽

Kendall Chaffin ◽

Steven E. Jacobsen

Keyword(s):

Gene Expression ◽

Dna Methylation ◽

Arabidopsis Thaliana ◽

Gene Regulation ◽

Nicotiana Tabacum ◽

New Technologies ◽

Catalytic Domain ◽

Epigenetic Mark ◽

Phenotypic Changes ◽

Promising Tool

DNA methylation is an important epigenetic mark involved in gene regulation and silencing of transposable elements. The presence or absence of DNA methylation at specific sites can influence nearby gene expression and cause phenotypic changes that remain stable over generations. Recently, development of new technologies has enabled the targeted addition or removal of DNA methylation at specific sites of the genome. Of these new technologies, the targeting of the catalytic domain of Nicotiana tabacum DOMAINS REARRANGED METHYLTRANSFERASE 2 (ntDRM2cd) offers a promising tool for the addition of DNA methylation as it can directly methylate DNA. However, the methylation targeting efficiency of constructs using ntDRM2cd thus far has been relatively low. Previous studies have shown that the use of different promoters or terminators can greatly improve genome-editing efficiencies. In this study, we systematically survey a variety of promoter and terminator combinations to identify optimal combinations to use when targeting the addition of DNA methylation in Arabidopsis thaliana.

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