Trends in Genetics
ReviewChromatin indexing in Arabidopsis: an epigenomic tale of tails and more
Section snippets
Chromatin and the epigenome
Long considered mainly a DNA packaging device, chromatin is now viewed as a highly dynamic structure that affects all DNA transactions within the nucleus, namely transcription, replication, repair, recombination and transposition, as well as chromosome segregation. Thus, mutations that influence the composition of chromatin along the genome – the so-called epigenome – can induce strong phenotypic alterations or impaired viability, mainly caused by increased genome instability and/or
Epigenomic mapping in Arabidopsis
Over 20 chromatin marks and proteins have been analyzed in Arabidopsis at the cytological level by immunostaining or tagging 4, 5, 6, 7, 8, 10 of which have also been characterized at higher resolution through epigenomic mapping approaches (Box 2). Most epigenomic maps have been obtained using chromatin immunoprecipitation or methyl-cytosine immunoprecipitation, followed by hybridization to genomic tiling microarrays (ChIP-chip or MeDIP-chip, respectively) 9, 10, 11, 12, 13, 14, 15, 16. DNA
Heterochromatin and repeat elements
Despite its small size, the Arabidopsis genome contains many transposable elements and other repeats, most of which are clustered in pericentromeric or interstitial heterochromatin [27]. Consistent with immunostaining experiments, these heterochromatic regions were found by epigenomic mapping to be highly enriched in H3K9me2 and 5mC compared with euchromatin (Figure 1) 9, 10, 13, 14, 15, 17, 28. Thanks to their high resolution, these maps also revealed that the enrichment in H3K9me2 and 5mC was
Euchromatin and genes
The 125 Mb long Arabidopsis genome contains ∼28 000 genes, or 1 gene per ∼4 kb on average [27], a figure close to that of the highly compact genome of yeasts (1 gene/∼2 kb; [54]). Furthermore, most Arabidopsis genes are localized within euchromatin, which encompasses ∼100 Mb. Therefore, epigenomic mapping of this compartment equates with determining the distribution of chromatin marks over genes and their immediate surroundings, with few interspersed repeat elements. The emerging picture is one
Concluding remarks
The first epigenomic maps produced in Arabidopsis, mostly from whole seedlings or entire organs, have revealed an organization of chromosomes into small and well-demarcated chromatin domains that often coincide with single genes or individual repeat elements, irrespective of their location within euchromatin or heterochromatin. Significantly, a similar organization seems to prevail in plant species with more abundant repeat elements such as rice and maize, although the localization of DNA
Acknowledgments
We apologize to authors whose work could not be cited owing to space constraints. We thank Edith Heard for critical reading of this manuscript. F.K.T. was supported by a PhD studentship from the Brazilian government (Coordenação de Aperfeiçoamento de Pessoal de Nivel Superior – CAPES). V.C. is a member of the European Union Network of Excellence “The Epigenome”. Work in the V.C. group is supported by grants from the French Agence Nationale de la Recherche (ANR Genoplante projects TAG and
References (81)
Chromatin modifications and their function
Cell
(2007)Organismal differences in post-translational modifications in histones H3 and H4
J. Biol. Chem.
(2007)Chromosomal histone modification patterns – from conservation to diversity
Trends Plant Sci.
(2006)Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis
Cell
(2006)Highly integrated single-base resolution maps of the epigenome in Arabidopsis
Cell
(2008)Specificity of ARGONAUTE7–miR390 interaction and dual functionality in TAS3 trans-acting siRNA formation
Cell
(2008)- et al.
Chromatin state maps: new technologies, new insights
Curr. Opin. Genet. Dev.
(2008) Position–effect variegation and the genetic dissection of chromatin regulation in Drosophila
Semin Cell Dev. Biol.
(2003)- et al.
Oxymoron no more: the expanding world of heterochromatic genes
Trends Genet
(2006) - et al.
Role of the Arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing
Curr. Biol.
(2002)
The SRA methyl–cytosine-binding domain links DNA and histone methylation
Curr. Biol.
Interplay between two epigenetic marks. DNA methylation and histone H3 lysine 9 methylation
Curr. Biol.
Yeasts illustrate the molecular mechanisms of eukaryotic genome evolution
Trends Genet
Diversity of polycomb group complexes in plants: same rules, different players?
Trends Genet.
Polycomb silencing of KNOX genes confines shoot stem cell niches in Arabidopsis
Curr. Biol.
A bivalent chromatin structure marks key developmental genes in embryonic stem cells
Cell
Epigenetic reprogramming and small RNA silencing of transposable elements in pollen
Cell
RNA interference guides histone modification during the S phase of chromosomal replication
Curr. Biol.
Progress and challenges in profiling the dynamics of chromatin and transcription factor binding with DNA microarrays
Curr. Opin. Genet Dev.
Genomic patterns of DNA methylation: targets and function of an epigenetic mark
Curr. Opin. Cell Biol.
The complex language of chromatin regulation during transcription
Nature
Histone modifications and dynamic regulation of genome accessibility in plants
Curr. Opin. Plant Biol.
Histone H2A.Z and DNA methylation are mutually antagonistic chromatin marks
Nature
The Arabidopsis LHP1 protein is a component of euchromatin
Planta
ATXR5 and ATXR6 are H3K27 monomethyltransferases required for chromatin structure and gene silencing
Nat Struct Mol Biol
Genome-wide association of histone H3 lysine nine methylation with CHG DNA methylation in Arabidopsis thaliana
PLoS ONE
Role of transposable elements in heterochromatin and epigenetic control
Nature
Genic and global functions for Paf1C in chromatin modification and gene expression in Arabidopsis
PLoS Genet
Whole-genome analysis of histone H3 lysine 27 trimethylation in Arabidopsis
PLoS Biol
Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription
Nat. Genet.
Arabidopsis TFL2/LHP1 specifically associates with genes marked by trimethylation of histone H3 lysine 27
PLoS Genet.
Epigenomic consequences of immortalized plant cell suspension culture
PLoS Biol.
Epigenetic natural variation in Arabidopsis thaliana
PLoS Biol.
Genome-wide, high-resolution DNA methylation profiling using bisulfite-mediated cytosine conversion
Genome Res.
Shotgun bisulfite sequencing of the Arabidopsis genome reveals DNA methylation patterning
Nature
The evolution of grass genome organization and function
Symp Soc Exp Biol
The mechanism selecting the guide strand from small RNA duplexes is different among argonaute proteins
Plant Cell Physiol.
Identification of in vivo DNA targets of chromatin proteins using tethered dam methyltransferase
Nat. Biotechnol.
The Arabidopsis LHP1 protein colocalizes with histone H3 Lys27 trimethylation
Nat. Struct. Mol. Biol.
Cited by (90)
Manipulating epigenetic diversity in crop plants: Techniques, challenges and opportunities
2024, Biochimica et Biophysica Acta - General SubjectsGenic C-Methylation in Soybean Is Associated with Gene Paralogs Relocated to Transposable Element-Rich Pericentromeres
2018, Molecular PlantCitation Excerpt :In animals, cytosine methylation occurs predominantly at symmetric CG sites (Chen et al., 2011; Lister et al., 2013), while in plants DNA methylation is found in three different sequence contexts, CG, CHG, and CHH (H = A, T, or C). Generation of high-resolution methylation maps in plants revealed that both genes and TEs can be methylated, but in different ways (Roudier et al., 2009; Niederhuth et al., 2016). Unlike gene body methylation that occurs in the CG context and is generally associated with moderately expressed genes (Tran et al., 2005; Coleman-Derr and Zilberman, 2012; Seymour et al., 2014; Kim et al., 2015), the concomitant methylation of TEs in all three contexts (CG, CHG and CHH) results in transcriptional silencing.
Systematic Profiling of Histone Readers in Arabidopsis thaliana
2018, Cell ReportsCitation Excerpt :We hypothesize that the combinatorial readout of Kac is highly conserved between Arabidopsis thaliana and human. Over 20 histone marks have been identified in Arabidopsis thaliana, and the major modification types are conserved among species (Roudier et al., 2009). Recent advances in lab-on-chip profiling of epigenetic interactions make high-throughput analysis of histone “mark-reader” pairs possible (Bae et al., 2017; Zhao et al., 2017b).
Innate immune memory in plants
2016, Seminars in ImmunologyHistone variants and modifications during abiotic stress response
2022, Frontiers in Plant ScienceCRISPR–Cas-mediated transcriptional control and epi-mutagenesis
2022, Plant Physiology
- *
These authors contributed equally to this work.