Linear organization of the Arabidopsis genome: lessons from chromatin motifs

by Joana Sequeira-Mendes, Ugo Bastolla and Crisanto Gutierrez

Chromatin is a greatly dynamic structure constituted by genomic DNA and a variety of proteins, among which are histones and a myriad of DNA binding factors.  This high order complex is directly involved in crucial cellular processes such as transcription, replication, endoreduplication, or chromosome segregation and orchestrates diverse patterns of cell differentiation and plasticity, in a fine tune regulation of the genome activity.

The basic unit of chromatin is the nucleosome, comprised of 147 bp of DNA wrapped around a histone octamer of H2A, H2B, H3, and H4. Each of these proteins can be covalently modified in several residues that, together with modifications in the DNA molecules and the action of small regulatory RNAs or chromatin remodeling complexes, can define distinct chromatin properties. Arabidopsis thaliana has been for long a model organism in the study of epigenetic marks, providing strong resources for far-reaching studies. Indeed, a recent report combining several epigenomic maps in Arabidopsis chromosome 4 described four main chromatin states, specifically active, repressed, silent, and intergenic domains (Roudier et al., 2011), frequently small and interspersed with each other.

 

In a study published in The Plant Cell, we present a detailed comprehensive analysis of the chromatin landscape in the Arabidopsis genome, based on the prevalent combinations of fifteen epigenetic modifications and nucleotide content (Sequeira-Mendes et al., 2014). We find nine predominant and robust chromatin types that sort the epigenome beyond the classical euchromatin and heterochromatin states.

Remarkably, we report unexpected combinations of active and repressive chromatin marks (H3K4me3 and H3K27me3). Sequential chromatin immunoprecipitation (Re-ChIP) experiments demonstrate the coincidence of these marks in the same chromatin fiber, thus defining bivalent chromatin states at the cellular level. Moreover, we describe two classes of heterochromatin that mainly differ in their nucleotide content.

 

One interesting output of this study is the detailed analysis of the linear relationships between neighbor chromatin states. Interestingly, it has been found that chromatin states are not located in the genome at random. Instead, each chromatin state exhibits a preference to occur next to only a subset of other states. Thus, classical heterochromatin never associates directly with the most active states and communicates with the Polycomb repressed chromatin through the AT-rich heterochromatin. These states are commonly in contact with a chromatin state, enriched in H3K27me3, which appears to facilitate the transition to intergenic chromatin states and regions of active chromatin. This linear organization of the Arabidopsis genome leads, in addition to the typical heterochromatin and Polycomb chromatin, to the occurrence of a relatively small number of motifs in euchromatin that define chromatin states characteristic of genic regions and of regions upstream of TSS, most likely acting as promoter and other regulatory domains.

 

Finally, our study provides an interesting resource that will be made available to the community in CoGe https://genomevolution.org/CoGe/GenomeView.pl?z=6&x=20000&gid=16911&chr=... and sets the ground for new lines of research, such as the role of bivalent chromatin in plant development or the function of polycomb marks in genome topography and functions.

 

References

 

Roudier, F. et al. Integrative epigenomic mapping defines four main chromatin states in Arabidopsis. The EMBO Journal 1–11 (2011). doi:10.1038/emboj.2011.103

 

Sequeira-Mendes, J. et al. The Functional Topography of the Arabidopsis Genome Is Organized in a Reduced Number of Linear Motifs of Chromatin States. THE PLANT CELL ONLINE (2014). doi:10.1105/tpc.114.124578

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