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Arabidopsis replacement histone variant H3.3 occupies promoters of regulated genes

Huan Shu1, Miyuki Nakamura2, Alexey Siretskiy2, Lorenzo Borghi1, Izabel Moraes2, Thomas Wildhaber1, Wilhelm Gruissem1 and Lars Hennig123*

Author Affiliations

1 Department of Biology and Zurich-Basel Plant Science Center, ETH Zurich, CH-8092 Zurich, Switzerland

2 Department of Plant Biology, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center for Plant Biology, SE-75007 Uppsala, Sweden

3 Science for Life Laboratory, SE-75007 Uppsala, Sweden

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Genome Biology 2014, 15:R62  doi:10.1186/gb-2014-15-4-r62

Published: 7 April 2014

Abstract

Background

Histone variants establish structural and functional diversity of chromatin by affecting nucleosome stability and histone-protein interactions. H3.3 is an H3 histone variant that is incorporated into chromatin outside of S-phase in various eukaryotes. In animals, H3.3 is associated with active transcription and possibly maintenance of transcriptional memory. Plant H3 variants, which evolved independently of their animal counterparts, are much less well understood.

Results

We profile the H3.3 distribution in Arabidopsis at mono-nucleosomal resolution using native chromatin immunoprecipitation. This results in the precise mapping of H3.3-containing nucleosomes, which are not only enriched in gene bodies as previously reported, but also at a subset of promoter regions and downstream of the 3′ ends of active genes. While H3.3 presence within transcribed regions is strongly associated with transcriptional activity, H3.3 at promoters is often independent of transcription. In particular, promoters with GA motifs carry H3.3 regardless of the gene expression levels. H3.3 on promoters of inactive genes is associated with H3K27me3 at gene bodies. In addition, H3.3-enriched plant promoters often contain RNA Pol II considerably upstream of the transcriptional start site. H3.3 and RNA Pol II are found on active as well as on inactive promoters and are enriched at strongly regulated genes.

Conclusions

In animals and plants, H3.3 organizes chromatin in transcribed regions and in promoters. The results suggest a function of H3.3 in transcriptional regulation and support a model that a single ancestral H3 evolved into H3 variants with similar sub-functionalization patterns in plants and animals.