Abstract

Polycomb Group (PcG) proteins mediate chromatin repression in plants and animals by catalyzing H3K27 methylation and H2AK118/119 mono-ubiquitination through the activity of the Polycomb repressive complex 2 (PRC2) and PRC1, respectively. PcG proteins were extensively studied in higher plants, but their function and target genes in unicellular branches of the green lineage remain largely unknown. To shed light on PcG function and modus operandi in a broad evolutionary context, we demonstrate phylogenetic relationship of core PRC1 and PRC2 proteins and H3K27me3 biochemical presence in several unicellular algae of different phylogenetic subclades. We focus then on one of the species, the model red alga Cyanidioschizon merolae, and show that H3K27me3 occupies both, genes and repetitive elements, and mediates the strength of repression depending on the differential occupancy over gene bodies. Furthermore, we report that H3K27me3 in C. merolae is enriched in telomeric and subtelomeric regions of the chromosomes and has unique preferential binding toward intein-containing genes involved in protein splicing. Thus, our study gives important insight for Polycomb-mediated repression in lower eukaryotes, uncovering a previously unknown link between H3K27me3 targets and protein splicing.

Highlights

  • In the eukaryotic cells, transcription state is dependent on the underlying chromatin state

  • We reveal that H3K27me3 target genes are enriched in the functional class of intein-mediated protein splicing

  • We focused on the representatives from subclades: Chlorophyta, Rhodophyta, Glaucophyta and Embryophyta

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Summary

Introduction

Transcription state is dependent on the underlying chromatin state. The fundamental structure of chromatin is based on a nucleosome, a complex of 147bp-long fragments of DNA wrapped around the core histone proteins (H2A, H2B, H3, H4). Chromatin state can be influenced by post-translational modifications deposited on the histones, either by direct structural changes in the nucleosomes or recruitment/displacement of secondary proteins involved in chromatin remodeling or transcription. The presence of particular histone modifications often determines the type of the chromatin and correlates with transcriptional activity of the target DNA. Tri-methylation of lysine 27 on histone H3 (H3K27me3) and mono-ubiquitination of histone H2AK118/H2AK119 (H2AK118ub/H2AK119ub) are commonly associated with transcriptionally silent facultative heterochromatin. Deposition of H3K27me and H2AK118ub/H2AK119ub is mediated by Polycomb group (PcG) proteins, whose function was initially shown to control developmentally regulated processes and

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