A balancing act: heterochromatin protein 1a and the Polycomb group coordinate their levels to silence chromatin in Drosophila.

Janel R Cabrera,Ursula Olcese,Jamila I Horabin

doi:10.1186/s13072-015-0010-z

Janel R Cabrera, Ursula Olcese + Show 1 more

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https://doi.org/10.1186/s13072-015-0010-z

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Abstract

BackgroundThe small non-histone protein Heterochromatin protein 1a (HP1a) plays a vital role in packaging chromatin, most notably in forming constitutive heterochromatin at the centromeres and telomeres. A second major chromatin regulating system is that of the Polycomb/trithorax groups of genes which, respectively, maintain the repressed/activated state of euchromatin. Recent analyses suggest they affect the expression of a multitude of genes, beyond the homeotics whose alteration in expression lead to their initial discovery.ResultsOur data suggest that early in Drosophila development, HP1a collaborates with the Polycomb/trithorax groups of proteins to regulate gene expression and that the two chromatin systems do not act separately as convention describes. HP1a affects the levels of both the Polycomb complexes and RNA polymerase II at promoters, as assayed by chromatin immunoprecipitation analysis. Deposition of both the repressive (H3K27me3) and activating (H3K4me3) marks promoted by the Polycomb/trithorax group genes at gene promoters is affected. Additionally, depending on which parent contributes the null mutation of the HP1a gene, the levels of the H3K27me3 and H3K9me3 silencing marks at both promoters and heterochromatin are different. Changes in levels of the H3K27me3 and H3K9me3 repressive marks show a mostly reciprocal nature. The time around the mid-blastula transition, when the zygotic genome begins to be actively transcribed, appears to be a transition/decision point for setting the levels.ConclusionsWe find that HP1a, which is normally critical for the formation of constitutive heterochromatin, also affects the generation of the epigenetic marks of the Polycomb/trithorax groups of proteins, chromatin modifiers which are key to maintaining gene expression in euchromatin. At gene promoters, deposition of both the repressive H3K27me3 and activating H3K4me3 marks of histone modifications shows a dependence on HP1a. Around the mid-blastula transition, when the zygotic genome begins to be actively transcribed, a pivotal decision for the level of silencing appears to take place. This is also when the embryo organizes its genome into heterochromatin and euchromatin. A balance between the HP1a and Polycomb group silencing systems appears to be set for the chromatin types that each system will primarily regulate.Electronic supplementary materialThe online version of this article (doi:10.1186/s13072-015-0010-z) contains supplementary material, which is available to authorized users.

Highlights

The small non-histone protein Heterochromatin protein 1a (HP1a) plays a vital role in packaging chromatin, most notably in forming constitutive heterochromatin at the centromeres and telomeres
In the event of reduced maternal HP1a levels, the PcG system serves as a back-up resulting in an increase in H3K27me3 levels at heterochromatin, presumably to decrease the transcription of repetitive sequences which are derepressed by the reduction in HP1a
Introducing a copy of the Su(var)2-505 null mutation (HP1a gene name) in heterozygotes of the Ubx130 loss of function allele worsened the phenotype making the haltere larger (Additional file 1: Figure S1). This indicates a decrease in Ubx levels and that HP1a has a positive effect on Ubx expression, similar to what we observed at

Summary

Introduction

The small non-histone protein Heterochromatin protein 1a (HP1a) plays a vital role in packaging chromatin, most notably in forming constitutive heterochromatin at the centromeres and telomeres. While nucleosomes define the basic unit, at the genome level chromatin is frequently viewed as being organized into two major forms: euchromatin which is generally associated with gene-rich regions and the chromatin is less condensed, whereas heterochromatin is highly condensed, late replicating, and mostly transcriptionally silent throughout the cell cycle. It is generally gene poor and is associated with telomeres, centromeres, and pericentric regions. Suggest HP1 affects the transcription of euchromatin genes and can act positively [3] (reviewed in [4])

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