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Genome-wide mapping of nucleosome positioning in Toxoplasma gondii implicates nucleosome-free regions as the major gene regulatory regions

ABSTRACT: Nucleosome organization is critical for the regulation of gene expression, and genome-scale mapping of nucleosomes has revealed a conserved, highly ordered pattern in nucleosome positioning. Most genome-wide studies have been performed in model organisms and little is known about nucleosome positioning in evolutionarily divergent eukaryotes. We generated a high-resolution nucleosome map of the protozoan parasite Toxoplasma gondii from four high quality MNase-Seq datasets. T. gondii nucleosomes are organised in phase around the transcription start sites (TSSs) with a canonical pattern that is conserved across eukaryotes. Nucleosome occupancy in exons is influenced by several factors, including GC content, length of exons and strength of splice sites. Poly(dA:dT) is enriched at the +1 nucleosome rather than nucleosome-free regions (NFRs) and serves as the key sequence associated with nucleosome formation in T. gondii. Motif analysis of sequences in NFR1, adjacent to the transcription start site, revealed enrichment of DNA-binding motifs recognized by members of the plant-like ApiAP2 transcription factor family that is conserved across Apicomplexa. Genes associated with the two most common motifs are enriched in genes upregulated during two major waves of mRNA accumulation within the cell cycle. Genome-wide peaks from T. gondii assays for transposase-accessible chromatin using sequencing (ATAC-seq) coincide with NFR1, consistent with the enrichment of T. gondii open chromatin regulatory regions localizing to close to transcription initiation sites. Finally, by integrating the map of nucleosome positions with ChIP-seq we suggest that nucleosome positioning and placement of histone variants and histone modifications play roles in splicing of genes in T. gondii.

ORGANISM(S): Toxoplasma gondii

PROVIDER: GSE86620 | GEO | 2017/09/08

SECONDARY ACCESSION(S): PRJNA342418

REPOSITORIES: GEO

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Project description:Nucleosome positioning dictates the DNA accessibility for regulatory proteins, and thus is critical for gene expression and regulation. It has been well documented that only a subset of nucleosomes are reproducibly positioned (phased) in eukaryotic genomes. The most prominent example of phased nucleosomes is the context of genes, where phased nucleosomes flank the transcriptional starts sites (TSSs). It is unclear, however, what factors influence nucleosome phasing in regions that are not close to genes. We performed a combinational mapping of nucleosome positioning and DNase I hypersensitive sites (DHSs) across the rice genome. We discovered that DHSs located in a variety of contexts, both genic and intergenic, were flanked by strongly phased nucleosome arrays. Our results support the barrier model for nucleosome organization as a general feature of eukaryote genomes, including plant genomes, and not limited to TSSs. Specifically, regions bound with regulatory proteins, including intergenic regions, can serve as barriers that organize phased nucleosome arrays on both sides. Our results also suggest that rice DHSs often span a single, phased nucleosome, similar to the H2A.Z-containing nucleosomes observed in DHSs in the human genome. We propose that genome-wide nucleosome positioning in the eukaryotic genomes is orchestrated by genomic regions associated with regulatory proteins. Rice chromatin was digested by micrococcal nuclease (MNase) into mono-nucleosome size. Mono-nucleosomal DNA was isolated and sequenced (MNase-seq) using Illumina sequencing platforms. We obtained a total of 38 million (M) single-end reads from our first MNase-seq experiment and mapped ~26 M to unique positions in the rice genome. We also conducted pair-end sequencing of an independent MNase-seq library, obtained 274 M paired-end reads, and mapped ~231 M read pairs to unique positions in the rice genome.We applied a strategy of combinational mapping of nucleosome positioning and DHSs (GSE26610) to examine whether nucleosome positioning is associated with all cis-regulatory elements in the rice genome. All datasets used in the analysis were developed using rice leaf tissue in the same developmental stage

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Genome-wide mapping of nucleosome positioning in Toxoplasma gondii implicates nucleosome-free regions as the major gene regulatory regions

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