Chemical map of Schizosaccharomyces pombe reveals species-specific features in nucleosome positioning

Georgette Moyle-Heyrman, Tetiana Zaichuk, Liqun Xi, Quanwei Zhang, Olke C Uhlenbeck, Robert A Holmgren*, Jonathan Widom, Jiping Wang

*Corresponding author for this work

Research output: Contribution to journalArticle

53 Citations (Scopus)

Abstract

Using a recently developed chemical approach, we have generated a genome-wide map of nucleosomes in vivo in Schizosaccharomyces pombe (S. pombe) at base pair resolution. The shorter linker length previously identified in S. pombe is due to a preponderance of nucleosomes separated by ∼4/5 bp, placing nucleosomes on opposite faces of the DNA. The periodic dinucleotide feature thought to position nucleosomes is equally strong in exons as in introns, demonstrating that nucleosome positioning information can be superimposed on coding information. Unlike the case in Saccharomyces cerevisiae, A/T-rich sequences are enriched in S. pombe nucleosomes, particularly at ±20 bp around the dyad. This difference in nucleosome binding preference gives rise to a major distinction downstream of the transcription start site, where nucleosome phasing is highly predictable by A/T frequency in S. pombe but not in S. cerevisiae, suggesting that the genomes and DNA binding preferences of nucleosomes have coevolved in different species. The poly (dA-dT) tracts affect but do not deplete nucleosomes in S. pombe, and they prefer special rotational positions within the nucleosome, with longer tracts enriched in the 10- to 30-bp region from the dyad. S. pombe does not have a well-defined nucleosome-depleted region immediately upstream of most transcription start sites; instead, the -1 nucleosome is positioned with the expected spacing relative to the +1 nucleosome, and its occupancy is negatively correlated with gene expression. Although there is generally very good agreement between nucleosome maps generated by chemical cleavage and micrococcal nuclease digestion, the chemical map shows consistently higher nucleosome occupancy on DNA with high A/T content.

Original languageEnglish (US)
Pages (from-to)20158-20163
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume110
Issue number50
DOIs
StatePublished - Dec 10 2013

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Schizosaccharomyces
Nucleosomes
Transcription Initiation Site
Saccharomyces cerevisiae
DNA
Poly dA-dT
Genome
Micrococcal Nuclease
Base Pairing
Introns

Keywords

  • Chromatin structure
  • Gene regulation
  • Heterochromatin

ASJC Scopus subject areas

  • General

Cite this

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title = "Chemical map of Schizosaccharomyces pombe reveals species-specific features in nucleosome positioning",
abstract = "Using a recently developed chemical approach, we have generated a genome-wide map of nucleosomes in vivo in Schizosaccharomyces pombe (S. pombe) at base pair resolution. The shorter linker length previously identified in S. pombe is due to a preponderance of nucleosomes separated by ∼4/5 bp, placing nucleosomes on opposite faces of the DNA. The periodic dinucleotide feature thought to position nucleosomes is equally strong in exons as in introns, demonstrating that nucleosome positioning information can be superimposed on coding information. Unlike the case in Saccharomyces cerevisiae, A/T-rich sequences are enriched in S. pombe nucleosomes, particularly at ±20 bp around the dyad. This difference in nucleosome binding preference gives rise to a major distinction downstream of the transcription start site, where nucleosome phasing is highly predictable by A/T frequency in S. pombe but not in S. cerevisiae, suggesting that the genomes and DNA binding preferences of nucleosomes have coevolved in different species. The poly (dA-dT) tracts affect but do not deplete nucleosomes in S. pombe, and they prefer special rotational positions within the nucleosome, with longer tracts enriched in the 10- to 30-bp region from the dyad. S. pombe does not have a well-defined nucleosome-depleted region immediately upstream of most transcription start sites; instead, the -1 nucleosome is positioned with the expected spacing relative to the +1 nucleosome, and its occupancy is negatively correlated with gene expression. Although there is generally very good agreement between nucleosome maps generated by chemical cleavage and micrococcal nuclease digestion, the chemical map shows consistently higher nucleosome occupancy on DNA with high A/T content.",
keywords = "Chromatin structure, Gene regulation, Heterochromatin",
author = "Georgette Moyle-Heyrman and Tetiana Zaichuk and Liqun Xi and Quanwei Zhang and Uhlenbeck, {Olke C} and Holmgren, {Robert A} and Jonathan Widom and Jiping Wang",
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Chemical map of Schizosaccharomyces pombe reveals species-specific features in nucleosome positioning. / Moyle-Heyrman, Georgette; Zaichuk, Tetiana; Xi, Liqun; Zhang, Quanwei; Uhlenbeck, Olke C; Holmgren, Robert A; Widom, Jonathan; Wang, Jiping.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 110, No. 50, 10.12.2013, p. 20158-20163.

Research output: Contribution to journalArticle

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AU - Moyle-Heyrman, Georgette

AU - Zaichuk, Tetiana

AU - Xi, Liqun

AU - Zhang, Quanwei

AU - Uhlenbeck, Olke C

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AU - Widom, Jonathan

AU - Wang, Jiping

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N2 - Using a recently developed chemical approach, we have generated a genome-wide map of nucleosomes in vivo in Schizosaccharomyces pombe (S. pombe) at base pair resolution. The shorter linker length previously identified in S. pombe is due to a preponderance of nucleosomes separated by ∼4/5 bp, placing nucleosomes on opposite faces of the DNA. The periodic dinucleotide feature thought to position nucleosomes is equally strong in exons as in introns, demonstrating that nucleosome positioning information can be superimposed on coding information. Unlike the case in Saccharomyces cerevisiae, A/T-rich sequences are enriched in S. pombe nucleosomes, particularly at ±20 bp around the dyad. This difference in nucleosome binding preference gives rise to a major distinction downstream of the transcription start site, where nucleosome phasing is highly predictable by A/T frequency in S. pombe but not in S. cerevisiae, suggesting that the genomes and DNA binding preferences of nucleosomes have coevolved in different species. The poly (dA-dT) tracts affect but do not deplete nucleosomes in S. pombe, and they prefer special rotational positions within the nucleosome, with longer tracts enriched in the 10- to 30-bp region from the dyad. S. pombe does not have a well-defined nucleosome-depleted region immediately upstream of most transcription start sites; instead, the -1 nucleosome is positioned with the expected spacing relative to the +1 nucleosome, and its occupancy is negatively correlated with gene expression. Although there is generally very good agreement between nucleosome maps generated by chemical cleavage and micrococcal nuclease digestion, the chemical map shows consistently higher nucleosome occupancy on DNA with high A/T content.

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