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Schizosaccharomyces pombe genome-wide nucleosome mapping reveals positioning mechanisms distinct from those of Saccharomyces cerevisiae

Nature Structural & Molecular Biology volume 17, pages 251257 (2010) | Download Citation

Abstract

Positioned nucleosomes limit the access of proteins to DNA and implement regulatory features encoded in eukaryotic genomes. Here we have generated the first genome-wide nucleosome positioning map for Schizosaccharomyces pombe and annotated transcription start and termination sites genome wide. Using this resource, we found surprising differences from the previously published nucleosome organization of the distantly related yeast Saccharomyces cerevisiae. DNA sequence guides nucleosome positioning differently: for example, poly(dA-dT) elements are not enriched in S. pombe nucleosome-depleted regions. Regular nucleosomal arrays emanate more asymmetrically—mainly codirectionally with transcription—from promoter nucleosome-depleted regions, but promoters harboring the histone variant H2A.Z also show regular arrays upstream of these regions. Regular nucleosome phasing in S. pombe has a very short repeat length of 154 base pairs and requires a remodeler, Mit1, that is conserved in humans but is not found in S. cerevisiae. Nucleosome positioning mechanisms are evidently not universal but evolutionarily plastic.

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Acknowledgements

We thank H. Bhuiyan and J. Walfridsson for generating the S. pombe expression data during their work in the group of K. Ekwall, R.R. Barrales (group of J.J. Ibeas, Universidad Pablo de Olavide, Sevilla, Spain) for bringing the first S. pombe strains into the Korber group, F. Thoma (ETH Zürich, Switzerland) for advice on chromatin analysis in S. pombe, F. Fagerström-Billai at the BEA microarray facility at Novum, Karolinska Institutet, for assistance, and F. Müller-Planitz (Adolf-Butenandt-Institut, Univ. Munich) for help with MATLAB. We are grateful for the communication of replication origin coordinates by C. Heichinger (Univ. Zürich) and of TSS coordinates by W. Lee (Stanford Univ.) and N. Dutrow (Univ. Utah). We thank H. Madhani and co-workers (Univ. California San Francisco) for sharing data before publication and for comments on the manuscript. This work was funded by the German Research Community (Transregio 5; P.K. and co-workers), the 6th Framework Programme of the European Union (NET programme; P.K. and K.E. and co-workers), the Swedish Cancer Society and Swedish Research Council (K.E. laboratory) and the Claudia Adams Barr Program (G.-C.Y.).

Author information

Author notes

    • Alexandra B Lantermann
    •  & Tobias Straub

    These authors contributed equally to this work.

Affiliations

  1. Adolf-Butenandt-Institut, University of Munich, Munich, Germany.

    • Alexandra B Lantermann
    • , Tobias Straub
    •  & Philipp Korber
  2. Karolinska Institutet, Department of Biosciences and Nutrition, Center for Biosciences NOVUM, Huddinge, Sweden.

    • Annelie Strålfors
    •  & Karl Ekwall
  3. Department of Biostatistics, Harvard School of Public Health, Boston, Massachusetts, USA.

    • Guo-Cheng Yuan
  4. Department of Biostatistics and Computational Biology, Dana-Farber Cancer Institute, Boston, Massachusetts, USA.

    • Guo-Cheng Yuan

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Contributions

A.B.L. carried out all preparation and experimental analysis of biological material besides the actual microarray hybridizations, which were done at the BEA Affymetrix core facility at Novum with the help of A.S. A.B.L. did the S. pombe TSS and TTS annotation. T.S. did the bioinformatics analyses. G.-C.Y. provided the N-score codes, applied the model of Kaplan et al.17, analyzed DNA sequence features and gave advice on bioinformatics. A.S. and K.E. introduced A.B.L. to the work with S. pombe and microarrays. K.E. provided strains and reference data. P.K. and K.E. initiated, designed and supervised the study. A.B.L. and T.S. generated the figures. P.K. and A.B.L. wrote the paper. A.B.L. and T.S. contributed equally to the study. All authors discussed results and commented on the manuscript

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Karl Ekwall or Philipp Korber.

Supplementary information

PDF files

  1. 1.

    Supplementary Text and Figures

    Supplementary Figures 1–7 and Supplementary Tables 1 and 4

Excel files

  1. 1.

    Supplementary Table 2

    Annotation of S. pombe transcription start sites (TSS) and transcription termination sites (TTS)

  2. 2.

    Supplementary Table 3

    Parameters of the N-score models trained with S. cerevisiae or S. pombe experimental data

  3. 3.

    Supplementary Table 5

    Genes with affected transcription levels in S. pombe mit1 mutant

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DOI

https://doi.org/10.1038/nsmb.1741

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