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Translational and rotational settings of H2A.Z nucleosomes across the Saccharomyces cerevisiae genome

Author

Listed:
  • Istvan Albert

    (Center for Comparative Genomics and Bioinformatics,)

  • Travis N. Mavrich

    (Center for Comparative Genomics and Bioinformatics,
    Center for Gene Regulation, The Pennsylvania State University, University Park, Pennsylvania 16802, USA)

  • Lynn P. Tomsho

    (Center for Comparative Genomics and Bioinformatics,)

  • Ji Qi

    (Center for Comparative Genomics and Bioinformatics,)

  • Sara J. Zanton

    (Center for Comparative Genomics and Bioinformatics,
    Center for Gene Regulation, The Pennsylvania State University, University Park, Pennsylvania 16802, USA)

  • Stephan C. Schuster

    (Center for Comparative Genomics and Bioinformatics,)

  • B. Franklin Pugh

    (Center for Comparative Genomics and Bioinformatics,
    Center for Gene Regulation, The Pennsylvania State University, University Park, Pennsylvania 16802, USA)

Abstract

The nucleosome is the fundamental building block of eukaryotic chromosomes. Access to genetic information encoded in chromosomes is dependent on the position of nucleosomes along the DNA. Alternative locations just a few nucleotides apart can have profound effects on gene expression1. Yet the nucleosomal context in which chromosomal and gene regulatory elements reside remains ill-defined on a genomic scale. Here we sequence the DNA of 322,000 individual Saccharomyces cerevisiae nucleosomes, containing the histone variant H2A.Z, to provide a comprehensive map of H2A.Z nucleosomes in functionally important regions. With a median 4-base-pair resolution, we identify new and established signatures of nucleosome positioning. A single predominant rotational setting and multiple translational settings are evident. Chromosomal elements, ranging from telomeres to centromeres and transcriptional units, are found to possess characteristic nucleosomal architecture that may be important for their function. Promoter regulatory elements, including transcription factor binding sites and transcriptional start sites, show topological relationships with nucleosomes, such that transcription factor binding sites tend to be rotationally exposed on the nucleosome surface near its border. Transcriptional start sites tended to reside about one helical turn inside the nucleosome border. These findings reveal an intimate relationship between chromatin architecture and the underlying DNA sequence it regulates.

Suggested Citation

  • Istvan Albert & Travis N. Mavrich & Lynn P. Tomsho & Ji Qi & Sara J. Zanton & Stephan C. Schuster & B. Franklin Pugh, 2007. "Translational and rotational settings of H2A.Z nucleosomes across the Saccharomyces cerevisiae genome," Nature, Nature, vol. 446(7135), pages 572-576, March.
    • Handle: RePEc:nat:nature:v:446:y:2007:i:7135:d:10.1038_nature05632
    DOI: 10.1038/nature05632
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    Citations

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    Cited by:

    1. Ji-Ping Wang & Yvonne Fondufe-Mittendorf & Liqun Xi & Guei-Feng Tsai & Eran Segal & Jonathan Widom, 2008. "Preferentially Quantized Linker DNA Lengths in Saccharomyces cerevisiae," PLOS Computational Biology, Public Library of Science, vol. 4(9), pages 1-10, September.
    2. Guo-Cheng Yuan & Jun S Liu, 2008. "Genomic Sequence Is Highly Predictive of Local Nucleosome Depletion," PLOS Computational Biology, Public Library of Science, vol. 4(1), pages 1-11, January.
    3. Kuan Pei Fen & Huebert Dana & Gasch Audrey & Keles Sunduz, 2009. "A Non-Homogeneous Hidden-State Model on First Order Differences for Automatic Detection of Nucleosome Positions," Statistical Applications in Genetics and Molecular Biology, De Gruyter, vol. 8(1), pages 1-45, June.
    4. Jiayi Fan & Andrew T. Moreno & Alexander S. Baier & Joseph J. Loparo & Craig L. Peterson, 2022. "H2A.Z deposition by SWR1C involves multiple ATP-dependent steps," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    5. Zing Tsung-Yeh Tsai & Shin-Han Shiu & Huai-Kuang Tsai, 2015. "Contribution of Sequence Motif, Chromatin State, and DNA Structure Features to Predictive Models of Transcription Factor Binding in Yeast," PLOS Computational Biology, Public Library of Science, vol. 11(8), pages 1-22, August.
    6. Shuxiang Li & Tiejun Wei & Anna R. Panchenko, 2023. "Histone variant H2A.Z modulates nucleosome dynamics to promote DNA accessibility," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    7. Wolfram Möbius & Ulrich Gerland, 2010. "Quantitative Test of the Barrier Nucleosome Model for Statistical Positioning of Nucleosomes Up- and Downstream of Transcription Start Sites," PLOS Computational Biology, Public Library of Science, vol. 6(8), pages 1-11, August.
    8. Sai Li & Michael R. Wasserman & Olga Yurieva & Lu Bai & Michael E. O’Donnell & Shixin Liu, 2022. "Nucleosome-directed replication origin licensing independent of a consensus DNA sequence," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    9. Alexander W. Blocker & Edoardo M. Airoldi, 2016. "Template-Based Models for Genome-Wide Analysis of Next-Generation Sequencing Data at Base-Pair Resolution," Journal of the American Statistical Association, Taylor & Francis Journals, vol. 111(515), pages 967-987, July.

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