Gene expression divergence in yeast is coupled to evolution of DNA-encoded nucleosome organization (original) (raw)

Nature Genetics volume 41, pages 438–445 (2009)Cite this article

Abstract

Eukaryotic transcription occurs within a chromatin environment, whose organization has an important regulatory function and is partly encoded in cis by the DNA sequence itself. Here, we examine whether evolutionary changes in gene expression are linked to changes in the DNA-encoded nucleosome organization of promoters. We find that in aerobic yeast species, where cellular respiration genes are active under typical growth conditions, the promoter sequences of these genes encode a relatively open (nucleosome-depleted) chromatin organization. This nucleosome-depleted organization requires only DNA sequence information, is independent of any cofactors and of transcription, and is a general property of growth-related genes. In contrast, in anaerobic yeast species, where cellular respiration genes are relatively inactive under typical growth conditions, respiration gene promoters encode relatively closed (nucleosome-occupied) chromatin organizations. Our results suggest a previously unidentified genetic mechanism underlying phenotypic diversity, consisting of DNA sequence changes that directly alter the DNA-encoded nucleosome organization of promoters.

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References

  1. Ihmels, J. et al. Rewiring of the yeast transcriptional network through the evolution of motif usage. Science 309, 938–940 (2005).
    Article CAS Google Scholar
  2. Borneman, A.R. et al. Divergence of transcription factor binding sites across related yeast species. Science 317, 815–819 (2007).
    Article CAS Google Scholar
  3. Lee, W. et al. A high-resolution atlas of nucleosome occupancy in yeast. Nat. Genet. 39, 1235–1244 (2007).
    Article CAS Google Scholar
  4. Yuan, G.C. et al. Genome-scale identification of nucleosome positions in S. cerevisiae. Science 309, 626–630 (2005).
    Article CAS Google Scholar
  5. Albert, I. et al. Translational and rotational settings of H2A.Z nucleosomes across the Saccharomyces cerevisiae genome. Nature 446, 572–576 (2007).
    Article CAS Google Scholar
  6. Shivaswamy, S. et al. Dynamic remodeling of individual nucleosomes across a eukaryotic genome in response to transcriptional perturbation. PLoS Biol. 6, e65 (2008).
    Article Google Scholar
  7. Whitehouse, I., Rando, O.J., Delrow, J. & Tsukiyama, T. Chromatin remodelling at promoters suppresses antisense transcription. Nature 450, 1031–1035 (2007).
    Article CAS Google Scholar
  8. Ozsolak, F., Song, J.S., Liu, X.S. & Fisher, D.E. High-throughput mapping of the chromatin structure of human promoters. Nat. Biotechnol. 25, 244–248 (2007).
    Article CAS Google Scholar
  9. Mavrich, T.N. et al. A barrier nucleosome model for statistical positioning of nucleosomes throughout the yeast genome. Genome Res 18, 1073–1083 (2008).
    Article CAS Google Scholar
  10. Segal, E. et al. A genomic code for nucleosome positioning. Nature 442, 772–778 (2006).
    Article CAS Google Scholar
  11. Ioshikhes, I.P., Albert, I., Zanton, S.J. & Pugh, B.F. Nucleosome positions predicted through comparative genomics. Nat. Genet. 38, 1210–1215 (2006).
    Article CAS Google Scholar
  12. Peckham, H.E. et al. Nucleosome positioning signals in genomic DNA. Genome Res. 17, 1170–1177 (2007).
    Article CAS Google Scholar
  13. Yuan, G.C. & Liu, J.S. Genomic sequence is highly predictive of local nucleosome depletion. PLoS Comput. Biol. 4, e13 (2008).
    Article Google Scholar
  14. Wapinski, I., Pfeffer, A., Friedman, N. & Regev, A. Natural history and evolutionary principles of gene duplication in fungi. Nature 449, 54–61 (2007).
    Article CAS Google Scholar
  15. Stuart, J.M., Segal, E., Koller, D. & Kim, S.K. A gene-coexpression network for global discovery of conserved genetic modules. Science 302, 249–255 (2003).
    Article CAS Google Scholar
  16. Bergmann, S., Ihmels, J. & Barkai, N. Similarities and differences in genome-wide expression data of six organisms. PLoS Biol. 2, E9 (2004).
    Article Google Scholar
  17. Ashburner, M. et al. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 25, 25–29 (2000).
    Article CAS Google Scholar
  18. Segal, E., Friedman, N., Koller, D. & Regev, A. A module map showing conditional activity of expression modules in cancer. Nat. Genet. 36, 1090–1098 (2004).
    Article CAS Google Scholar
  19. Gasch, A.P. et al. Genomic expression programs in the response of yeast cells to environmental changes. Mol. Biol. Cell 11, 4241–4257 (2000).
    Article CAS Google Scholar
  20. Mager, W.H. & Planta, R.J. Coordinate expression of ribosomal protein genes in yeast as a function of cellular growth rate. Mol. Cell. Biochem. 104, 181–187 (1991).
    Article CAS Google Scholar
  21. Field, Y. et al. Distinct modes of regulation by chromatin encoded through nucleosome positioning signals. PLoS Comput. Biol. 4, e1000216 (2008).
    Article Google Scholar
  22. Hanley, J.A. & McNeil, B.J. The meaning and use of the area under a receiver operating characteristic (ROC) curve. Radiology 143, 29–36 (1982).
    Article CAS Google Scholar
  23. Thastrom, A., Bingham, L.M. & Widom, J. Nucleosomal locations of dominant DNA sequence motifs for histone-DNA interactions and nucleosome positioning. J. Mol. Biol. 338, 695–709 (2004).
    Article CAS Google Scholar
  24. Kaplan, N. et al. The DNA-encoded nucleosome organization of a eukaryotic genome. Nature advance online publication, doi:10.1038/nature07667 (17 December 2008).
  25. Man, O. & Pilpel, Y. Differential translation efficiency of orthologous genes is involved in phenotypic divergence of yeast species. Nat. Genet. 39, 415–421 (2007).
    Article CAS Google Scholar
  26. Piskur, J. & Langkjaer, R.B. Yeast genome sequencing: the power of comparative genomics. Mol. Microbiol. 53, 381–389 (2004).
    Article CAS Google Scholar
  27. Feng, H.P., Scherl, D.S. & Widom, J. Lifetime of the histone octamer studied by continuous-flow quasielastic light scattering: test of a model for nucleosome transcription. Biochemistry 32, 7824–7831 (1993).
    Article CAS Google Scholar
  28. Altschul, S.F., Gish, W., Miller, W., Myers, E.W. & Lipman, D.J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).
    Article CAS Google Scholar

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Acknowledgements

We acknowledge with gratitude the gift of strains, protocols and advice from J. Berman (University of Minnesota), and thank H. Kelkar (University of North Carolina) for help with the Illumina sequencing data and the members of our respective laboratories for discussions and comments on the manuscript. This work was supported by grants from the US National Institutes of Health to J.D.L., from the NIH to J.W., and from the European Research Council (ERC) and NIH to E.S. N.K. is a Clore scholar. E.S. is the incumbent of the Soretta and Henry Shapiro career development chair.

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Author notes

  1. Yair Field and Yvonne Fondufe-Mittendorf: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Computer Science and Applied Mathematics, Weizmann Institute of Science, Rehovot, 76100, Israel
    Yair Field, Noam Kaplan, Yaniv Lubling & Eran Segal
  2. Department of Biochemistry, Molecular Biology, and Cell Biology, Northwestern University, 2153 Sheridan Road, Evanston, 60208, Illinois, USA
    Yvonne Fondufe-Mittendorf, Irene K Moore & Jonathan Widom
  3. Department of Biology, Carolina Center for Genome Sciences, and Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill, Chapel Hill, 27599, North Carolina, USA
    Piotr Mieczkowski & Jason D Lieb
  4. Department of Molecular Cell Biology, Weizmann Institute of Science, Rehovot, 76100, Israel
    Eran Segal

Authors

  1. Yair Field
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  2. Yvonne Fondufe-Mittendorf
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  3. Irene K Moore
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  4. Piotr Mieczkowski
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  5. Noam Kaplan
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  6. Yaniv Lubling
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  7. Jason D Lieb
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  8. Jonathan Widom
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  9. Eran Segal
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Contributions

Y.F., I.K.M., J.D.L., J.W. and E.S. conceived and designed the experiments. Y.F.-M. and I.K.M. performed the experiments. P.M. performed the sequencing. Y.F., N.K., Y.L., J.D.L., J.W. and E.S. analyzed the data. Y.F., J.D.L., J.W. and E.S. wrote the paper.

Corresponding authors

Correspondence toJonathan Widom or Eran Segal.

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Field, Y., Fondufe-Mittendorf, Y., Moore, I. et al. Gene expression divergence in yeast is coupled to evolution of DNA-encoded nucleosome organization.Nat Genet 41, 438–445 (2009). https://doi.org/10.1038/ng.324

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