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Gene expression divergence in yeast is coupled to evolution of DNA-encoded nucleosome organization

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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Figure 1: S. cerevisiae and C. albicans show large-scale changes in the transcriptional programs of cellular respiration and mitochondrial function genes.
Figure 2: The expression divergence of cellular respiration genes is accompanied by changes in the DNA-encoded nucleosome organization of their promoters.
Figure 3: The DNA-encoded nucleosome organization of promoters driving genes involved in cellular respiration has diverged between S. cerevisiae and C. albicans.
Figure 4: The emergence of anaerobic yeast species coincides with an evolutionary change in the DNA-encoded nucleosome organization of cellular respiration gene promoters.
Figure 5: A global relationship between evolutionary changes in the DNA-encoded nucleosome organization and evolutionary changes in expression.

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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

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  1. Yair Field
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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 to Jonathan Widom or Eran Segal.

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Supplementary Figures 1–3 and Supplementary Tables 1 and 2 (PDF 748 kb)

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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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