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

Yair Field, Yvonne Fondufe-Mittendorf, Irene K. Moore, Piotr Mieczkowski, Noam Kaplan, Yaniv Lubling, Jason D. Lieb, Jonathan Widom, Eran Segal

Research output: Contribution to journalArticlepeer-review

116 Scopus citations

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.

Original languageEnglish
Pages (from-to)438-445
Number of pages8
JournalNature Genetics
Volume41
Issue number4
DOIs
StatePublished - Apr 2009

Bibliographical note

Funding Information:
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.

ASJC Scopus subject areas

  • Genetics

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