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Gene Expression Divergence in Yeast is Coupled to Evolution of DNA-Encoded Nucleosome Organization

Yair Field^1*, Yvonne Fondufe-Mittendorf^2*, Irene Moore², Piotr Mieczkowski³, Noam Kaplan¹, Yaniv Lubling¹, Jason D. Lieb^3,†, Jonathan Widom^2,†, Eran Segal^1,4,†

Eukaryotic transcription occurs within a chromatin environment, whose organization plays an important regulatory role 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 co-factors and of transcription, and is a general property of growth-related genes. In contrast, in anaerobic yeast species, where cellular respiration genes are inactive under typical growth conditions, respiration gene promoters encode relatively closed (nucleosome-occupied) chromatin organizations. Thus, 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.

Illustration: A global relationship between transcriptional programs and the DNA-encoded nucleosome organization of promoters that is remarkably conserved across yeast species, even in the presence of expression divergence. Shown are Gene Ontology gene sets mapped for C. albicans (y-axis) and S. cerevisiae (x-axis) according to their expression correlation with growth-related genes (left panel) and according to their promoters' DNA-encoded nucleosome organization (right panel). In both species, promoters of growth-related genes (category I, red) encode relatively open nucleosome organizations, while promoters of condition-specific genes (category II, green) encode relatively closed nucleosome organizations. Accordingly, the expression divergence of the aerobic respiration genes (category III, blue) is coupled to a change in their DNA-encoded nucleosome organization of promoters.

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^* These authors contributed equally to this work.
^† Correspondence should be addressed to E.S. , J.W. or J.D.L
¹ Dept. of Computer Science and Applied Mathematics, Weizmann Institute of Science, Rehovot 76100, Israel.
² Department of Biochemistry, Molecular Biology, and Cell Biology, Northwestern University, 2153 Sheridan Road, Evanston, IL 60208 USA.
³ Department of Biology, Carolina Center for Genome Sciences, and Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599, USA.
⁴ Department of Molecular Cell Biology, Weizmann Institute of Science, Rehovot, 76100, Israel.