The role of nucleosome positioning in the evolution of gene regulation

• Published in: PLoS biology Vol. 8; no. 7; p. e1000414
• Main Authors: Tsankov, Alexander M, Thompson, Dawn Anne, Socha, Amanda, Regev, Aviv, Rando, Oliver J
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 01.07.2010; Public Library of Science (PLoS)
• Subjects: Alternative Splicing - genetics; Analysis; Ascomycota - enzymology; Ascomycota - genetics; Binding sites; Chromosome Positioning - genetics; Conserved Sequence; Cytoskeleton - genetics; DNA Packaging - genetics; DNA-Directed RNA Polymerases - metabolism; Evolution; Evolution, Molecular; Evolutionary Biology/Genomics; Fermentation; Fungal Proteins - genetics; Fungal Proteins - metabolism; Gene Duplication; Gene expression; Gene Expression Regulation, Fungal; Genes, Fungal - genetics; Genetic aspects; Genetic regulation; Genetics; Genetics and Genomics/Chromosome Biology; Genetics and Genomics/Comparative Genomics; Genetics and Genomics/Functional Genomics; Genetics and Genomics/Gene Expression; Genetics and Genomics/Genomics; Genetics and Genomics/Nuclear Structure and Function; Genomes; Genomics; Meiosis - genetics; Mitochondria - genetics; Molecular Biology/Chromosome Structure; Molecular evolution; Nuclear Pore - genetics; Nucleosomes; Nucleosomes - genetics; Open Reading Frames - genetics; Peroxisomes - genetics; Phylogeny; Physiological aspects; Proteasome Endopeptidase Complex - genetics; Proteins; Scholarships & fellowships; Species Specificity; Transcription Factors - genetics; Transcription Factors - metabolism; United States; Ascomycota; Chromosome Positioning; Gene Duplication; Gene Expression Regulation, Fungal; Alternative Splicing; Species Specificity; Open Reading Frames; Fungal Proteins; Meiosis; Phylogeny; Proteasome Endopeptidase Complex; Mitochondria; Peroxisomes; DNA Packaging; DNA-Directed RNA Polymerases; Conserved Sequence; Cytoskeleton; Genes, Fungal; Nucleosomes; Transcription Factors; Nuclear Pore; Evolution, Molecular
• ISSN: 1545-7885; 1544-9173; 1545-7885
• DOI: 10.1371/journal.pbio.1000414

Chromatin organization plays a major role in gene regulation and can affect the function and evolution of new transcriptional programs. However, it can be difficult to decipher the basis of changes in chromatin organization and their functional effect on gene expression. Here, we present a large-scale comparative genomic analysis of the relationship between chromatin organization and gene expression, by measuring mRNA abundance and nucleosome positions genome-wide in 12 Hemiascomycota yeast species. We found substantial conservation of global and functional chromatin organization in all species, including prominent nucleosome-free regions (NFRs) at gene promoters, and distinct chromatin architecture in growth and stress genes. Chromatin organization has also substantially diverged in both global quantitative features, such as spacing between adjacent nucleosomes, and in functional groups of genes. Expression levels, intrinsic anti-nucleosomal sequences, and trans-acting chromatin modifiers all play important, complementary, and evolvable roles in determining NFRs. We identify five mechanisms that couple chromatin organization to evolution of gene regulation and have contributed to the evolution of respiro-fermentation and other key systems, including (1) compensatory evolution of alternative modifiers associated with conserved chromatin organization, (2) a gradual transition from constitutive to trans-regulated NFRs, (3) a loss of intrinsic anti-nucleosomal sequences accompanying changes in chromatin organization and gene expression, (4) re-positioning of motifs from NFRs to nucleosome-occluded regions, and (5) the expanded use of NFRs by paralogous activator-repressor pairs. Our study sheds light on the molecular basis of chromatin organization, and on the role of chromatin organization in the evolution of gene regulation.