Dataset Information

Genome urbanization: clusters of topologically co-regulated genes delineate functional compartments in the genome of Saccharomyces cerevisiae.

ABSTRACT: The eukaryotic genome evolves under the dual constraint of maintaining coordinated gene transcription and performing effective DNA replication and cell division, the coupling of which brings about inevitable DNA topological tension. DNA supercoiling is resolved and, in some cases, even harnessed by the genome through the function of DNA topoisomerases, as has been shown in the concurrent transcriptional activation and suppression of genes upon transient deactivation of topoisomerase II (topoII). By analyzing a genome-wide transcription run-on experiment upon thermal inactivation of topoII in Saccharomyces cerevisiae we were able to define 116 gene clusters of consistent response (either positive or negative) to topological stress. A comprehensive analysis of these topologically co-regulated gene clusters reveals pronounced preferences regarding their functional, regulatory and structural attributes. Genes that negatively respond to topological stress, are positioned in gene-dense pericentromeric regions, are more conserved and associated to essential functions, while upregulated gene clusters are preferentially located in the gene-sparse nuclear periphery, associated with secondary functions and under complex regulatory control. We propose that genome architecture evolves with a core of essential genes occupying a compact genomic 'old town', whereas more recently acquired, condition-specific genes tend to be located in a more spacious 'suburban' genomic periphery.

SUBMITTER: Tsochatzidou M

PROVIDER: S-EPMC5449599 | biostudies-literature | 2017 Jun

REPOSITORIES: biostudies-literature

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Genome urbanization: clusters of topologically co-regulated genes delineate functional compartments in the genome of Saccharomyces cerevisiae.

Tsochatzidou Maria M Malliarou Maria M Papanikolaou Nikolas N Roca Joaquim J Nikolaou Christoforos C

Nucleic acids research 20170601 10

The eukaryotic genome evolves under the dual constraint of maintaining coordinated gene transcription and performing effective DNA replication and cell division, the coupling of which brings about inevitable DNA topological tension. DNA supercoiling is resolved and, in some cases, even harnessed by the genome through the function of DNA topoisomerases, as has been shown in the concurrent transcriptional activation and suppression of genes upon transient deactivation of topoisomerase II (topoII). ...[more]

PMID: 28369650

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Project description:BACKGROUND: Protein subcellular localization and differences in oxidation state between subcellular compartments are two well-studied features of the the cellular organization of S. cerevisiae (yeast). Theories about the origin of subcellular organization are assisted by computational models that can integrate data from observations of compositional and chemical properties of the system. PRESENTATION AND IMPLICATIONS OF THE HYPOTHESIS: I adopt the hypothesis that the state of yeast subcellular organization is in a local energy minimum. This hypothesis implies that equilibrium thermodynamic models can yield predictions about the interdependence between populations of proteins and their subcellular chemical environments. TESTING THE HYPOTHESIS: Three types of tests are proposed. First, there should be correlations between modeled and observed oxidation states for different compartments. Second, there should be a correspondence between the energy requirements of protein formation and the order the appearance of organelles during cellular development. Third, there should be correlations between the predicted and observed relative abundances of interacting proteins within compartments. RESULTS: The relative metastability fields of subcellular homologs of glutaredoxin and thioredoxin indicate a trend from less to more oxidizing as mitochondrion - cytoplasm - nucleus. Representing the overall amino acid compositions of proteins in 23 different compartments each with a single reference model protein suggests that the formation reactions for proteins in the vacuole (in relatively oxidizing conditions), ER and early Golgi (in relatively reducing conditions) are relatively highly favored, while that for the microtubule is the most costly. The relative abundances of model proteins for each compartment inferred from experimental data were found in some cases to correlate with the predicted abundances, and both positive and negative correlations were found for some assemblages of proteins in known complexes. CONCLUSION: The results of these calculations and tests suggest that a tendency toward a metastable energy minimum could underlie some organizational links between the the chemical thermodynamic properties of proteins and subcellular chemical environments. Future models of this kind will benefit from consideration of additional thermodynamic variables together with more detailed subcellular observations.

Dataset Information

Genome urbanization: clusters of topologically co-regulated genes delineate functional compartments in the genome of Saccharomyces cerevisiae.

Publications

Genome urbanization: clusters of topologically co-regulated genes delineate functional compartments in the genome of Saccharomyces cerevisiae.

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