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Superhelical destabilization in regulatory regions of stress response genes.

Wang H, Benham CJ - PLoS Comput. Biol. (2008)

Bottom Line: We observe this statistically significant association of SIDD sites with upstream regions of genes functioning in transcription in 38 of 43 genomes of free-living bacteria, but in only four of 18 genomes of endosymbionts or obligate parasitic bacteria.These results suggest that strong SIDD sites 5' to participating genes may be involved in transcriptional responses to environmental changes, which are known to transiently alter superhelicity.We propose that these SIDD sites are active and necessary participants in superhelically mediated regulatory mechanisms governing changes in the global pattern of gene expression in prokaryotes in response to physiological or environmental changes.

View Article: PubMed Central - PubMed

Affiliation: UC Davis Genome Center, University of California Davis, Davis, California, United States of America.

ABSTRACT
Stress-induced DNA duplex destabilization (SIDD) analysis exploits the known structural and energetic properties of DNA to predict sites that are susceptible to strand separation under negative superhelical stress. When this approach was used to calculate the SIDD profile of the entire Escherichia coli K12 genome, it was found that strongly destabilized sites occur preferentially in intergenic regions that are either known or inferred to contain promoters, but rarely occur in coding regions. Here, we investigate whether the genes grouped in different functional categories have characteristic SIDD properties in their upstream flanks. We report that strong SIDD sites in the E. coli K12 genome are statistically significantly overrepresented in the upstream regions of genes encoding transcriptional regulators. In particular, the upstream regions of genes that directly respond to physiological and environmental stimuli are more destabilized than are those regions of genes that are not involved in these responses. Moreover, if a pathway is controlled by a transcriptional regulator whose gene has a destabilized 5' flank, then the genes (operons) in that pathway also usually contain strongly destabilized SIDD sites in their 5' flanks. We observe this statistically significant association of SIDD sites with upstream regions of genes functioning in transcription in 38 of 43 genomes of free-living bacteria, but in only four of 18 genomes of endosymbionts or obligate parasitic bacteria. These results suggest that strong SIDD sites 5' to participating genes may be involved in transcriptional responses to environmental changes, which are known to transiently alter superhelicity. We propose that these SIDD sites are active and necessary participants in superhelically mediated regulatory mechanisms governing changes in the global pattern of gene expression in prokaryotes in response to physiological or environmental changes.

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Related in: MedlinePlus

Genes in the E. coli K12 Genome according to Their Upstream SIDD SitesThe genes in the E. coli K12 genome are grouped according to the most destabilized SIDD sites in their whole upstream regions (yellow columns), or the most destabilized SIDD site in their immediate 50-bp or 250-bp upstream regions (blue or red columns), respectively. The former classification shows the highest SIDD0 fraction because there are fewer of them; 3,656 genes have 5′ intergenic flanks, while all 4,518 genes in the May 2006 release of GenProtEC are included in the other cases.
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pcbi-0040017-g001: Genes in the E. coli K12 Genome according to Their Upstream SIDD SitesThe genes in the E. coli K12 genome are grouped according to the most destabilized SIDD sites in their whole upstream regions (yellow columns), or the most destabilized SIDD site in their immediate 50-bp or 250-bp upstream regions (blue or red columns), respectively. The former classification shows the highest SIDD0 fraction because there are fewer of them; 3,656 genes have 5′ intergenic flanks, while all 4,518 genes in the May 2006 release of GenProtEC are included in the other cases.

Mentions: The distributions of E. coli K12 genes into SIDD groups are summarized in Figure 1 for each of the three definitions of what constitutes an upstream region. As shown there, the largest SIDD category in all cases is the SIDD8+ group; for example, 45.4% of all E. coli genes are not destabilized in their immediate 250-bp upstream regions. In all cases, however, the next largest category is SIDD0, which are the most strongly destabilized sites. This holds despite the fact that these are the most rare SIDD sites in the genome [28]. Although there are only 506 SIDD0 sites in the entire genome, 457 of them occur in upstream flanks of genes.


Superhelical destabilization in regulatory regions of stress response genes.

Wang H, Benham CJ - PLoS Comput. Biol. (2008)

Genes in the E. coli K12 Genome according to Their Upstream SIDD SitesThe genes in the E. coli K12 genome are grouped according to the most destabilized SIDD sites in their whole upstream regions (yellow columns), or the most destabilized SIDD site in their immediate 50-bp or 250-bp upstream regions (blue or red columns), respectively. The former classification shows the highest SIDD0 fraction because there are fewer of them; 3,656 genes have 5′ intergenic flanks, while all 4,518 genes in the May 2006 release of GenProtEC are included in the other cases.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2211533&req=5

pcbi-0040017-g001: Genes in the E. coli K12 Genome according to Their Upstream SIDD SitesThe genes in the E. coli K12 genome are grouped according to the most destabilized SIDD sites in their whole upstream regions (yellow columns), or the most destabilized SIDD site in their immediate 50-bp or 250-bp upstream regions (blue or red columns), respectively. The former classification shows the highest SIDD0 fraction because there are fewer of them; 3,656 genes have 5′ intergenic flanks, while all 4,518 genes in the May 2006 release of GenProtEC are included in the other cases.
Mentions: The distributions of E. coli K12 genes into SIDD groups are summarized in Figure 1 for each of the three definitions of what constitutes an upstream region. As shown there, the largest SIDD category in all cases is the SIDD8+ group; for example, 45.4% of all E. coli genes are not destabilized in their immediate 250-bp upstream regions. In all cases, however, the next largest category is SIDD0, which are the most strongly destabilized sites. This holds despite the fact that these are the most rare SIDD sites in the genome [28]. Although there are only 506 SIDD0 sites in the entire genome, 457 of them occur in upstream flanks of genes.

Bottom Line: We observe this statistically significant association of SIDD sites with upstream regions of genes functioning in transcription in 38 of 43 genomes of free-living bacteria, but in only four of 18 genomes of endosymbionts or obligate parasitic bacteria.These results suggest that strong SIDD sites 5' to participating genes may be involved in transcriptional responses to environmental changes, which are known to transiently alter superhelicity.We propose that these SIDD sites are active and necessary participants in superhelically mediated regulatory mechanisms governing changes in the global pattern of gene expression in prokaryotes in response to physiological or environmental changes.

View Article: PubMed Central - PubMed

Affiliation: UC Davis Genome Center, University of California Davis, Davis, California, United States of America.

ABSTRACT
Stress-induced DNA duplex destabilization (SIDD) analysis exploits the known structural and energetic properties of DNA to predict sites that are susceptible to strand separation under negative superhelical stress. When this approach was used to calculate the SIDD profile of the entire Escherichia coli K12 genome, it was found that strongly destabilized sites occur preferentially in intergenic regions that are either known or inferred to contain promoters, but rarely occur in coding regions. Here, we investigate whether the genes grouped in different functional categories have characteristic SIDD properties in their upstream flanks. We report that strong SIDD sites in the E. coli K12 genome are statistically significantly overrepresented in the upstream regions of genes encoding transcriptional regulators. In particular, the upstream regions of genes that directly respond to physiological and environmental stimuli are more destabilized than are those regions of genes that are not involved in these responses. Moreover, if a pathway is controlled by a transcriptional regulator whose gene has a destabilized 5' flank, then the genes (operons) in that pathway also usually contain strongly destabilized SIDD sites in their 5' flanks. We observe this statistically significant association of SIDD sites with upstream regions of genes functioning in transcription in 38 of 43 genomes of free-living bacteria, but in only four of 18 genomes of endosymbionts or obligate parasitic bacteria. These results suggest that strong SIDD sites 5' to participating genes may be involved in transcriptional responses to environmental changes, which are known to transiently alter superhelicity. We propose that these SIDD sites are active and necessary participants in superhelically mediated regulatory mechanisms governing changes in the global pattern of gene expression in prokaryotes in response to physiological or environmental changes.

Show MeSH
Related in: MedlinePlus