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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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SIDD Profile of the Genomic Region Containing the Gene for the LysR-Type Transcription Regulator ilvY and its Target Gene ilvCThese form a divergently oriented gene pair that are known to be coordinately regulated by transcriptional coupling [53].
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pcbi-0040017-g004: SIDD Profile of the Genomic Region Containing the Gene for the LysR-Type Transcription Regulator ilvY and its Target Gene ilvCThese form a divergently oriented gene pair that are known to be coordinately regulated by transcriptional coupling [53].

Mentions: The divergent arrangement of these genes allows simultaneous bidirectional control of both, possibly involving transcriptional coupling between them through transcriptionally induced superhelicity. An example where this is known to occur is the ilvYC operon. Here, IlvY is in the LTTR family, and ilvC is the target gene it regulates. The SIDD profile for this operon is given in Figure 4. It has been demonstrated that transcriptional coupling of these two genes is mediated by the negative supercoiling generated by RNA polymerase translocation [52,53].


Superhelical destabilization in regulatory regions of stress response genes.

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

SIDD Profile of the Genomic Region Containing the Gene for the LysR-Type Transcription Regulator ilvY and its Target Gene ilvCThese form a divergently oriented gene pair that are known to be coordinately regulated by transcriptional coupling [53].
© Copyright Policy
Related In: Results  -  Collection

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

pcbi-0040017-g004: SIDD Profile of the Genomic Region Containing the Gene for the LysR-Type Transcription Regulator ilvY and its Target Gene ilvCThese form a divergently oriented gene pair that are known to be coordinately regulated by transcriptional coupling [53].
Mentions: The divergent arrangement of these genes allows simultaneous bidirectional control of both, possibly involving transcriptional coupling between them through transcriptionally induced superhelicity. An example where this is known to occur is the ilvYC operon. Here, IlvY is in the LTTR family, and ilvC is the target gene it regulates. The SIDD profile for this operon is given in Figure 4. It has been demonstrated that transcriptional coupling of these two genes is mediated by the negative supercoiling generated by RNA polymerase translocation [52,53].

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