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Characterization of relationships between transcriptional units and operon structures in Bacillus subtilis and Escherichia coli.

Okuda S, Kawashima S, Kobayashi K, Ogasawara N, Kanehisa M, Goto S - BMC Genomics (2007)

Bottom Line: Consequently, we found that the levels of gene co-regulation was correlated to intergenic distances and gene expression levels.Most interestingly, we found that functional associations in SOPs were more observed in the environmental and genetic information processes.In addition, such differences may play an important role in the evolution of gene order across genomes.

View Article: PubMed Central - HTML - PubMed

Affiliation: Bioinformatics Center, Institute for Chemical Research, Kyoto University, Gokasho, Uji, Kyoto 611-0011, Japan. okuda@kuicr.kyoto-u.ac.jp <okuda@kuicr.kyoto-u.ac.jp>

ABSTRACT

Background: Operon structures play an important role in transcriptional regulation in prokaryotes. However, there have been fewer studies on complicated operon structures in which the transcriptional units vary with changing environmental conditions. Information about such complicated operons is helpful for predicting and analyzing operon structures, as well as understanding gene functions and transcriptional regulation.

Results: We systematically analyzed the experimentally verified transcriptional units (TUs) in Bacillus subtilis and Escherichia coli obtained from ODB and RegulonDB. To understand the relationships between TUs and operons, we defined a new classification system for adjacent gene pairs, divided into three groups according to the level of gene co-regulation: operon pairs (OP) belong to the same TU, sub-operon pairs (SOP) that are at the transcriptional boundaries within an operon, and non-operon pairs (NOP) belonging to different operons. Consequently, we found that the levels of gene co-regulation was correlated to intergenic distances and gene expression levels. Additional analysis revealed that they were also correlated to the levels of conservation across about 200 prokaryotic genomes. Most interestingly, we found that functional associations in SOPs were more observed in the environmental and genetic information processes.

Conclusion: Complicated operon structures were correlated with genome organization and gene expression profiles. Such intricately regulated operons allow functional differences depending on environmental conditions. These regulatory mechanisms are helpful in accommodating the variety of changes that happen around the cell. In addition, such differences may play an important role in the evolution of gene order across genomes.

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Co-expression profile of operons: the schematic model of the operon diversity and its examples. (A) Schematic model of a diverse operon. In this model, we assume that there is a longer TU and a shorter TU. Arrows indicate the region transcribed as a TU. Open boxes to the side and above the grid indicate genes. Each box in the grid indicates the level of correlation of gene expression as colors from blue to red correspond to the correlation coefficients. The gene pairs without the TU boundary should show strong correlation with vivid red color. On the other hand, gene pairs across the boundary should show a slightly weaker correlation with orange color. (B) The sigB operon. There are two promoters in the sigB operon. The first one is located in the upstream of the first gene of the operon, and second one is located in between fourth and fifth genes. Therefore, two different transcripts cause this pattern. (rsbV in this operon was not measured in the microarray experiments, so the region of this gene is not colored.) (C) The clpC operon. The transcription of this operon is basically promoted by sigma B, while the last two genes (sms and yacK) were reported to be also transcribed by sigma M.
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Figure 6: Co-expression profile of operons: the schematic model of the operon diversity and its examples. (A) Schematic model of a diverse operon. In this model, we assume that there is a longer TU and a shorter TU. Arrows indicate the region transcribed as a TU. Open boxes to the side and above the grid indicate genes. Each box in the grid indicates the level of correlation of gene expression as colors from blue to red correspond to the correlation coefficients. The gene pairs without the TU boundary should show strong correlation with vivid red color. On the other hand, gene pairs across the boundary should show a slightly weaker correlation with orange color. (B) The sigB operon. There are two promoters in the sigB operon. The first one is located in the upstream of the first gene of the operon, and second one is located in between fourth and fifth genes. Therefore, two different transcripts cause this pattern. (rsbV in this operon was not measured in the microarray experiments, so the region of this gene is not colored.) (C) The clpC operon. The transcription of this operon is basically promoted by sigma B, while the last two genes (sms and yacK) were reported to be also transcribed by sigma M.

Mentions: Figure 6 illustrates the levels of co-expression of genes comprising an operon with possible overlapped TUs. Boxes colored from blue to red, corresponding to increasing values of the correlation coefficients, indicate the levels of co-expression. They are arranged in the order of genes on the genome. As a simple case, suppose that there is an operon with two different sized TUs (Figure 6A). The longer TU has an additional two genes compared to the shorter one but both start from the same gene. In this case, the gene pairs crossing the boundary between the shorter and longer TUs will be correlated, but the other gene pairs should be more strongly correlated (Figure 6A).


Characterization of relationships between transcriptional units and operon structures in Bacillus subtilis and Escherichia coli.

Okuda S, Kawashima S, Kobayashi K, Ogasawara N, Kanehisa M, Goto S - BMC Genomics (2007)

Co-expression profile of operons: the schematic model of the operon diversity and its examples. (A) Schematic model of a diverse operon. In this model, we assume that there is a longer TU and a shorter TU. Arrows indicate the region transcribed as a TU. Open boxes to the side and above the grid indicate genes. Each box in the grid indicates the level of correlation of gene expression as colors from blue to red correspond to the correlation coefficients. The gene pairs without the TU boundary should show strong correlation with vivid red color. On the other hand, gene pairs across the boundary should show a slightly weaker correlation with orange color. (B) The sigB operon. There are two promoters in the sigB operon. The first one is located in the upstream of the first gene of the operon, and second one is located in between fourth and fifth genes. Therefore, two different transcripts cause this pattern. (rsbV in this operon was not measured in the microarray experiments, so the region of this gene is not colored.) (C) The clpC operon. The transcription of this operon is basically promoted by sigma B, while the last two genes (sms and yacK) were reported to be also transcribed by sigma M.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC1808063&req=5

Figure 6: Co-expression profile of operons: the schematic model of the operon diversity and its examples. (A) Schematic model of a diverse operon. In this model, we assume that there is a longer TU and a shorter TU. Arrows indicate the region transcribed as a TU. Open boxes to the side and above the grid indicate genes. Each box in the grid indicates the level of correlation of gene expression as colors from blue to red correspond to the correlation coefficients. The gene pairs without the TU boundary should show strong correlation with vivid red color. On the other hand, gene pairs across the boundary should show a slightly weaker correlation with orange color. (B) The sigB operon. There are two promoters in the sigB operon. The first one is located in the upstream of the first gene of the operon, and second one is located in between fourth and fifth genes. Therefore, two different transcripts cause this pattern. (rsbV in this operon was not measured in the microarray experiments, so the region of this gene is not colored.) (C) The clpC operon. The transcription of this operon is basically promoted by sigma B, while the last two genes (sms and yacK) were reported to be also transcribed by sigma M.
Mentions: Figure 6 illustrates the levels of co-expression of genes comprising an operon with possible overlapped TUs. Boxes colored from blue to red, corresponding to increasing values of the correlation coefficients, indicate the levels of co-expression. They are arranged in the order of genes on the genome. As a simple case, suppose that there is an operon with two different sized TUs (Figure 6A). The longer TU has an additional two genes compared to the shorter one but both start from the same gene. In this case, the gene pairs crossing the boundary between the shorter and longer TUs will be correlated, but the other gene pairs should be more strongly correlated (Figure 6A).

Bottom Line: Consequently, we found that the levels of gene co-regulation was correlated to intergenic distances and gene expression levels.Most interestingly, we found that functional associations in SOPs were more observed in the environmental and genetic information processes.In addition, such differences may play an important role in the evolution of gene order across genomes.

View Article: PubMed Central - HTML - PubMed

Affiliation: Bioinformatics Center, Institute for Chemical Research, Kyoto University, Gokasho, Uji, Kyoto 611-0011, Japan. okuda@kuicr.kyoto-u.ac.jp <okuda@kuicr.kyoto-u.ac.jp>

ABSTRACT

Background: Operon structures play an important role in transcriptional regulation in prokaryotes. However, there have been fewer studies on complicated operon structures in which the transcriptional units vary with changing environmental conditions. Information about such complicated operons is helpful for predicting and analyzing operon structures, as well as understanding gene functions and transcriptional regulation.

Results: We systematically analyzed the experimentally verified transcriptional units (TUs) in Bacillus subtilis and Escherichia coli obtained from ODB and RegulonDB. To understand the relationships between TUs and operons, we defined a new classification system for adjacent gene pairs, divided into three groups according to the level of gene co-regulation: operon pairs (OP) belong to the same TU, sub-operon pairs (SOP) that are at the transcriptional boundaries within an operon, and non-operon pairs (NOP) belonging to different operons. Consequently, we found that the levels of gene co-regulation was correlated to intergenic distances and gene expression levels. Additional analysis revealed that they were also correlated to the levels of conservation across about 200 prokaryotic genomes. Most interestingly, we found that functional associations in SOPs were more observed in the environmental and genetic information processes.

Conclusion: Complicated operon structures were correlated with genome organization and gene expression profiles. Such intricately regulated operons allow functional differences depending on environmental conditions. These regulatory mechanisms are helpful in accommodating the variety of changes that happen around the cell. In addition, such differences may play an important role in the evolution of gene order across genomes.

Show MeSH
Related in: MedlinePlus