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Co-evolution of transcription factors and their targets depends on mode of regulation

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Genome Biology

BioMed Central

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      Abstract

      Analysis of transcription regulatory networks in γ-proteobacteria reveals that repressors co-evolve tightly with their target genes, whereas activators can be lost independently of their targets.

      Abstract

      Background

      Differences in the transcription regulation network are at the root of much of the phenotypic variation observed among organisms. These differences may be achieved either by changing the repertoire of regulators and/or their targets, or by rewiring the network. Following these changes and studying their logic is crucial for understanding the evolution of regulatory networks.

      Results

      We use the well characterized transcription regulatory network of Escherichia coli K12 and follow the evolutionary changes in the repertoire of regulators and their targets across a large number of fully sequenced γ-proteobacteria. By focusing on close relatives of E. coli K12, we study the dynamics of the evolution of transcription regulation across a relatively short evolutionary timescale. We show significant differences in the evolution of repressors and activators. Repressors are only lost from a genome once their targets have themselves been lost, or once the network has significantly rewired. In contrast, activators are often lost even when their targets remain in the genome. As a result, E. coli K12 repressors that regulate many targets are rarely absent from organisms that are closely related to E. coli K12, while activators with a similar number of targets are often absent in these organisms.

      Conclusion

      We demonstrate that the mode of regulation exerted by transcription factors has a strong effect on their evolution. Repressors co-evolve tightly with their target genes. In contrast, activators can be lost independently of their targets. In fact, loss of an activator can lead to efficient shutdown of an unnecessary pathway.

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      Most cited references 26

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      We have developed three computer programs for comparisons of protein and DNA sequences. They can be used to search sequence data bases, evaluate similarity scores, and identify periodic structures based on local sequence similarity. The FASTA program is a more sensitive derivative of the FASTP program, which can be used to search protein or DNA sequence data bases and can compare a protein sequence to a DNA sequence data base by translating the DNA data base as it is searched. FASTA includes an additional step in the calculation of the initial pairwise similarity score that allows multiple regions of similarity to be joined to increase the score of related sequences. The RDF2 program can be used to evaluate the significance of similarity scores using a shuffling method that preserves local sequence composition. The LFASTA program can display all the regions of local similarity between two sequences with scores greater than a threshold, using the same scoring parameters and a similar alignment algorithm; these local similarities can be displayed as a "graphic matrix" plot or as individual alignments. In addition, these programs have been generalized to allow comparison of DNA or protein sequences based on a variety of alternative scoring matrices.
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        A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli.

        A small RNA, RyhB, was found as part of a genomewide search for novel small RNAs in Escherichia coli. The RyhB 90-nt RNA down-regulates a set of iron-storage and iron-using proteins when iron is limiting; it is itself negatively regulated by the ferric uptake repressor protein, Fur (Ferric uptake regulator). RyhB RNA levels are inversely correlated with mRNA levels for the sdhCDAB operon, encoding succinate dehydrogenase, as well as five other genes previously shown to be positively regulated by Fur by an unknown mechanism. These include two other genes encoding enzymes in the tricarboxylic acid cycle, acnA and fumA, two ferritin genes, ftnA and bfr, and a gene for superoxide dismutase, sodB. Fur positive regulation of all these genes is fully reversed in an ryhB mutant. Our results explain the previously observed inability of fur mutants to grow on succinate. RyhB requires the RNA-binding protein, Hfq, for activity. Sequences within RyhB are complementary to regions within each of the target genes, suggesting that RyhB acts as an antisense RNA. In sdhCDAB, the complementary region is at the end of the first gene of the sdhCDAB operon; full-length sdhCDAB message disappears and a truncated message, equivalent in size to the region upstream of the complementarity, is detected when RyhB is expressed. RyhB provides a mechanism for the cell to down-regulate iron-storage proteins and nonessential iron-containing proteins when iron is limiting, thus modulating intracellular iron usage to supplement mechanisms for iron uptake directly regulated by Fur.
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          The regulation of bacterial transcription initiation.

          Bacteria use their genetic material with great effectiveness to make the right products in the correct amounts at the appropriate time. Studying bacterial transcription initiation in Escherichia coli has served as a model for understanding transcriptional control throughout all kingdoms of life. Every step in the pathway between gene and function is exploited to exercise this control, but for reasons of economy, it is plain that the key step to regulate is the initiation of RNA-transcript formation.
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            Author and article information

            Affiliations
            [1]Department of Molecular Genetics and Biotechnology, Faculty of Medicine, The Hebrew University of Jerusalem, Jerusalem 91120, Israel
            Contributors
            Journal
            Genome Biol
            Genome Biology
            BioMed Central (London)
            1465-6906
            1465-6914
            2006
            19 July 2006
            : 7
            : 7
            : R62
            1779565
            gb-2006-7-7-r62
            16859509
            10.1186/gb-2006-7-7-r62
            Copyright © 2006 Hershberg and Margalit; licensee BioMed Central Ltd.

            This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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