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

Genome Biology - Tập 7 - Trang 1-11 - 2006
Ruth Hershberg1, Hanah Margalit1
1Department of Molecular Genetics and Biotechnology, Faculty of Medicine, The Hebrew University of Jerusalem, Jerusalem, Israel

Tóm tắt

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. 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. 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.

Tài liệu tham khảo

Carroll SB: Evolution at two levels: on genes and form. PLoS Biol. 2005, 3: e245-10.1371/journal.pbio.0030245. Olson MV, Varki A: Sequencing the chimpanzee genome: insights into human evolution and disease. Nat Rev Genet. 2003, 4: 20-28. 10.1038/nrg981. Wagner R: Transcription Regulation in Prokaryotes. 2000, Oxford: Oxford University press, 1 Browning DF, Busby SJ: The regulation of bacterial transcription initiation. Nat Rev Microbiol. 2004, 2: 57-65. 10.1038/nrmicro787. Ihmels J, Bergmann S, Gerami-Nejad M, Yanai I, McClellan M, Berman J, Barkai N: Rewiring of the yeast transcriptional network through the evolution of motif usage. Science. 2005, 309: 938-940. 10.1126/science.1113833. Gasch AP, Moses AM, Chiang DY, Fraser HB, Berardini M, Eisen MB: Conservation and evolution of cis-regulatory systems in ascomycete fungi. PLoS Biol. 2004, 2: e398-10.1371/journal.pbio.0020398. Tanay A, Regev A, Shamir R: Conservation and evolvability in regulatory networks: the evolution of ribosomal regulation in yeast. Proc Natl Acad Sci USA. 2005, 102: 7203-7208. 10.1073/pnas.0502521102. Teichmann SA, Babu MM: Gene regulatory network growth by duplication. Nat Genet. 2004, 36: 492-496. 10.1038/ng1340. Ma HW, Kumar B, Ditges U, Gunzer F, Buer J, Zeng AP: An extended transcriptional regulatory network of Escherichia coli and analysis of its hierarchical structure and network motifs. Nucleic Acids Res. 2004, 32: 6643-6649. 10.1093/nar/gkh1009. Madan Babu M, Teichmann SA, Aravind L: Evolutionary dynamics of prokaryotic transcriptional regulatory networks. J Mol Biol. 2006, 358: 614-633. 10.1016/j.jmb.2006.02.019. Martinez-Antonio A, Collado-Vides J: Identifying global regulators in transcriptional regulatory networks in bacteria. Curr Opin Microbiol. 2003, 6: 482-489. 10.1016/j.mib.2003.09.002. Struhl K: Fundamentally different logic of gene regulation in eukaryotes and prokaryotes. Cell. 1999, 98: 1-4. 10.1016/S0092-8674(00)80599-1. Soutourina OA, Bertin PN: Regulation cascade of flagellar expression in Gram-negative bacteria. FEMS Microbiol Rev. 2003, 27: 505-523. 10.1016/S0168-6445(03)00064-0. Tominaga A, Lan R, Reeves PR: Evolutionary changes of the flhDC flagellar master operon in Shigella strains. J Bacteriol. 2005, 187: 4295-4302. 10.1128/JB.187.12.4295-4302.2005. Krieg N: Bergey's Manual of Systematic Bacteriology. 1984, Baltimore: Williams & Wilkins, 1: Giron JA: Expression of flagella and motility by Shigella. Mol Microbiol. 1995, 18: 63-75. 10.1111/j.1365-2958.1995.mmi_18010063.x. Dahl MK, Manson MD: Interspecific reconstitution of maltose transport and chemotaxis in Escherichia coli with maltose-binding protein from various enteric bacteria. J Bacteriol. 1985, 164: 1057-1063. Jin Q, Yuan Z, Xu J, Wang Y, Shen Y, Lu W, Wang J, Liu H, Yang J, Yang F, et al: Genome sequence of Shigella flexneri 2a: insights into pathogenicity through comparison with genomes of Escherichia coli K12 and O157. Nucleic Acids Res. 2002, 30: 4432-4441. 10.1093/nar/gkf566. Masse E, Gottesman S: A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli. Proc Natl Acad Sci USA. 2002, 99: 4620-4625. 10.1073/pnas.032066599. Atkinson MR, Ninfa AJ: Characterization of Escherichia coli glnL mutations affecting nitrogen regulation. J Bacteriol. 1992, 174: 4538-4548. Zhang A, Wassarman KM, Rosenow C, Tjaden BC, Storz G, Gottesman S: Global analysis of small RNA and mRNA targets of Hfq. Mol Microbiol. 2003, 50: 1111-1124. 10.1046/j.1365-2958.2003.03734.x. Beaud D, Tailliez P, Anba-Mondoloni J: Genetic characterization of the beta-glucuronidase enzyme from a human intestinal bacterium, Ruminococcus gnavus. Microbiology. 2005, 151: 2323-2330. 10.1099/mic.0.27712-0. Salgado H, Gama-Castro S, Peralta-Gil M, Diaz-Peredo E, Sanchez-Solano F, Santos-Zavaleta A, Martinez-Flores I, Jimenez-Jacinto V, Bonavides-Martinez C, Segura-Salazar J, et al: RegulonDB (version 5.0): Escherichia coli K-12 transcriptional regulatory network, operon organization, and growth conditions. Nucleic Acids Res. 2006, 34: D394-397. 10.1093/nar/gkj156. Keseler IM, Collado-Vides J, Gama-Castro S, Ingraham J, Paley S, Paulsen IT, Peralta-Gil M, Karp PD: EcoCyc: a comprehensive database resource for Escherichia coli. Nucleic Acids Res. 2005, 33: D334-337. 10.1093/nar/gki108. Rudd KE: EcoGene: a genome sequence database for Escherichia coli K-12. Nucleic Acids Res. 2000, 28: 60-64. 10.1093/nar/28.1.60. NCBI ftp Server. [http://www.ncbi.nlm.nih.gov/Ftp/] Pearson WR, Lipman DJ: Improved tools for biological sequence comparison. Proc Natl Acad Sci USA. 1988, 85: 2444-2448. 10.1073/pnas.85.8.2444.