This Article
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Condon, C.
Right arrow Articles by Squires, C. L.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Condon, C.
Right arrow Articles by Squires, C. L.

 Previous Article  |  Next Article 

Microbiol. Rev., 12 1995, 623-645, Vol 59, No. 4
Copyright © 1995, American Society for Microbiology

Control of rRNA transcription in Escherichia coli

C Condon, C Squires and CL Squires
Department of Molecular Biology and Microbiology, Tufts University Health Sciences Campus, Boston, Massachusetts 02111, USA.

The control of rRNA synthesis in response to both extra- and intracellular signals has been a subject of interest to microbial physiologists for nearly four decades, beginning with the observations that Salmonella typhimurium cells grown on rich medium are larger and contain more RNA than those grown on poor medium. This was followed shortly by the discovery of the stringent response in Escherichia coli, which has continued to be the organism of choice for the study of rRNA synthesis. In this review, we summarize four general areas of E. coli rRNA transcription control: stringent control, growth rate regulation, upstream activation, and anti-termination. We also cite similar mechanisms in other bacteria and eukaryotes. The separation of growth rate-dependent control of rRNA synthesis from stringent control continues to be a subject of controversy. One model holds that the nucleotide ppGpp is the key effector for both mechanisms, while another school holds that it is unlikely that ppGpp or any other single effector is solely responsible for growth rate-dependent control. Recent studies on activation of rRNA synthesis by cis-acting upstream sequences has led to the discovery of a new class of promoters that make contact with RNA polymerase at a third position, called the UP element, in addition to the well-known -10 and -35 regions. Lastly, clues as to the role of antitermination in rRNA operons have begun to appear. Transcription complexes modified at the antiterminator site appear to elongate faster and are resistant to the inhibitory effects of ppGpp during the stringent response.


This article has been cited by other articles:

  • Tambong, J. T., Xu, R., Bromfield, E. S. P. (2009). Intercistronic heterogeneity of the 16S-23S rRNA spacer region among Pseudomonas strains isolated from subterranean seeds of hog peanut (Amphicarpa bracteata). Microbiology 155: 2630-2640 [Abstract] [Full Text]  
  • Prasch, S., Jurk, M., Washburn, R. S., Gottesman, M. E., Wohrl, B. M., Rosch, P. (2009). RNA-binding specificity of E. coli NusA. Nucleic Acids Res 37: 4736-4742 [Abstract] [Full Text]  
  • Cabrera, J. E., Cagliero, C., Quan, S., Squires, C. L., Jin, D. J. (2009). Active Transcription of rRNA Operons Condenses the Nucleoid in Escherichia coli: Examining the Effect of Transcription on Nucleoid Structure in the Absence of Transertion. J. Bacteriol. 191: 4180-4185 [Abstract] [Full Text]  
  • Klumpp, S., Hwa, T. (2008). Stochasticity and traffic jams in the transcription of ribosomal RNA: Intriguing role of termination and antitermination. Proc. Natl. Acad. Sci. USA 105: 18159-18164 [Abstract] [Full Text]  
  • Baaklini, I., Usongo, V., Nolent, F., Sanscartier, P., Hraiky, C., Drlica, K., Drolet, M. (2008). Hypernegative Supercoiling Inhibits Growth by Causing RNA Degradation. J. Bacteriol. 190: 7346-7356 [Abstract] [Full Text]  
  • Arnvig, K. B., Zeng, S., Quan, S., Papageorge, A., Zhang, N., Villapakkam, A. C., Squires, C. L. (2008). Evolutionary Comparison of Ribosomal Operon Antitermination Function. J. Bacteriol. 190: 7251-7257 [Abstract] [Full Text]  
  • Lewis, P. J., Doherty, G. P., Clarke, J. (2008). Transcription factor dynamics. Microbiology 154: 1837-1844 [Abstract] [Full Text]  
  • Greive, S. J., Weitzel, S. E., Goodarzi, J. P., Main, L. J., Pasman, Z., von Hippel, P. H. (2008). Monitoring RNA transcription in real time by using surface plasmon resonance. Proc. Natl. Acad. Sci. USA 105: 3315-3320 [Abstract] [Full Text]  
  • DeVito, J. A. (2008). Recombineering with tolC as a Selectable/Counter-selectable Marker: remodeling the rRNA Operons of Escherichia coli. Nucleic Acids Res 36: e4-e4 [Abstract] [Full Text]  
  • Wang, J., Gardiol, N., Burr, T., Salmond, G. P. C., Welch, M. (2007). RelA-Dependent (p)ppGpp Production Controls Exoenzyme Synthesis in Erwinia carotovora subsp. atroseptica. J. Bacteriol. 189: 7643-7652 [Abstract] [Full Text]  
  • Matsuda, K., Tsuji, H., Asahara, T., Kado, Y., Nomoto, K. (2007). Sensitive Quantitative Detection of Commensal Bacteria by rRNA-Targeted Reverse Transcription-PCR. Appl. Environ. Microbiol. 73: 32-39 [Abstract] [Full Text]  
  • Mallik, P., Paul, B. J., Rutherford, S. T., Gourse, R. L., Osuna, R. (2006). DksA Is Required for Growth Phase-Dependent Regulation, Growth Rate-Dependent Control, and Stringent Control of fis Expression in Escherichia coli.. J. Bacteriol. 188: 5775-5782 [Abstract] [Full Text]  
  • Doherty, G. P., Meredith, D. H., Lewis, P. J. (2006). Subcellular Partitioning of Transcription Factors in Bacillus subtilis. J. Bacteriol. 188: 4101-4110 [Abstract] [Full Text]  
  • Mani, N., Dupuy, B., Sonenshein, A. L. (2006). Isolation of RNA Polymerase from Clostridium difficile and Characterization of Glutamate Dehydrogenase and rRNA Gene Promoters In Vitro and In Vivo. J. Bacteriol. 188: 96-102 [Abstract] [Full Text]  
  • Fiola, K., Perreault, J.-P., Cousineau, B. (2006). Gene Targeting in the Gram-Positive Bacterium Lactococcus lactis, Using Various Delta Ribozymes. Appl. Environ. Microbiol. 72: 869-879 [Abstract] [Full Text]  
  • Greive, S. J., Lins, A. F., von Hippel, P. H. (2005). Assembly of an RNA-Protein Complex: BINDING OF NusB AND NusE (S10) PROTEINS TO boxA RNA NUCLEATES THE FORMATION OF THE ANTITERMINATION COMPLEX INVOLVED IN CONTROLLING rRNA TRANSCRIPTION IN ESCHERICHIA COLI. J. Biol. Chem. 280: 36397-36408 [Abstract] [Full Text]  
  • Cytryn, E., van Rijn, J., Schramm, A., Gieseke, A., de Beer, D., Minz, D. (2005). Identification of Bacteria Potentially Responsible for Oxic and Anoxic Sulfide Oxidation in Biofilters of a Recirculating Mariculture System. Appl. Environ. Microbiol. 71: 6134-6141 [Abstract] [Full Text]  
  • Tucker, D. L., Karouia, F., Wang, J., Luo, Y., Li, T.-B., Willson, R. C., Fofanov, Y., Fox, G. E. (2005). Effect of an Artificial RNA Marker on Gene Expression in Escherichia coli. Appl. Environ. Microbiol. 71: 4156-4159 [Abstract] [Full Text]  
  • Ramamoorthy, R., McClain, N. A., Gautam, A., Scholl-Meeker, D. (2005). Expression of the bmpB Gene of Borrelia burgdorferi Is Modulated by Two Distinct Transcription Termination Events. J. Bacteriol. 187: 2592-2600 [Abstract] [Full Text]  
  • Quan, S., Zhang, N., French, S., Squires, C. L. (2005). Transcriptional Polarity in rRNA Operons of Escherichia coli nusA and nusB Mutant Strains. J. Bacteriol. 187: 1632-1638 [Abstract] [Full Text]  
  • Arnvig, K. B., Gopal, B., Papavinasasundaram, K. G., Cox, R. A., Colston, M. J. (2005). The mechanism of upstream activation in the rrnB operon of Mycobacterium smegmatis is different from the Escherichia coli paradigm. Microbiology 151: 467-473 [Abstract] [Full Text]  
  • Menendez, M. d. C., Rebollo, M. J., Nunez, M. d. C., Cox, R. A., Garcia, M. J. (2005). Analysis of the Precursor rRNA Fractions of Rapidly Growing Mycobacteria: Quantification by Methods That Include the Use of a Promoter (rrnA P1) as a Novel Standard. J. Bacteriol. 187: 534-543 [Abstract] [Full Text]  
  • Arnvig, K. B., Pennell, S., Gopal, B., Colston, M. J. (2004). A high-affinity interaction between NusA and the rrn nut site in Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. USA 101: 8325-8330 [Abstract] [Full Text]  
  • Carter, H. D., Svetlov, V., Artsimovitch, I. (2004). Highly Divergent RfaH Orthologs from Pathogenic Proteobacteria Can Substitute for Escherichia coli RfaH both In Vivo and In Vitro. J. Bacteriol. 186: 2829-2840 [Abstract] [Full Text]  
  • King, R. A., Weisberg, R. A. (2003). Suppression of Factor-Dependent Transcription Termination by Antiterminator RNA. J. Bacteriol. 185: 7085-7091 [Abstract] [Full Text]  
  • Battermann, A., Disse-Kromker, C., Dreiseikelmann, B. (2003). A functional plasmid-borne rrn operon in soil isolates belonging to the genus Paracoccus. Microbiology 149: 3587-3593 [Abstract] [Full Text]  
  • Schneider, D. A., Gourse, R. L. (2003). Changes in Escherichia coli rRNA Promoter Activity Correlate with Changes in Initiating Nucleoside Triphosphate and Guanosine 5' Diphosphate 3'-Diphosphate Concentrations after Induction of Feedback Control of Ribosome Synthesis. J. Bacteriol. 185: 6185-6191 [Abstract] [Full Text]  
  • Epshtein, V., Nudler, E. (2003). Cooperation Between RNA Polymerase Molecules in Transcription Elongation. Science 300: 801-805 [Abstract] [Full Text]  
  • Lee, H., Vazquez-Laslop, N., Klyachko, K. A., Neyfakh, A. A. (2003). Isolation of Antibiotic Hypersusceptibility Mutants of Acinetobacter spp. by Selection for DNA Release. Antimicrob. Agents Chemother. 47: 1267-1274 [Abstract] [Full Text]  
  • Corbella, M. E., Puyet, A. (2003). Real-Time Reverse Transcription-PCR Analysis of Expression of Halobenzoate and Salicylate Catabolism-Associated Operons in Two Strains of Pseudomonas aeruginosa. Appl. Environ. Microbiol. 69: 2269-2275 [Abstract] [Full Text]  
  • Kabadjova, P., Dousset, X., Le Cam, V., Prevost, H. (2002). Differentiation of Closely Related Carnobacterium Food Isolates Based on 16S-23S Ribosomal DNA Intergenic Spacer Region Polymorphism. Appl. Environ. Microbiol. 68: 5358-5366 [Abstract] [Full Text]  
  • Bugrysheva, J., Dobrikova, E. Y., Godfrey, H. P., Sartakova, M. L., Cabello, F. C. (2002). Modulation of Borrelia burgdorferi Stringent Response and Gene Expression during Extracellular Growth with Tick Cells. Infect. Immun. 70: 3061-3067 [Abstract] [Full Text]  
  • Aiyar, S. E., Gaal, T., Gourse, R. L. (2002). rRNA Promoter Activity in the Fast-Growing Bacterium Vibrio natriegens. J. Bacteriol. 184: 1349-1358 [Abstract] [Full Text]  
  • Barker, M. M., Gourse, R. L. (2001). Regulation of rRNA Transcription Correlates with Nucleoside Triphosphate Sensing. J. Bacteriol. 183: 6315-6323 [Abstract] [Full Text]  
  • Clementino, M. M., de Filippis, I., Nascimento, C. R., Branquinho, R., Rocha, C. L., Martins, O. B. (2001). PCR Analyses of tRNA Intergenic Spacer, 16S-23S Internal Transcribed Spacer, and Randomly Amplified Polymorphic DNA Reveal Inter- and Intraspecific Relationships of Enterobacter cloacae Strains. J. Clin. Microbiol. 39: 3865-3870 [Abstract] [Full Text]  
  • Garcia-Martinez, J., Bescos, I., Rodriguez-Sala, J. J., Rodriguez-Valera, F. (2001). RISSC: a novel database for ribosomal 16S-23S RNA genes spacer regions. Nucleic Acids Res 29: 178-180 [Abstract] [Full Text]  
  • NOMURA, M. (2001). Ribosomal RNA Genes, RNA Polymerases, Nucleolar Structures, and Synthesis of rRNA in the Yeast Saccharomyces cerevisiae. Cold Spring Harb Symp Quant Biol 66: 555-566 [Abstract]  
  • Kempsell, K. E., Cox, C. J., Hurle, M., Wong, A., Wilkie, S., Zanders, E. D., Gaston, J. S. H., Crowe, J. S. (2000). Reverse Transcriptase-PCR Analysis of Bacterial rRNA for Detection and Characterization of Bacterial Species in Arthritis Synovial Tissue. Infect. Immun. 68: 6012-6026 [Abstract] [Full Text]  
  • Iteman, I., Rippka, R., Tandeau de Marsac, N., Herdman, M. (2000). Comparison of conserved structural and regulatory domains within divergent 16S rRNA-23S rRNA spacer sequences of cyanobacteria. Microbiology 146: 1275-1286 [Abstract] [Full Text]  
  • Bartlett, M. S., Gaal, T., Ross, W., Gourse, R. L. (2000). Regulation of rRNA Transcription Is Remarkably Robust: FIS Compensates for Altered Nucleoside Triphosphate Sensing by Mutant RNA Polymerases at Escherichia coli rrn P1 Promoters. J. Bacteriol. 182: 1969-1977 [Abstract] [Full Text]  
  • Voulgaris, J., Pokholok, D., Holmes, W. M., Squires, C., Squires, C. L. (2000). The Feedback Response of Escherichia coli rRNA Synthesis Is Not Identical to the Mechanism of Growth Rate-Dependent Control. J. Bacteriol. 182: 536-539 [Abstract] [Full Text]  
  • Yanofsky, C. (2000). Transcription Attenuation: Once Viewed as a Novel Regulatory Strategy. J. Bacteriol. 182: 1-8 [Full Text]  
  • O'Connell, K. P., Gustafson, A. M., Lehmann, M. D., Thomashow, M. F. (2000). Identification of Cold Shock Gene Loci in Sinorhizobium meliloti by Using a luxAB Reporter Transposon. Appl. Environ. Microbiol. 66: 401-405 [Abstract] [Full Text]  
  • Nomura, M. (1999). Regulation of Ribosome Biosynthesis in Escherichia coli and Saccharomyces cerevisiae: Diversity and Common Principles. J. Bacteriol. 181: 6857-6864 [Full Text]  
  • Gonzalez-y-Merchand, J. A., Colston, M. J., Cox, R. A. (1999). Effects of Growth Conditions on Expression of Mycobacterial murA and tyrS Genes and Contributions of Their Transcripts to Precursor rRNA Synthesis. J. Bacteriol. 181: 4617-4627 [Abstract] [Full Text]  
  • Voulgaris, J., French, S., Gourse, R. L., Squires, C., Squires, C. L. (1999). Increased rrn Gene Dosage Causes Intermittent Transcription of rRNA in Escherichia coli. J. Bacteriol. 181: 4170-4175 [Abstract] [Full Text]  
  • Verma, A., Sampla, A. K., Tyagi, J. S. (1999). Mycobacterium tuberculosis rrn Promoters: Differential Usage and Growth Rate-Dependent Control. J. Bacteriol. 181: 4326-4333 [Abstract] [Full Text]  
  • Asai, T., Condon, C., Voulgaris, J., Zaporojets, D., Shen, B., Al-Omar, M., Squires, C., Squires, C. L. (1999). Construction and Initial Characterization of Escherichia coli Strains with Few or No Intact Chromosomal rRNA Operons. J. Bacteriol. 181: 3803-3809 [Abstract] [Full Text]  
  • Chun, J., Huq, A., Colwell, R. R. (1999). Analysis of 16S-23S rRNA Intergenic Spacer Regions of Vibrio cholerae and Vibrio mimicus. Appl. Environ. Microbiol. 65: 2202-2208 [Abstract] [Full Text]  
  • Weisberg, R. A., Gottesman, M. E. (1999). Processive Antitermination. J. Bacteriol. 181: 359-367 [Full Text]  
  • Scoarughi, G. L., Cimmino, C., Donini, P. (1999). Helicobacter pylori: a Eubacterium Lacking the Stringent Response. J. Bacteriol. 181: 552-555 [Abstract] [Full Text]  
  • Luz, S. P., Rodríguez-Valera, F., Lan, R., Reeves, P. R. (1998). Variation of the Ribosomal Operon 16S-23S Gene Spacer Region in Representatives of Salmonella enterica Subspecies. J. Bacteriol. 180: 2144-2151 [Abstract] [Full Text]  
  • Mogridge, J., Greenblatt, J. (1998). Specific Binding of Escherichia coli Ribosomal Protein S1 to boxA Transcriptional Antiterminator RNA. J. Bacteriol. 180: 2248-2252 [Abstract] [Full Text]  
  • Stevenson, B. S., Schmidt, T. M. (1998). Growth Rate-Dependent Accumulation of RNA from Plasmid-Borne rRNA Operons in Escherichia coli. J. Bacteriol. 180: 1970-1972 [Abstract] [Full Text]  
  • Appleman, J. A., Ross, W., Salomon, J., Gourse, R. L. (1998). Activation of Escherichia coli rRNA Transcription by FIS during a Growth Cycle. J. Bacteriol. 180: 1525-1532 [Abstract] [Full Text]  
  • Hartzog, G. A., Wada, T., Handa, H., Winston, F. (1998). Evidence that Spt4, Spt5, and Spt6 control transcription elongation by RNA polymerase II in Saccharomyces cerevisiae. Genes Dev. 12: 357-369 [Abstract] [Full Text]  
  • GOURSE, R.L., GAAL, T., AIYAR, S.E., BARKER, M.M., ESTREM, S.T., HIRVONEN, C.A., ROSS, W. (1998). Strength and Regulation without Transcription Factors: Lessons from Bacterial rRNA Promoters. Cold Spring Harb Symp Quant Biol 63: 131-140 [Abstract]  
  • Gaal, T., Bartlett, M. S., Ross, W., Turnbough Jr., C. L., Gourse, R. L. (1997). Transcription Regulation by Initiating NTP Concentration: rRNA Synthesis in Bacteria. Science 278: 2092-2097 [Abstract] [Full Text]  
  • Iratni, R., Diederich, L., Harrak, H., Bligny, M., Lerbs-Mache, S. (1997). Organ-specific Transcription of the rrn Operon in Spinach Plastids. J. Biol. Chem. 272: 13676-13682 [Abstract] [Full Text]  
  • Vogel, U., Jensen, K. F. (1997). NusA Is Required for Ribosomal Antitermination and for Modulation of the Transcription Elongation Rate of both Antiterminated RNA and mRNA. J. Biol. Chem. 272: 12265-12271 [Abstract] [Full Text]  
  • Masse, E., Phoenix, P., Drolet, M. (1997). DNA Topoisomerases Regulate R-loop Formation during Transcription of the rrnB Operon in Escherichia coli. J. Biol. Chem. 272: 12816-12823 [Abstract] [Full Text]  
  • Carlsson, J. (1997). Bacterial Metabolism in Dental Biofilms. ADR 11: 75-80 [Abstract]  
  • Gaudino, R. J., Pikaard, C. S. (1997). Cytokinin Induction of RNA Polymerase I Transcription in Arabidopsis thaliana. J. Biol. Chem. 272: 6799-6804 [Abstract] [Full Text]  
  • Tedin, K., Blasi, U. (1996). The RNA Chain Elongation Rate of the lambda Late mRNA Is Unaffected by High Levels of ppGpp in the Absence of Amino Acid Starvation. J. Biol. Chem. 271: 17675-17686 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»