Conserved features of coordinately regulated<i>E.coli</i>promoters

Travers, Andrew

doi:10.1093/nar/12.6.2605

Cited by 162 publications

(117 citation statements)

References 41 publications

(30 reference statements)

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“…The rRNA P1 promoters have previously been suggested to harbor important regulatory elements for stringent control and growth rate-dependent regulation (23). Analysis of the sequence downstream of the -10 region of the trmA promoter revealed a sequence similar to the previously suggested discrimninatory region for stringent and growth rate-dependent genes (46) in accordance with the present data and the previously observed regulation of trmA gene expression (34). Analysis of the sequence extending upstream from the -10 region showed an additional sequence homology to rRNA P1 promoters.…”

Section: Discussionsupporting

confidence: 92%

“…4). Immediately downstream from the -10 region of the trmA promoter is a sequence, CGCCGCG, similar to the discriminatory region for stringently controlled promoters (46), although the trmA promoter extends the GC base pairing with 3 extra GC bp (GCG) compared with the 2 bp (ACC) of the rRNA P1 promoter. In addition, we found a conserved sequence motif, TCCC, immediately upstream from the -10 region, previously found only in the P1 promoters of rRNA genes and some tRNA promoters (Fig.…”

Section: Resultsmentioning

confidence: 99%

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The trmA promoter has regulatory features and sequence elements in common with the rRNA P1 promoter family of Escherichia coli

et al. 1991

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The tRNA(m5U54)methyltransferase, whose structural gene is designated trmA, catalyzes the formation of 5-methyluridine in position 54 of all tRNA species in Escherichia coli. The synthesis of this enzyme has previously been shown to be both growth rate dependent and stringently regulated, suggesting regulatory features similar to those of rRNA. We have determined the complete nucleotide sequence of the trmA operon in E. coli and the sequence of the trmA promoter region in SalmoneUa typhimurium and also analyzed the transcriptional regulation of the gene. The trmA and the btuB (encoding the vitamin B12 outer membrane receptor protein) promoters are divergent promoters separated by 102 bp between the transcriptional start sites. The trmA promoters of both E. coli and S. typhimurium share promoter elements with the rRNA P1 promoter. The sequence downstream from the -10 region of the trmA promoter is homologous to the discriminatory region found in stringently regulated promoters. Next to and upstream from the -10 region is a sequence, TCCC, in the trmA promoter that is present in all of the seven rRNA P1 promoters and in some tRNA promoters but not in any other Co70 promoter. However, a similar motif is also found in promoters transcribed by the heat shock sigma factor CJ32. The trmA gene is transcribed as a monocistronic operon, and the 3' end of the transcript is shown to be located downstream from a dyad symmetry region not followed by a poly(U) stretch. Using a trmA-cat operon fusion, we show that the growth rate-dependent regulation of trmA resembles that of rRNA and operates at the level of transcription.

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Section: Discussionsupporting

confidence: 92%

Section: Resultsmentioning

confidence: 99%

The trmA promoter has regulatory features and sequence elements in common with the rRNA P1 promoter family of Escherichia coli

et al. 1991

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“…The G+C-rich sequence just downstream of the -10 hexamer (termed the discriminator [44]) has been implicated previously in growth rate regulation on the basis of sequence conservation among stable RNA promoters (11,43) and on the basis of measurements at different growth rates of a promoter with multiple mutations in this region (46). This region has also been implicated in the stringent response in vivo (24) and in responses to ppGpp in vitro (32,42).…”

Section: Discussionmentioning

confidence: 99%

Identification of promoter mutants defective in growth-rate-dependent regulation of rRNA transcription in Escherichia coli

et al. 1989

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We measured the activities of 50 operon fusions from a collection of mutant and wild-type rrnB P1 (rrnBlp in the nomenclature of B. J. Bachmann and K. B. Low [Microbiol. Rev. 44:1-56, 1980]) promoters under different nutritional conditions in order to analyze the DNA sequence determinants of growth rate-dependent regulation of rRNA transcription in Escherichia coli. Mutants which deviated from the wild-type -10 or -35 hexamers or from the wild-type 16-base-pair spacer length between the hexamers were unregulated, regardless of whether the mutations brought the promoters closer to the E. coli promoter consensus sequence and increased activity or whether the changes took the promoters further away from the consensus and reduced activity. These data suggest that rRNA promoters have evolved to maintain their regulatory abilities rather than to maximize promoter strength. Some double substitutions outside the consensus hexamers were almost completely unregulated, while single substitutions at several positions outside the -10 and -35 consensus hexamers exerted smaller but significant effects on regulation. These studies suggest roles for specific promoter sequences and/or structures in interactions with regulatory molecules and suggest experimental tests for models of rRNA regulation.Ribosome synthesis rates in Escherichia coli are a direct function of rRNA transcription rates under most growth conditions (26,34). In order to meet the cell's requirements for protein synthesis, cells transcribe rRNA and tRNA at approximately the square of the growth rate, a phenomenon termed growth rate-dependent regulation (29).The mechanism responsible for growth rate control remains unclear. Previously, it was shown that a negative feedback system is responsible for rRNA and tRNA regulation (15-17, 28, 39) and that the system responds to the level of ribosomes that are capable of translation (10, 49). The magnitude of the signal made in response to the cell's translational capacity varies with the nutritional state of the culture. The identity of the signal is not known, although guanosine tetraphosphate (ppGpp) has been implicated as playing some role because of the virtually perfect inverse correlation between stable RNA synthesis and ppGpp concentration (36).The target of the signal, whatever its identity, has been shown in at least three of the seven rRNA operons to be P1, the more upstream of the two rRNA promoters (rrnB and rrnE [15]; rrnA [37] there is a region called the upstream activation sequence (UAS), which is required for maximal promoter activity (4,15,23).Mutations have been targeted to specific sites in the promoters rrnB P1 and tyrT, and activities resulting from the fusion of the mutant promoters to "reporter" genes have been measured under different growth conditions (15,46). Such experiments have implicated DNA sequences required for growth rate-dependent control in the region between -20 and -50 (15) and in the region just downstream of the -10 hexamer (46). The mutations examined in both studies contained ...

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“…P2 also contains an UP element; however, it has a much smaller effect on promoter activity than that exerted by the P1 UP element (Ross et al, 1993). Both P1 and P2 contain a G+C rich region (Travers, 1984) between the 210 and the transcription start site that is required for stringent control (Josaitis et al, 1995;Murray et al, 2003).…”

Section: Introductionmentioning

confidence: 99%

Comparison of Bacteroides thetaiotaomicron and Escherichia coli 16S rRNA gene expression signals

2009

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There are barriers to cross-expression of genes between Bacteroides spp. and Escherichia coli. In this study, a lux-based reporter system was developed for Bacteroides and used to compare the promoter structure and function of a Bacteroides thetaiotaomicron 4001 (BT4001) 16S rRNA promoter with those of E. coli in vivo. Analysis of the BT4001 sequences upstream of the 16S rRNA gene revealed the same overall structure known for E. coli 16S rRNA promoters in that there were two promoters separated by~150 bp. However, the BT4001 16S rRNA promoter contains the proposed Bacteroides "7 and "33 consensus sequences instead of the E. coli "10 and "35 consensus sequences. The biological activity of various configurations of the BT4001 16S rRNA promoter was analysed. Experiments pairing the BT4001 16S rRNA promoter with an E. coli RBS, and vice-versa, confirmed that gene expression between the two species is restricted at the level of transcription. In Bacteroides, a difference in translation initiation also appears to limit expression of foreign genes.

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Conserved features of coordinately regulatedE.colipromoters

Cited by 162 publications

References 41 publications

The trmA promoter has regulatory features and sequence elements in common with the rRNA P1 promoter family of Escherichia coli

The trmA promoter has regulatory features and sequence elements in common with the rRNA P1 promoter family of Escherichia coli

Identification of promoter mutants defective in growth-rate-dependent regulation of rRNA transcription in Escherichia coli

Comparison of Bacteroides thetaiotaomicron and Escherichia coli 16S rRNA gene expression signals

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