Home LiteratureArticle Details
PMID: 7862645 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Stringent control and growth-rate-dependent control have nonidentical promoter sequence requirements.

Josaitis CA, Gaal T, Gourse RL

Abstract

Escherichia coli uses at least two regulatory systems, stringent control and growth-rate-dependent control, to adjust rRNA output to amino acid availability and the steady-state growth rate, respectively. We examined transcription from rrnB P1 promoters containing or lacking the cis-acting UP element and FIS protein binding sites after amino acid starvation. The "core promoter" responds to amino acid starvation like the full-length wild-type promoter; thus, neither the UP element nor FIS plays a role in stringent control. To clarify the relationship between growth-rate-dependent regulation and stringent control, we measured transcription from growth-rate-independent promoters during amino acid starvation. Four rrnB P1 mutants defective for growth-rate control and two other growth-rate-independent promoters (rrnB P2 and pS10) still displayed stringent regulation. Thus, the two systems have different promoter determinants, consistent with the idea that they function by different mechanisms. Two mutations disrupted stringent control of rrnB P1: (i) a multiple base change in the "discriminator" region between the -10 hexamer and the transcription start site and (ii) a double substitution making the promoter resemble the E sigma 70 consensus promoter. These results have important implications for the mechanisms of both stringent control and growth-rate-dependent control of rRNA transcription.

Related Genes
MeSH Terms
Base Sequence Cell Division/genetics DNA, Bacterial Escherichia coli/genetics,growth & development Gene Expression Regulation, Bacterial Molecular Sequence Data Mutation Promoter Regions, Genetic Transcription, Genetic rRNA Operon
Chemicals
DNA, Bacterial
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Josaitis C A
Department of Bacteriology, University of Wisconsin, Madison 53706.
Gaal T
Gourse R L
References (34)
34 references, click to expand
  1. Stringency without ppGpp accumulation.
    Nature. 1981 May 21;291(5812):256-8 PMID: 6164923
  2. Isolated P2 rRNA promoters of Escherichia coli are strong promoters that are subject to stringent control.
    J Mol Biol. 1994 Oct 21;243(2):152-6 PMID: 7523681
  3. Control of rRNA and tRNA syntheses in Escherichia coli by guanosine tetraphosphate.
    J Bacteriol. 1982 Sep;151(3):1261-8 PMID: 6179924
  4. Differential stringent control of the tandem E. coli ribosomal RNA promoters from the rrnA operon expressed in vivo in multicopy plasmids.
    Cell. 1983 Apr;32(4):1337-46 PMID: 6188537
  5. Regulation of the synthesis of ribosomes and ribosomal components.
    Annu Rev Biochem. 1984;53:75-117 PMID: 6206783
  6. A versatile plasmid system for the study of prokaryotic transcription signals in Escherichia coli.
    Gene. 1984 Oct;30(1-3):251-5 PMID: 6096219
  7. Genetically separable functional elements mediate the optimal expression and stringent regulation of a bacterial tRNA gene.
    Cell. 1985 Feb;40(2):319-26 PMID: 3881184
  8. Feedback regulation of rRNA and tRNA synthesis and accumulation of free ribosomes after conditional expression of rRNA genes.
    Proc Natl Acad Sci U S A. 1985 Feb;82(4):1069-73 PMID: 3156375
  9. Genetic dissection of stringent control and nutritional shift-up response of the Escherichia coli S10 ribosomal protein operon.
    J Mol Biol. 1985 Oct 20;185(4):701-12 PMID: 2414454
  10. DNA determinants of rRNA synthesis in E. coli: growth rate dependent regulation, feedback inhibition, upstream activation, antitermination.
    Cell. 1986 Jan 17;44(1):197-205 PMID: 2416474
  11. Feedback regulation of rRNA synthesis in Escherichia coli. Requirement for initiation factor IF2.
    J Mol Biol. 1987 Dec 5;198(3):383-92 PMID: 2448483
  12. Saturation mutagenesis of an Escherichia coli rRNA promoter and initial characterization of promoter variants.
    J Bacteriol. 1989 Sep;171(9):4852-61 PMID: 2527844
  13. Identification of promoter mutants defective in growth-rate-dependent regulation of rRNA transcription in Escherichia coli.
    J Bacteriol. 1989 Sep;171(9):4862-70 PMID: 2670896
  14. Influence of the GCGC discriminator motif introduced into the ribosomal RNA P2- and tac promoter on growth-rate control and stringent sensitivity.
    EMBO J. 1989 Nov;8(11):3357-63 PMID: 2479545
  15. Characterization of the relA1 mutation and a comparison of relA1 with new relA null alleles in Escherichia coli.
    J Biol Chem. 1989 Dec 15;264(35):21146-52 PMID: 2556396
  16. Guanosine tetraphosphate (ppGpp) dependence of the growth rate control of rrnB P1 promoter activity in Escherichia coli.
    J Biol Chem. 1990 Jul 15;265(20):11605-14 PMID: 2114400
  17. Guanosine 3'-diphosphate 5'-diphosphate is not required for growth rate-dependent control of rRNA synthesis in Escherichia coli.
    Proc Natl Acad Sci U S A. 1990 Jul;87(14):5533-7 PMID: 2196571
  18. E.coli Fis protein activates ribosomal RNA transcription in vitro and in vivo.
    EMBO J. 1990 Nov;9(11):3733-42 PMID: 2209559
  19. An unusual correlation between ppGpp pool size and rate of ribosome synthesis during partial pyrimidine starvation of Escherichia coli.
    J Bacteriol. 1991 Feb;173(3):1168-74 PMID: 1704003
  20. Culture medium for enterobacteria.
    J Bacteriol. 1974 Sep;119(3):736-47 PMID: 4604283
  21. RNA polymerase specificity and the control of growth.
    Nature. 1976 Oct 21;263(5579):641-6 PMID: 790197
  22. Identification of initiation sites for the in vitro transcription of rRNA operons rrnE and rrnA in E. coli.
    Cell. 1979 May;17(1):211-24 PMID: 378406
  23. Promoter sequence for stringent control of bacterial ribonucleic acid synthesis.
    J Bacteriol. 1980 Feb;141(2):973-6 PMID: 6154042
  24. Overexpression of the relA gene in Escherichia coli.
    J Biol Chem. 1991 Feb 25;266(6):3760-7 PMID: 1899866
  25. Residual guanosine 3',5'-bispyrophosphate synthetic activity of relA null mutants can be eliminated by spoT null mutations.
    J Biol Chem. 1991 Mar 25;266(9):5980-90 PMID: 2005134
  26. Factor-independent activation of Escherichia coli rRNA transcription. II. characterization of complexes of rrnB P1 promoters containing or lacking the upstream activator region with Escherichia coli RNA polymerase.
    J Mol Biol. 1991 Aug 5;220(3):569-83 PMID: 1651394
  27. The Escherichia coli K-12 "wild types" W3110 and MG1655 have an rph frameshift mutation that leads to pyrimidine starvation due to low pyrE expression levels.
    J Bacteriol. 1993 Jun;175(11):3401-7 PMID: 8501045
  28. Depletion of functional ribosomal RNA operons in Escherichia coli causes increased expression of the remaining intact copies.
    EMBO J. 1993 Nov;12(11):4305-15 PMID: 8223440
  29. Two modes of transcription initiation in vitro at the rrnB P1 promoter of Escherichia coli.
    J Biol Chem. 1993 Nov 5;268(31):23477-82 PMID: 8226874
  30. A third recognition element in bacterial promoters: DNA binding by the alpha subunit of RNA polymerase.
    Science. 1993 Nov 26;262(5138):1407-13 PMID: 8248780
  31. Factor independent activation of rrnB P1. An "extended" promoter with an upstream element that dramatically increases promoter strength.
    J Mol Biol. 1994 Feb 4;235(5):1421-35 PMID: 8107083
  32. High concentrations of ppGpp decrease the RNA chain growth rate. Implications for protein synthesis and translational fidelity during amino acid starvation in Escherichia coli.
    J Mol Biol. 1994 Feb 18;236(2):441-54 PMID: 7508988
  33. Growth rate-dependent control of the rrnB P1 core promoter in Escherichia coli.
    J Bacteriol. 1994 Sep;176(17):5560-4 PMID: 8071240
  34. Regulation of the S10 ribosomal protein operon in E. coli: nucleotide sequence at the start of the operon.
    Cell. 1981 Oct;26(2 Pt 2):205-11 PMID: 7037196
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1995-02-14
Pages
1117-21
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC42649
Subset
IM
Grants
NIGMS NIH HHS · GM37048 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]