Contributions of UP Elements and the Transcription Factor FIS to Expression from the Seven rrn P1 Promoters inEscherichia coli

ABSTRACT The high activity of the rrnB P1 promoter inEscherichia coli results from acis-acting DNA sequence, the UP element, and atrans-acting transcription factor, FIS. In this study, we examine the effects of FIS and the UP element at the other sixrrn P1 promoters. We find that UP elements are present at all of the rrn P1 promoters, but they make different relative contributions to promoter activity. Similarly, FIS binds upstream of, and activates, all seven rrn P1 promoters but to different extents. The total number of FIS binding sites, as well as their positions relative to the transcription start site, differ at each rrn P1 promoter. Surprisingly, the FIS sites upstream of site I play a much larger role in transcription from most rrn P1 promoters compared to rrnBP1. Our studies indicate that the overall activities of the sevenrrn P1 promoters are similar, and the same contributors are responsible for these high activities, but these inputs make different relative contributions and may act through slightly different mechanisms at each promoter. These studies have implications for the control of gene expression of unlinked multigene families.

[1]  A. T.,et al.  On Stringent Response , 1972, Nature.

[2]  Jeffrey H. Miller.  Experiments in molecular genetics , 1972 .

[3]  R. Gourse,et al.  Defective antitermination of rRNA transcription and derepression of rRNA and tRNA synthesis in the nusB5 mutant of Escherichia coli. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[4]  R. Gourse,et al.  DNA determinants of rRNA synthesis in E. coli: Growth rate dependent regulation, feedback inhibition, upstream activation, antitermination , 1986, Cell.

[5]  F. Neidhardt,et al.  Escherichia Coli and Salmonella: Typhimurium Cellular and Molecular Biology , 1987 .

[6]  M. Simon,et al.  Spatial relationship of the Fis binding sites for Hin recombinational enhancer activity , 1987, Nature.

[7]  C. Ball,et al.  Isolation of the gene encoding the Hin recombinational enhancer binding protein. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[8]  G. Glaser,et al.  Ribosome associated protein(s) specifically bind(s) to the upstream activator sequence of the E. coli rrnA P1 promoter. , 1989, Nucleic Acids Research.

[9]  R. Gourse,et al.  E.coli Fis protein activates ribosomal RNA transcription in vitro and in vivo. , 1990, The EMBO journal.

[10]  R. Gourse,et al.  Sequences upstream of the-35 hexamer of rrnB P1 affect promoter strength and upstream activation. , 1990, Biochimica et biophysica acta.

[11]  T. D. Schneider,et al.  Sequence logos: a new way to display consensus sequences. , 1990, Nucleic acids research.

[12]  L. Bosch,et al.  Potential binding sites of the trans-activator FIS are present upstream of all rRNA operons and of many but not all tRNA operons. , 1990, Biochimica et biophysica acta.

[13]  L. Bosch,et al.  The role of FIS in trans activation of stable RNA operons of E. coli. , 1990, The EMBO journal.

[14]  R. Gourse,et al.  Factor-independent activation of Escherichia coli rRNA transcription. I. Kinetic analysis of the roles of the upstream activator region and supercoiling on transcription of the rrnB P1 promoter in vitro. , 1991, Journal of molecular biology.

[15]  R. C. Johnson,et al.  The Fis protein: it's not just for DNA inversion anymore , 1992, Molecular microbiology.

[16]  C. Condon,et al.  Comparison of the expression of the seven ribosomal RNA operons in Escherichia coli. , 1992, The EMBO journal.

[17]  L. Bosch,et al.  The mechanism of trans-activation of the Escherichia coli operon thrU(tufB) by the protein FIS. A model. , 1992, Nucleic acids research.

[18]  M. Zacharias,et al.  Analysis of the Fis-dependent and Fis-independent transcription activation mechanisms of the Escherichia coli ribosomal RNA P1 promoter. , 1992, Biochemistry.

[19]  C. Ball,et al.  Dramatic changes in Fis levels upon nutrient upshift in Escherichia coli , 1992, Journal of bacteriology.

[20]  C. Condon,et al.  Depletion of functional ribosomal RNA operons in Escherichia coli causes increased expression of the remaining intact copies. , 1993, The EMBO journal.

[21]  P. Sander,et al.  Mechanisms of upstream activation of the rrnD promoter P1 of Escherichia coli. , 1993, The Journal of biological chemistry.

[22]  R. Gourse,et al.  A third recognition element in bacterial promoters: DNA binding by the alpha subunit of RNA polymerase. , 1993, Science.

[23]  R. Gourse,et al.  Localization of the intrinsically bent DNA region upstream of the E.coli rrnB P1 promoter. , 1994, Nucleic acids research.

[24]  V. de Lorenzo,et al.  Co-regulation by bent DNA. Functional substitutions of the integration host factor site at sigma 54-dependent promoter Pu of the upper-TOL operon by intrinsically curved sequences. , 1994, The Journal of biological chemistry.

[25]  R. Gourse,et al.  Factor independent activation of rrnB P1. An "extended" promoter with an upstream element that dramatically increases promoter strength. , 1994, Journal of molecular biology.

[26]  C. Condon,et al.  rRNA operon multiplicity in Escherichia coli and the physiological implications of rrn inactivation , 1995, Journal of bacteriology.

[27]  R. C. Johnson,et al.  Fis activates the RpoS-dependent stationary-phase expression of proP in Escherichia coli , 1995, Journal of bacteriology.

[28]  O. Ozoline,et al.  Structure of open promoter complexes with Escherichia coli RNA polymerase as revealed by the DNase I footprinting technique: compilation analysis. , 1995, Nucleic acids research.

[29]  R. Gourse,et al.  The transcriptional activator protein FIS: DNA interactions and cooperative interactions with RNA polymerase at the Escherichia coli rrnB P1 promoter. , 1995, Journal of molecular biology.

[30]  R. Gourse,et al.  rRNA transcription and growth rate-dependent regulation of ribosome synthesis in Escherichia coli. , 1996, Annual Review of Microbiology.

[31]  R. C. Johnson,et al.  Variable structures of Fis-DNA complexes determined by flanking DNA-protein contacts. , 1996, Journal of molecular biology.

[32]  Y. Kyōgoku,et al.  Flexible linker in the RNA polymerase alpha subunit facilitates the independent motion of the C-terminal activator contact domain. , 1997, Journal of molecular biology.

[33]  R. Gourse,et al.  Molecular anatomy of a transcription activation patch: FIS–RNA polymerase interactions at the Escherichia coli rrnB P1 promoter , 1997, The EMBO journal.

[34]  M. Buckle,et al.  FIS activates sequential steps during transcription initiation at a stable RNA promoter , 1997, The EMBO journal.

[35]  T. D. Schneider,et al.  Information analysis of Fis binding sites. , 1997, Nucleic acids research.

[36]  T. D. Schneider,et al.  Information content of individual genetic sequences. , 1997, Journal of theoretical biology.

[37]  C. Turnbough,et al.  Transcription regulation by initiating NTP concentration: rRNA synthesis in bacteria. , 1997, Science.

[38]  K. Murakami,et al.  Positioning of two alpha subunit carboxy-terminal domains of RNA polymerase at promoters by two transcription factors. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[39]  R. Gourse,et al.  RNA polymerase mutants that destabilize RNA polymerase-promoter complexes alter NTP-sensing by rrn P1 promoters. , 1998, Journal of molecular biology.

[40]  R. Gourse,et al.  Identification of an UP element consensus sequence for bacterial promoters. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[41]  R. Gourse,et al.  Activation of Escherichia coli rRNA Transcription by FIS during a Growth Cycle , 1998, Journal of bacteriology.

[42]  S. Busby,et al.  Transcription activation at promoters carrying tandem DNA sites for the Escherichia coli cyclic AMP receptor protein: organisation of the RNA polymerase alpha subunits. , 1998, Journal of molecular biology.

[43]  S. Aiyar,et al.  Escherichia coli Promoters with UP Elements of Different Strengths: Modular Structure of Bacterial Promoters , 1998, Journal of bacteriology.

[44]  R. Ebright,et al.  Bacterial promoter architecture: subsite structure of UP elements and interactions with the carboxy-terminal domain of the RNA polymerase alpha subunit. , 1999, Genes & development.

[45]  R. Gourse,et al.  Activation of Escherichia coli leuVTranscription by FIS , 1999, Journal of bacteriology.

[46]  C. Condon,et al.  Construction and Initial Characterization of Escherichia coli Strains with Few or No Intact Chromosomal rRNA Operons , 1999, Journal of bacteriology.

[47]  S. Ueda,et al.  Growth Phase-Dependent Variation in Protein Composition of the Escherichia coli Nucleoid , 1999, Journal of bacteriology.

[48]  H. Bremer.  Modulation of Chemical Composition and Other Parameters of the Cell by Growth Rate , 1999 .

[49]  R. Gourse,et al.  UPs and downs in bacterial transcription initiation: the role of the alpha subunit of RNA polymerase in promoter recognition , 2000, Molecular microbiology.

[50]  T. Schmidt,et al.  rRNA Operon Copy Number Reflects Ecological Strategies of Bacteria , 2000, Applied and Environmental Microbiology.

[51]  Younggyu Kim,et al.  Structural Organization of the RNA Polymerase-Promoter Open Complex , 2000, Cell.

[52]  V. de Lorenzo,et al.  The black cat/white cat principle of signal integration in bacterial promoters , 2001 .

[53]  R. Gourse,et al.  Mechanism of regulation of transcription initiation by ppGpp. I. Effects of ppGpp on transcription initiation in vivo and in vitro. , 2001, Journal of molecular biology.

[54]  R. Gourse,et al.  Fine structure of E. coli RNA polymerase-promoter interactions: alpha subunit binding to the UP element minor groove. , 2001, Genes & development.