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. 1986 May;83(9):2860–2864. doi: 10.1073/pnas.83.9.2860

Identification, nucleotide sequence, and control of developmentally regulated promoters in the hook operon region of Caulobacter crescentus.

L S Chen, D Mullin, A Newton
PMCID: PMC323406  PMID: 3517878

Abstract

The major flagellar proteins, including the flagellins and the hook protein, are synthesized periodically in the Caulobacter crescentus cell cycle at the time of flagellum assembly. Although fla genes are regulated at the transcriptional level [Ohta, N., Chen, L.-S., Swanson, E. & Newton, A. (1985) J. Mol. Biol. 186, 107-115], the 5' regulatory regions of C. crescentus genes have not been identified. We describe here the results of nuclease S1 protection assays that map the 5' ends of mRNAs synthesized in vivo from transcription units II (hook operon) and II.1 of the hook gene cluster and locate the corresponding promoter regions PII and PII.1. The two promoters are regulated with different periodicities in the cell cycle and have different genetic requirements for expression. The failure to detect transcripts from either PI or PII in Escherichia coli suggests that developmentally regulated promoters of C. crescentus have different recognition sequences from those of E. coli. There is little nucleotide sequence homology between PII and PII.1. There are, however, three regions of homology between PII and the nucleotide sequence 5' to the 29-kDa-flagellin-related gene, and two of these are in regions of dyad symmetry. We discuss the possibility that DNA-protein interactions at homologous nucleotide sequences like those identified in PII are part of a regulatory gene cascade that participates in timing fla gene expression in the C. crescentus cell cycle.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Berk A. J., Sharp P. A. Sizing and mapping of early adenovirus mRNAs by gel electrophoresis of S1 endonuclease-digested hybrids. Cell. 1977 Nov;12(3):721–732. doi: 10.1016/0092-8674(77)90272-0. [DOI] [PubMed] [Google Scholar]
  2. Brosius J., Cate R. L., Perlmutter A. P. Precise location of two promoters for the beta-lactamase gene of pBR322. S1 mapping of ribonucleic acid isolated from Escherichia coli or synthesized in vitro. J Biol Chem. 1982 Aug 10;257(15):9205–9210. [PubMed] [Google Scholar]
  3. Bryan R., Purucker M., Gomes S. L., Alexander W., Shapiro L. Analysis of the pleiotropic regulation of flagellar and chemotaxis gene expression in Caulobacter crescentus by using plasmid complementation. Proc Natl Acad Sci U S A. 1984 Mar;81(5):1341–1345. doi: 10.1073/pnas.81.5.1341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Delaney A. D. A DNA sequence handling program. Nucleic Acids Res. 1982 Jan 11;10(1):61–67. doi: 10.1093/nar/10.1.61. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Ditta G., Stanfield S., Corbin D., Helinski D. R. Broad host range DNA cloning system for gram-negative bacteria: construction of a gene bank of Rhizobium meliloti. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7347–7351. doi: 10.1073/pnas.77.12.7347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Evinger M., Agabian N. Envelope-associated nucleoid from Caulobacter crescentus stalked and swarmer cells. J Bacteriol. 1977 Oct;132(1):294–301. doi: 10.1128/jb.132.1.294-301.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gill P. R., Agabian N. The nucleotide sequence of the Mr = 28,500 flagellin gene of Caulobacter crescentus. J Biol Chem. 1983 Jun 25;258(12):7395–7401. [PubMed] [Google Scholar]
  8. Hentschel C., Irminger J. C., Bucher P., Birnstiel M. L. Sea urchin histone mRNA termini are located in gene regions downstream from putative regulatory sequences. Nature. 1980 May 15;285(5761):147–151. doi: 10.1038/285147a0. [DOI] [PubMed] [Google Scholar]
  9. Komeda Y. Fusions of flagellar operons to lactose genes on a mu lac bacteriophage. J Bacteriol. 1982 Apr;150(1):16–26. doi: 10.1128/jb.150.1.16-26.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Lagenaur C., Agabian N. Caulobacter flagellar organelle: synthesis, compartmentation, and assembly. J Bacteriol. 1978 Sep;135(3):1062–1069. doi: 10.1128/jb.135.3.1062-1069.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Malan T. P., McClure W. R. Dual promoter control of the Escherichia coli lactose operon. Cell. 1984 Nov;39(1):173–180. doi: 10.1016/0092-8674(84)90203-4. [DOI] [PubMed] [Google Scholar]
  12. Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
  13. Milhausen M., Agabian N. Caulobacter flagellin mRNA segregates asymmetrically at cell division. Nature. 1983 Apr 14;302(5909):630–632. doi: 10.1038/302630a0. [DOI] [PubMed] [Google Scholar]
  14. Moran C. P., Jr, Lang N., Banner C. D., Haldenwang W. G., Losick R. Promoter for a developmentally regulated gene in Bacillus subtilis. Cell. 1981 Sep;25(3):783–791. doi: 10.1016/0092-8674(81)90186-0. [DOI] [PubMed] [Google Scholar]
  15. Moran C. P., Jr, Lang N., LeGrice S. F., Lee G., Stephens M., Sonenshein A. L., Pero J., Losick R. Nucleotide sequences that signal the initiation of transcription and translation in Bacillus subtilis. Mol Gen Genet. 1982;186(3):339–346. doi: 10.1007/BF00729452. [DOI] [PubMed] [Google Scholar]
  16. Ohta N., Chen L. S., Newton A. Isolation and expression of cloned hook protein gene from Caulobacter crescentus. Proc Natl Acad Sci U S A. 1982 Aug;79(16):4863–4867. doi: 10.1073/pnas.79.16.4863. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Ohta N., Chen L. S., Swanson E., Newton A. Transcriptional regulation of a periodically controlled flagellar gene operon in Caulobacter crescentus. J Mol Biol. 1985 Nov 5;186(1):107–115. doi: 10.1016/0022-2836(85)90261-x. [DOI] [PubMed] [Google Scholar]
  18. Ohta N., Swanson E., Ely B., Newton A. Physical mapping and complementation analysis of transposon Tn5 mutations in Caulobacter crescentus: organization of transcriptional units in the hook gene cluster. J Bacteriol. 1984 Jun;158(3):897–904. doi: 10.1128/jb.158.3.897-904.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Osley M. A., Newton A. Temporal control of the cell cycle in Caulobacter crescentus: roles of DNA chain elongation and completion. J Mol Biol. 1980 Mar 25;138(1):109–128. doi: 10.1016/s0022-2836(80)80007-6. [DOI] [PubMed] [Google Scholar]
  20. Osley M. A., Sheffery M., Newton A. Regulation of flagellin synthesis in the cell cycle of caulobacter: dependence on DNA replication. Cell. 1977 Oct;12(2):393–400. doi: 10.1016/0092-8674(77)90115-5. [DOI] [PubMed] [Google Scholar]
  21. Sheffery M., Newton A. Purification and characterization of a polyhook protein from Caulobacter crescentus. J Bacteriol. 1979 May;138(2):575–583. doi: 10.1128/jb.138.2.575-583.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Sheffery M., Newton A. Regulation of periodic protein synthesis in the cell cycle: control of initiation and termination of flagellar gene expression. Cell. 1981 Apr;24(1):49–57. doi: 10.1016/0092-8674(81)90500-6. [DOI] [PubMed] [Google Scholar]
  23. Siebenlist U., Simpson R. B., Gilbert W. E. coli RNA polymerase interacts homologously with two different promoters. Cell. 1980 Jun;20(2):269–281. doi: 10.1016/0092-8674(80)90613-3. [DOI] [PubMed] [Google Scholar]
  24. Spassky A., Busby S., Buc H. On the action of the cyclic AMP-cyclic AMP receptor protein complex at the Escherichia coli lactose and galactose promoter regions. EMBO J. 1984 Jan;3(1):43–50. doi: 10.1002/j.1460-2075.1984.tb01759.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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