Skip to main content
The EMBO Journal logoLink to The EMBO Journal
. 1990 Nov;9(11):3787–3794. doi: 10.1002/j.1460-2075.1990.tb07592.x

Division genes in Escherichia coli are expressed coordinately to cell septum requirements by gearbox promoters.

M Aldea 1, T Garrido 1, J Pla 1, M Vicente 1
PMCID: PMC552138  PMID: 1698623

Abstract

The cell division ftsQAZ cluster and the ftsZ-dependent bolA morphogene of Escherichia coli are found to be driven by gearboxes, a distinct class of promoters characterized by showing an activity that is inversely dependent on growth rate. These promoters contain specific sequences upstream from the mRNA start point, and their -10 region is essential for the inverse growth rate dependence. Gearbox promoters are essential for driving ftsQAZ and bolA gene expression so that the encoded products are synthesized at constant amounts per cell independently of cell size. This mode of regulation would be expected for the expression of proteins that either play a regulatory role in cell division or form a stoichiometric component of the septum, a structure that, independently of cell size and growth rate, is produced once per cell cycle.

Full text

PDF
3791

Images in this article

Selected References

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

  1. Aldea M., Claverie-Martín F., Díaz-Torres M. R., Kushner S. R. Transcript mapping using [35S]DNA probes, trichloroacetate solvent and dideoxy sequencing ladders: a rapid method for identification of transcriptional start points. Gene. 1988 May 15;65(1):101–110. doi: 10.1016/0378-1119(88)90421-0. [DOI] [PubMed] [Google Scholar]
  2. Aldea M., Garrido T., Hernández-Chico C., Vicente M., Kushner S. R. Induction of a growth-phase-dependent promoter triggers transcription of bolA, an Escherichia coli morphogene. EMBO J. 1989 Dec 1;8(12):3923–3931. doi: 10.1002/j.1460-2075.1989.tb08573.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Aldea M., Hernández-Chico C., de la Campa A. G., Kushner S. R., Vicente M. Identification, cloning, and expression of bolA, an ftsZ-dependent morphogene of Escherichia coli. J Bacteriol. 1988 Nov;170(11):5169–5176. doi: 10.1128/jb.170.11.5169-5176.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Begg K. J., Hatfull G. F., Donachie W. D. Identification of new genes in a cell envelope-cell division gene cluster of Escherichia coli: cell division gene ftsQ. J Bacteriol. 1980 Oct;144(1):435–437. doi: 10.1128/jb.144.1.435-437.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Braun R. E., O'Day K., Wright A. Autoregulation of the DNA replication gene dnaA in E. coli K-12. Cell. 1985 Jan;40(1):159–169. doi: 10.1016/0092-8674(85)90319-8. [DOI] [PubMed] [Google Scholar]
  6. Chiaramello A. E., Zyskind J. W. Expression of Escherichia coli dnaA and mioC genes as a function of growth rate. J Bacteriol. 1989 Aug;171(8):4272–4280. doi: 10.1128/jb.171.8.4272-4280.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Connell N., Han Z., Moreno F., Kolter R. An E. coli promoter induced by the cessation of growth. Mol Microbiol. 1987 Sep;1(2):195–201. doi: 10.1111/j.1365-2958.1987.tb00512.x. [DOI] [PubMed] [Google Scholar]
  8. Dewar S. J., Kagan-Zur V., Begg K. J., Donachie W. D. Transcriptional regulation of cell division genes in Escherichia coli. Mol Microbiol. 1989 Oct;3(10):1371–1377. doi: 10.1111/j.1365-2958.1989.tb00118.x. [DOI] [PubMed] [Google Scholar]
  9. Fuller R. S., Funnell B. E., Kornberg A. The dnaA protein complex with the E. coli chromosomal replication origin (oriC) and other DNA sites. Cell. 1984 Oct;38(3):889–900. doi: 10.1016/0092-8674(84)90284-8. [DOI] [PubMed] [Google Scholar]
  10. Gourse R. L., de Boer H. A., Nomura M. 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. doi: 10.1016/0092-8674(86)90498-8. [DOI] [PubMed] [Google Scholar]
  11. Harley C. B., Reynolds R. P. Analysis of E. coli promoter sequences. Nucleic Acids Res. 1987 Mar 11;15(5):2343–2361. doi: 10.1093/nar/15.5.2343. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Jones C. A., Holland I. B. Inactivation of essential division genes, ftsA, ftsZ, suppresses mutations at sfiB, a locus mediating division inhibition during the SOS response in E. coli. EMBO J. 1984 May;3(5):1181–1186. doi: 10.1002/j.1460-2075.1984.tb01948.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kunkel T. A. Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc Natl Acad Sci U S A. 1985 Jan;82(2):488–492. doi: 10.1073/pnas.82.2.488. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Lin-Chao S., Bremer H. Effect of the bacterial growth rate on replication control of plasmid pBR322 in Escherichia coli. Mol Gen Genet. 1986 Apr;203(1):143–149. doi: 10.1007/BF00330395. [DOI] [PubMed] [Google Scholar]
  15. Lutkenhaus J. F. Coupling of DNA replication and cell division: sulB is an allele of ftsZ. J Bacteriol. 1983 Jun;154(3):1339–1346. doi: 10.1128/jb.154.3.1339-1346.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lutkenhaus J. Regulation of cell division in E. coli. Trends Genet. 1990 Jan;6(1):22–25. doi: 10.1016/0168-9525(90)90045-8. [DOI] [PubMed] [Google Scholar]
  17. Løbner-Olesen A., Skarstad K., Hansen F. G., von Meyenburg K., Boye E. The DnaA protein determines the initiation mass of Escherichia coli K-12. Cell. 1989 Jun 2;57(5):881–889. doi: 10.1016/0092-8674(89)90802-7. [DOI] [PubMed] [Google Scholar]
  18. Masters M., Paterson T., Popplewell A. G., Owen-Hughes T., Pringle J. H., Begg K. J. The effect of DnaA protein levels and the rate of initiation at oriC on transcription originating in the ftsQ and ftsA genes: in vivo experiments. Mol Gen Genet. 1989 Apr;216(2-3):475–483. doi: 10.1007/BF00334393. [DOI] [PubMed] [Google Scholar]
  19. Messer W., Seufert W., Schaefer C., Gielow A., Hartmann H., Wende M. Functions of the DnaA protein of Escherichia coli in replication and transcription. Biochim Biophys Acta. 1988 Dec 20;951(2-3):351–358. doi: 10.1016/0167-4781(88)90106-6. [DOI] [PubMed] [Google Scholar]
  20. Messing J., Gronenborn B., Müller-Hill B., Hans Hopschneider P. Filamentous coliphage M13 as a cloning vehicle: insertion of a HindII fragment of the lac regulatory region in M13 replicative form in vitro. Proc Natl Acad Sci U S A. 1977 Sep;74(9):3642–3646. doi: 10.1073/pnas.74.9.3642. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Robinson A. C., Kenan D. J., Hatfull G. F., Sullivan N. F., Spiegelberg R., Donachie W. D. DNA sequence and transcriptional organization of essential cell division genes ftsQ and ftsA of Escherichia coli: evidence for overlapping transcriptional units. J Bacteriol. 1984 Nov;160(2):546–555. doi: 10.1128/jb.160.2.546-555.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Robinson A. C., Kenan D. J., Sweeney J., Donachie W. D. Further evidence for overlapping transcriptional units in an Escherichia coli cell envelope-cell division gene cluster: DNA sequence and transcriptional organization of the ddl ftsQ region. J Bacteriol. 1986 Sep;167(3):809–817. doi: 10.1128/jb.167.3.809-817.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Simons R. W., Houman F., Kleckner N. Improved single and multicopy lac-based cloning vectors for protein and operon fusions. Gene. 1987;53(1):85–96. doi: 10.1016/0378-1119(87)90095-3. [DOI] [PubMed] [Google Scholar]
  24. Tormo A., Ayala J. A., de Pedro M. A., Aldea M., Vicente M. Interaction of FtsA and PBP3 proteins in the Escherichia coli septum. J Bacteriol. 1986 Jun;166(3):985–992. doi: 10.1128/jb.166.3.985-992.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Tormo A., Dopazo A., de la Campa A. G., Aldea M., Vicente M. Coupling between DNA replication and cell division mediated by the FtsA protein in Escherichia coli: a pathway independent of the SOS response, the "TER" pathway. J Bacteriol. 1985 Nov;164(2):950–953. doi: 10.1128/jb.164.2.950-953.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Tormo A., Vicente M. The ftsA gene product participates in formation of the Escherichia coli septum structure. J Bacteriol. 1984 Mar;157(3):779–784. doi: 10.1128/jb.157.3.779-784.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Wanner B. L., Kodaira R., Neidhardt F. C. Physiological regulation of a decontrolled lac operon. J Bacteriol. 1977 Apr;130(1):212–222. doi: 10.1128/jb.130.1.212-222.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Yi Q. M., Rockenbach S., Ward J. E., Jr, Lutkenhaus J. Structure and expression of the cell division genes ftsQ, ftsA and ftsZ. J Mol Biol. 1985 Aug 5;184(3):399–412. doi: 10.1016/0022-2836(85)90290-6. [DOI] [PubMed] [Google Scholar]
  30. de Boer P. A., Crossley R. E., Rothfield L. I. A division inhibitor and a topological specificity factor coded for by the minicell locus determine proper placement of the division septum in E. coli. Cell. 1989 Feb 24;56(4):641–649. doi: 10.1016/0092-8674(89)90586-2. [DOI] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES