Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1995 Apr;177(7):1662–1669. doi: 10.1128/jb.177.7.1662-1669.1995

Coordinate cell cycle control of a Caulobacter DNA methyltransferase and the flagellar genetic hierarchy.

C M Stephens 1, G Zweiger 1, L Shapiro 1
PMCID: PMC176791  PMID: 7896686

Abstract

The expression of the Caulobacter ccrM gene and the activity of its product, the M.Ccr II DNA methyltransferase, are limited to a discrete portion of the cell cycle (G. Zweiger, G. Marczynski, and L. Shapiro, J. Mol. Biol. 235:472-485, 1994). Temporal control of DNA methylation has been shown to be critical for normal development in the dimorphic Caulobacter life cycle. To understand the mechanism by which ccrM expression is regulated during the cell cycle, we have identified and characterized the ccrM promoter region. We have found that it belongs to an unusual promoter family used by several Caulobacter class II flagellar genes. The expression of these class II genes initiates assembly of the flagellum just prior to activation of the ccrM promoter in the predivisional cell. Mutational analysis of two M.Ccr II methylation sites located 3' to the ccrM promoter suggests that methylation might influence the temporally controlled inactivation of ccrM transcription. An additional parallel between the ccrM and class II flagellar promoters is that their transcription responds to a cell cycle DNA replication checkpoint. We propose that a common regulatory system coordinates the expression of functionally diverse genes during the Caulobacter cell cycle.

Full Text

The Full Text of this article is available as a PDF (325.4 KB).

Selected References

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

  1. Banks J. A., Masson P., Fedoroff N. Molecular mechanisms in the developmental regulation of the maize Suppressor-mutator transposable element. Genes Dev. 1988 Nov;2(11):1364–1380. doi: 10.1101/gad.2.11.1364. [DOI] [PubMed] [Google Scholar]
  2. Bi E., Lutkenhaus J. Cell division inhibitors SulA and MinCD prevent formation of the FtsZ ring. J Bacteriol. 1993 Feb;175(4):1118–1125. doi: 10.1128/jb.175.4.1118-1125.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Boye E., Løbner-Olesen A. The role of dam methyltransferase in the control of DNA replication in E. coli. Cell. 1990 Sep 7;62(5):981–989. doi: 10.1016/0092-8674(90)90272-g. [DOI] [PubMed] [Google Scholar]
  4. Boyes J., Bird A. DNA methylation inhibits transcription indirectly via a methyl-CpG binding protein. Cell. 1991 Mar 22;64(6):1123–1134. doi: 10.1016/0092-8674(91)90267-3. [DOI] [PubMed] [Google Scholar]
  5. Braaten B. A., Nou X., Kaltenbach L. S., Low D. A. Methylation patterns in pap regulatory DNA control pyelonephritis-associated pili phase variation in E. coli. Cell. 1994 Feb 11;76(3):577–588. doi: 10.1016/0092-8674(94)90120-1. [DOI] [PubMed] [Google Scholar]
  6. Brun Y. V., Marczynski G., Shapiro L. The expression of asymmetry during Caulobacter cell differentiation. Annu Rev Biochem. 1994;63:419–450. doi: 10.1146/annurev.bi.63.070194.002223. [DOI] [PubMed] [Google Scholar]
  7. Busslinger M., Hurst J., Flavell R. A. DNA methylation and the regulation of globin gene expression. Cell. 1983 Aug;34(1):197–206. doi: 10.1016/0092-8674(83)90150-2. [DOI] [PubMed] [Google Scholar]
  8. Campbell J. L., Kleckner N. E. coli oriC and the dnaA gene promoter are sequestered from dam methyltransferase following the passage of the chromosomal replication fork. Cell. 1990 Sep 7;62(5):967–979. doi: 10.1016/0092-8674(90)90271-f. [DOI] [PubMed] [Google Scholar]
  9. Champer R., Dingwall A., Shapiro L. Cascade regulation of Caulobacter flagellar and chemotaxis genes. J Mol Biol. 1987 Mar 5;194(1):71–80. doi: 10.1016/0022-2836(87)90716-9. [DOI] [PubMed] [Google Scholar]
  10. Degnen S. T., Newton A. Dependence of cell division on the completion of chromosome replication in Caulobacter. J Bacteriol. 1972 Jun;110(3):852–856. doi: 10.1128/jb.110.3.852-856.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dingwall A., Zhuang W. Y., Quon K., Shapiro L. Expression of an early gene in the flagellar regulatory hierarchy is sensitive to an interruption in DNA replication. J Bacteriol. 1992 Mar;174(6):1760–1768. doi: 10.1128/jb.174.6.1760-1768.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Ely B. Genetics of Caulobacter crescentus. Methods Enzymol. 1991;204:372–384. doi: 10.1016/0076-6879(91)04019-k. [DOI] [PubMed] [Google Scholar]
  13. Enoch T., Nurse P. Mutation of fission yeast cell cycle control genes abolishes dependence of mitosis on DNA replication. Cell. 1990 Feb 23;60(4):665–673. doi: 10.1016/0092-8674(90)90669-6. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. Gober J. W., Champer R., Reuter S., Shapiro L. Expression of positional information during cell differentiation of Caulobacter. Cell. 1991 Jan 25;64(2):381–391. doi: 10.1016/0092-8674(91)90646-g. [DOI] [PubMed] [Google Scholar]
  16. Hare J. T., Taylor J. H. One role for DNA methylation in vertebrate cells is strand discrimination in mismatch repair. Proc Natl Acad Sci U S A. 1985 Nov;82(21):7350–7354. doi: 10.1073/pnas.82.21.7350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Huisman O., D'Ari R., Gottesman S. Cell-division control in Escherichia coli: specific induction of the SOS function SfiA protein is sufficient to block septation. Proc Natl Acad Sci U S A. 1984 Jul;81(14):4490–4494. doi: 10.1073/pnas.81.14.4490. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Ireton K., Grossman A. D. A developmental checkpoint couples the initiation of sporulation to DNA replication in Bacillus subtilis. EMBO J. 1994 Apr 1;13(7):1566–1573. doi: 10.1002/j.1460-2075.1994.tb06419.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Ireton K., Grossman A. D. Coupling between gene expression and DNA synthesis early during development in Bacillus subtilis. Proc Natl Acad Sci U S A. 1992 Sep 15;89(18):8808–8812. doi: 10.1073/pnas.89.18.8808. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Itaya M. Isolation and characterization of a second RNase H (RNase HII) of Escherichia coli K-12 encoded by the rnhB gene. Proc Natl Acad Sci U S A. 1990 Nov;87(21):8587–8591. doi: 10.1073/pnas.87.21.8587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Modrich P. Methyl-directed DNA mismatch correction. J Biol Chem. 1989 Apr 25;264(12):6597–6600. [PubMed] [Google Scholar]
  22. Murray A. W. Creative blocks: cell-cycle checkpoints and feedback controls. Nature. 1992 Oct 15;359(6396):599–604. doi: 10.1038/359599a0. [DOI] [PubMed] [Google Scholar]
  23. Newton A., Ohta N., Ramakrishnan G., Mullin D., Raymond G. Genetic switching in the flagellar gene hierarchy of Caulobacter requires negative as well as positive regulation of transcription. Proc Natl Acad Sci U S A. 1989 Sep;86(17):6651–6655. doi: 10.1073/pnas.86.17.6651. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Nou X., Skinner B., Braaten B., Blyn L., Hirsch D., Low D. Regulation of pyelonephritis-associated pili phase-variation in Escherichia coli: binding of the PapI and the Lrp regulatory proteins is controlled by DNA methylation. Mol Microbiol. 1993 Feb;7(4):545–553. doi: 10.1111/j.1365-2958.1993.tb01145.x. [DOI] [PubMed] [Google Scholar]
  25. Ogden G. B., Pratt M. J., Schaechter M. The replicative origin of the E. coli chromosome binds to cell membranes only when hemimethylated. Cell. 1988 Jul 1;54(1):127–135. doi: 10.1016/0092-8674(88)90186-9. [DOI] [PubMed] [Google Scholar]
  26. Ohta N., Masurekar M., Newton A. Cloning and cell cycle-dependent expression of DNA replication gene dnaC from Caulobacter crescentus. J Bacteriol. 1990 Dec;172(12):7027–7034. doi: 10.1128/jb.172.12.7027-7034.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Osley M. A., Newton A. Mutational analysis of developmental control in Caulobacter crescentus. Proc Natl Acad Sci U S A. 1977 Jan;74(1):124–128. doi: 10.1073/pnas.74.1.124. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. 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]
  29. 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]
  30. Roberts D., Hoopes B. C., McClure W. R., Kleckner N. IS10 transposition is regulated by DNA adenine methylation. Cell. 1985 Nov;43(1):117–130. doi: 10.1016/0092-8674(85)90017-0. [DOI] [PubMed] [Google Scholar]
  31. Salser W., Gesteland R. F., Bolle A. In vitro synthesis of bacteriophage lysozyme. Nature. 1967 Aug 5;215(5101):588–591. doi: 10.1038/215588a0. [DOI] [PubMed] [Google Scholar]
  32. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Stephens C. M., Shapiro L. An unusual promoter controls cell-cycle regulation and dependence on DNA replication of the Caulobacter fliLM early flagellar operon. Mol Microbiol. 1993 Sep;9(6):1169–1179. doi: 10.1111/j.1365-2958.1993.tb01246.x. [DOI] [PubMed] [Google Scholar]
  34. Tomasiewicz H. G., McHenry C. S. Sequence analysis of the Escherichia coli dnaE gene. J Bacteriol. 1987 Dec;169(12):5735–5744. doi: 10.1128/jb.169.12.5735-5744.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Van Way S. M., Newton A., Mullin A. H., Mullin D. A. Identification of the promoter and a negative regulatory element, ftr4, that is needed for cell cycle timing of fliF operon expression in Caulobacter crescentus. J Bacteriol. 1993 Jan;175(2):367–376. doi: 10.1128/jb.175.2.367-376.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Walworth N., Davey S., Beach D. Fission yeast chk1 protein kinase links the rad checkpoint pathway to cdc2. Nature. 1993 May 27;363(6427):368–371. doi: 10.1038/363368a0. [DOI] [PubMed] [Google Scholar]
  37. Wingrove J. A., Mangan E. K., Gober J. W. Spatial and temporal phosphorylation of a transcriptional activator regulates pole-specific gene expression in Caulobacter. Genes Dev. 1993 Oct;7(10):1979–1992. doi: 10.1101/gad.7.10.1979. [DOI] [PubMed] [Google Scholar]
  38. Xu H., Dingwall A., Shapiro L. Negative transcriptional regulation in the Caulobacter flagellar hierarchy. Proc Natl Acad Sci U S A. 1989 Sep;86(17):6656–6660. doi: 10.1073/pnas.86.17.6656. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Yu J., Shapiro L. Early Caulobacter crescentus genes fliL and fliM are required for flagellar gene expression and normal cell division. J Bacteriol. 1992 May;174(10):3327–3338. doi: 10.1128/jb.174.10.3327-3338.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Zhuang W. Y., Shapiro L. Caulobacter FliQ and FliR membrane proteins, required for flagellar biogenesis and cell division, belong to a family of virulence factor export proteins. J Bacteriol. 1995 Jan;177(2):343–356. doi: 10.1128/jb.177.2.343-356.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Zweiger G., Marczynski G., Shapiro L. A Caulobacter DNA methyltransferase that functions only in the predivisional cell. J Mol Biol. 1994 Jan 14;235(2):472–485. doi: 10.1006/jmbi.1994.1007. [DOI] [PubMed] [Google Scholar]
  42. al-Khodairy F., Carr A. M. DNA repair mutants defining G2 checkpoint pathways in Schizosaccharomyces pombe. EMBO J. 1992 Apr;11(4):1343–1350. doi: 10.1002/j.1460-2075.1992.tb05179.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES