Abstract
Caulobacter crescentus flagellar (fla, flb, or flg) genes are periodically expressed in the cell cycle and they are organized in a regulatory hierarchy. We have analyzed the genetic interactions required for fla gene expression by determining the effect of mutations in 30 known fla genes on transcription from four operons in the hook gene cluster. These results show that the flaO (transcription unit III) and flbF (transcription unit IV) operons are located at or near the top of the hierarchy. They also reveal an extensive network of negative transcriptional controls that are superimposed on the positive regulatory cascade described previously. The strong negative autoregulation observed for the flaN (transcription unit I), flbG (transcription unit II), and flaO (transcription unit III) promoters provides one possible mechanism for turning off fla gene expression at the end of the respective synthetic periods. We suggest that these positive and negative transcriptional interactions are components of genetic switches that determine the sequence in which fla genes are turned on and off in the C. crescentus cell cycle.
Full text
PDF![6651](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/e8cf/297903/de2e7e577d81/pnas00284-0219.png)
![6652](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/e8cf/297903/c2d87ee70cc7/pnas00284-0220.png)
![6653](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/e8cf/297903/9229f41ff51c/pnas00284-0221.png)
![6654](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/e8cf/297903/2b54efb2ef7b/pnas00284-0222.png)
![6655](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/e8cf/297903/8367eca88820/pnas00284-0223.png)
Images in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Ausubel F. M. Regulation of nitrogen fixation genes. Cell. 1984 May;37(1):5–6. doi: 10.1016/0092-8674(84)90294-0. [DOI] [PubMed] [Google Scholar]
- Champer R., Bryan R., Gomes S. L., Purucker M., Shapiro L. Temporal and spatial control of flagellar and chemotaxis gene expression during Caulobacter cell differentiation. Cold Spring Harb Symp Quant Biol. 1985;50:831–840. doi: 10.1101/sqb.1985.050.01.101. [DOI] [PubMed] [Google Scholar]
- 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]
- Chen L. S., Mullin D., Newton A. Identification, nucleotide sequence, and control of developmentally regulated promoters in the hook operon region of Caulobacter crescentus. Proc Natl Acad Sci U S A. 1986 May;83(9):2860–2864. doi: 10.1073/pnas.83.9.2860. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Hahnenberger K. M., Shapiro L. Identification of a gene cluster involved in flagellar basal body biogenesis in Caulobacter crescentus. J Mol Biol. 1987 Mar 5;194(1):91–103. doi: 10.1016/0022-2836(87)90718-2. [DOI] [PubMed] [Google Scholar]
- Hahnenberger K. M., Shapiro L. Organization and temporal expression of a flagellar basal body gene in Caulobacter crescentus. J Bacteriol. 1988 Sep;170(9):4119–4124. doi: 10.1128/jb.170.9.4119-4124.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Johnson R. C., Ely B. Analysis of nonmotile mutants of the dimorphic bacterium Caulobacter crescentus. J Bacteriol. 1979 Jan;137(1):627–634. doi: 10.1128/jb.137.1.627-634.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Johnson R. C., Ferber D. M., Ely B. Synthesis and assembly of flagellar components by Caulobacter crescentus motility mutants. J Bacteriol. 1983 Jun;154(3):1137–1144. doi: 10.1128/jb.154.3.1137-1144.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Komeda Y. Transcriptional control of flagellar genes in Escherichia coli K-12. J Bacteriol. 1986 Dec;168(3):1315–1318. doi: 10.1128/jb.168.3.1315-1318.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Minnich S. A., Newton A. Promoter mapping and cell cycle regulation of flagellin gene transcription in Caulobacter crescentus. Proc Natl Acad Sci U S A. 1987 Mar;84(5):1142–1146. doi: 10.1073/pnas.84.5.1142. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mullin D., Minnich S., Chen L. S., Newton A. A set of positively regulated flagellar gene promoters in Caulobacter crescentus with sequence homology to the nif gene promoters of Klebsiella pneumoniae. J Mol Biol. 1987 Jun 20;195(4):939–943. doi: 10.1016/0022-2836(87)90497-9. [DOI] [PubMed] [Google Scholar]
- Ninfa A. J., Mullin D. A., Ramakrishnan G., Newton A. Escherichia coli sigma 54 RNA polymerase recognizes Caulobacter crescentus flbG and flaN flagellar gene promoters in vitro. J Bacteriol. 1989 Jan;171(1):383–391. doi: 10.1128/jb.171.1.383-391.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- Purucker M., Bryan R., Amemiya K., Ely B., Shapiro L. Isolation of a Caulobacter gene cluster specifying flagellum production by using nonmotile Tn5 insertion mutants. Proc Natl Acad Sci U S A. 1982 Nov;79(22):6797–6801. doi: 10.1073/pnas.79.22.6797. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schoenlein P. V., Gallman L. S., Ely B. Organization of the flaFG gene cluster and identification of two additional genes involved in flagellum biogenesis in Caulobacter crescentus. J Bacteriol. 1989 Mar;171(3):1544–1553. doi: 10.1128/jb.171.3.1544-1553.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shapiro L. Generation of polarity during Caulobacter cell differentiation. Annu Rev Cell Biol. 1985;1:173–207. doi: 10.1146/annurev.cb.01.110185.001133. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]