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. 1993 Nov;175(22):7341–7347. doi: 10.1128/jb.175.22.7341-7347.1993

Multilevel regulation of the sporulation transcription factor sigma K in Bacillus subtilis.

V Oke 1, R Losick 1
PMCID: PMC206878  PMID: 8226681

Abstract

Gene expression in the mother-cell compartment of the Bacillus subtilis sporangium is governed in part by the sporulation transcription factor sigma K. The production of sigma K is controlled at three levels: by a chromosomal rearrangement that generates the sigma K-coding sequence (sigK), by compartment-specific transcription of sigK, and by conversion of the inactive pro-protein product of sigK (pro-sigma K) to sigma K. To investigate the function of these multiple levels of regulation, we constructed a set of strains that bypass the chromosomal rearrangement, pro-protein processing, or both levels of control. Here we show that one of the functions of the chromosomal rearrangement and pro-protein processing is to prevent inappropriate production of sigma K under nonsporulation conditions. In the absence of both of these levels of control, a low level of sigma K-directed gene expression is observed during stationary phase after growth in rich medium. The appearance of sigma K under these conditions is probably due to a low level of sigma K-directed transcription from the sigK promoter in a positive feedback loop. We also report the construction of a strain that produces high levels of sigma K during growth. Using this strain, we demonstrate that the production of sigma K during growth is sufficient to induce a cascade of gene expression that closely mimics late events in the mother-cell line of gene expression.

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Selected References

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

  1. Brehm S. P., Staal S. P., Hoch J. A. Phenotypes of pleiotropic-negative sporulation mutants of Bacillus subtilis. J Bacteriol. 1973 Sep;115(3):1063–1070. doi: 10.1128/jb.115.3.1063-1070.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Cutting S., Driks A., Schmidt R., Kunkel B., Losick R. Forespore-specific transcription of a gene in the signal transduction pathway that governs Pro-sigma K processing in Bacillus subtilis. Genes Dev. 1991 Mar;5(3):456–466. doi: 10.1101/gad.5.3.456. [DOI] [PubMed] [Google Scholar]
  3. Cutting S., Oke V., Driks A., Losick R., Lu S., Kroos L. A forespore checkpoint for mother cell gene expression during development in B. subtilis. Cell. 1990 Jul 27;62(2):239–250. doi: 10.1016/0092-8674(90)90362-i. [DOI] [PubMed] [Google Scholar]
  4. Cutting S., Panzer S., Losick R. Regulatory studies on the promoter for a gene governing synthesis and assembly of the spore coat in Bacillus subtilis. J Mol Biol. 1989 May 20;207(2):393–404. doi: 10.1016/0022-2836(89)90262-3. [DOI] [PubMed] [Google Scholar]
  5. Halberg R., Kroos L. Fate of the SpoIIID switch protein during Bacillus subtilis sporulation depends on the mother-cell sigma factor, sigma K. J Mol Biol. 1992 Dec 5;228(3):840–849. doi: 10.1016/0022-2836(92)90868-k. [DOI] [PubMed] [Google Scholar]
  6. Jaacks K. J., Healy J., Losick R., Grossman A. D. Identification and characterization of genes controlled by the sporulation-regulatory gene spo0H in Bacillus subtilis. J Bacteriol. 1989 Aug;171(8):4121–4129. doi: 10.1128/jb.171.8.4121-4129.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Karmazyn-Campelli C., Bonamy C., Savelli B., Stragier P. Tandem genes encoding sigma-factors for consecutive steps of development in Bacillus subtilis. Genes Dev. 1989 Feb;3(2):150–157. doi: 10.1101/gad.3.2.150. [DOI] [PubMed] [Google Scholar]
  8. Kirchman P. A., DeGrazia H., Kellner E. M., Moran C. P., Jr Forespore-specific disappearance of the sigma-factor antagonist spoIIAB: implications for its role in determination of cell fate in Bacillus subtilis. Mol Microbiol. 1993 May;8(4):663–671. doi: 10.1111/j.1365-2958.1993.tb01610.x. [DOI] [PubMed] [Google Scholar]
  9. Kroos L., Kunkel B., Losick R. Switch protein alters specificity of RNA polymerase containing a compartment-specific sigma factor. Science. 1989 Jan 27;243(4890):526–529. doi: 10.1126/science.2492118. [DOI] [PubMed] [Google Scholar]
  10. Kunkel B., Kroos L., Poth H., Youngman P., Losick R. Temporal and spatial control of the mother-cell regulatory gene spoIIID of Bacillus subtilis. Genes Dev. 1989 Nov;3(11):1735–1744. doi: 10.1101/gad.3.11.1735. [DOI] [PubMed] [Google Scholar]
  11. Kunkel B., Losick R., Stragier P. The Bacillus subtilis gene for the development transcription factor sigma K is generated by excision of a dispensable DNA element containing a sporulation recombinase gene. Genes Dev. 1990 Apr;4(4):525–535. doi: 10.1101/gad.4.4.525. [DOI] [PubMed] [Google Scholar]
  12. Kunkel B., Sandman K., Panzer S., Youngman P., Losick R. The promoter for a sporulation gene in the spoIVC locus of Bacillus subtilis and its use in studies of temporal and spatial control of gene expression. J Bacteriol. 1988 Aug;170(8):3513–3522. doi: 10.1128/jb.170.8.3513-3522.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Losick R., Stragier P. Crisscross regulation of cell-type-specific gene expression during development in B. subtilis. Nature. 1992 Feb 13;355(6361):601–604. doi: 10.1038/355601a0. [DOI] [PubMed] [Google Scholar]
  14. Lu S., Halberg R., Kroos L. Processing of the mother-cell sigma factor, sigma K, may depend on events occurring in the forespore during Bacillus subtilis development. Proc Natl Acad Sci U S A. 1990 Dec;87(24):9722–9726. doi: 10.1073/pnas.87.24.9722. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Rather P. N., Coppolecchia R., DeGrazia H., Moran C. P., Jr Negative regulator of sigma G-controlled gene expression in stationary-phase Bacillus subtilis. J Bacteriol. 1990 Feb;172(2):709–715. doi: 10.1128/jb.172.2.709-715.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Sandman K., Kroos L., Cutting S., Youngman P., Losick R. Identification of the promoter for a spore coat protein gene in Bacillus subtilis and studies on the regulation of its induction at a late stage of sporulation. J Mol Biol. 1988 Apr 5;200(3):461–473. doi: 10.1016/0022-2836(88)90536-0. [DOI] [PubMed] [Google Scholar]
  17. Stragier P., Kunkel B., Kroos L., Losick R. Chromosomal rearrangement generating a composite gene for a developmental transcription factor. Science. 1989 Jan 27;243(4890):507–512. doi: 10.1126/science.2536191. [DOI] [PubMed] [Google Scholar]
  18. Yansura D. G., Henner D. J. Use of the Escherichia coli lac repressor and operator to control gene expression in Bacillus subtilis. Proc Natl Acad Sci U S A. 1984 Jan;81(2):439–443. doi: 10.1073/pnas.81.2.439. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Youngman P., Perkins J. B., Losick R. Construction of a cloning site near one end of Tn917 into which foreign DNA may be inserted without affecting transposition in Bacillus subtilis or expression of the transposon-borne erm gene. Plasmid. 1984 Jul;12(1):1–9. doi: 10.1016/0147-619x(84)90061-1. [DOI] [PubMed] [Google Scholar]
  20. Zheng L. B., Losick R. Cascade regulation of spore coat gene expression in Bacillus subtilis. J Mol Biol. 1990 Apr 20;212(4):645–660. doi: 10.1016/0022-2836(90)90227-d. [DOI] [PubMed] [Google Scholar]
  21. Zheng L., Halberg R., Roels S., Ichikawa H., Kroos L., Losick R. Sporulation regulatory protein GerE from Bacillus subtilis binds to and can activate or repress transcription from promoters for mother-cell-specific genes. J Mol Biol. 1992 Aug 20;226(4):1037–1050. doi: 10.1016/0022-2836(92)91051-p. [DOI] [PubMed] [Google Scholar]

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