Skip to main content
PMC home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1991 Nov 15;88(22):9934–9938. doi: 10.1073/pnas.88.22.9934

Compartmentalized expression of a gene under the control of sporulation transcription factor sigma E in Bacillus subtilis.

A Driks 1, R Losick 1
PMCID: PMC52841  PMID: 1946462

Abstract

Immunoelectron microscopy was used to visualize the expression of a gene under the control of developmental transcription factor sigma E during spore formation in Bacillus subtilis. sigma E is generated by cleavage of an inactive proprotein (pro-sigma E) shortly after the formation of the sporulation septum, which partitions the sporangium into mother-cell and forespore compartments. Specific antibodies and gold-conjugated secondary antibodies were used to localize beta-galactosidase in thin sections of sporangia from cells bearing a lacZ transcriptional fusion to a gene (spoIID) under the direct control of sigma E. Transcription of spoIID was found to be induced shortly after the formation of the sporulation septum and was largely confined to the mother cell. Cell-type-specific transcription of genes under the control of sigma E could be responsible for establishing the mother-cell line of gene expression.

Full text

PDF
9935

Images in this article

9936Image
on p.9936
9937Image
on p.9937

Selected References

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

  1. Beall B., Lutkenhaus J. FtsZ in Bacillus subtilis is required for vegetative septation and for asymmetric septation during sporulation. Genes Dev. 1991 Mar;5(3):447–455. doi: 10.1101/gad.5.3.447. [DOI] [PubMed] [Google Scholar]
  2. Carlson H. C., Haldenwang W. G. The sigma E subunit of Bacillus subtilis RNA polymerase is present in both forespore and mother cell compartments. J Bacteriol. 1989 Apr;171(4):2216–2218. doi: 10.1128/jb.171.4.2216-2218.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Clarke S., Lopez-Diaz I., Mandelstam J. Use of lacZ gene fusions to determine the dependence pattern of the sporulation gene spoIID in spo mutants of Bacillus subtilis. J Gen Microbiol. 1986 Nov;132(11):2987–2994. doi: 10.1099/00221287-132-11-2987. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. 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]
  6. 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]
  7. Gholamhoseinian A., Piggot P. J. Timing of spoII gene expression relative to septum formation during sporulation of Bacillus subtilis. J Bacteriol. 1989 Oct;171(10):5747–5749. doi: 10.1128/jb.171.10.5747-5749.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Illing N., Errington J. Genetic regulation of morphogenesis in Bacillus subtilis: roles of sigma E and sigma F in prespore engulfment. J Bacteriol. 1991 May;173(10):3159–3169. doi: 10.1128/jb.173.10.3159-3169.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Jonas R. M., Haldenwang W. G. Influence of spo mutations on sigma E synthesis in Bacillus subtilis. J Bacteriol. 1989 Sep;171(9):5226–5228. doi: 10.1128/jb.171.9.5226-5228.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Jonas R. M., Peters H. K., 3rd, Haldenwang W. G. Phenotypes of Bacillus subtilis mutants altered in the precursor-specific region of sigma E. J Bacteriol. 1990 Aug;172(8):4178–4186. doi: 10.1128/jb.172.8.4178-4186.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Jonas R. M., Weaver E. A., Kenney T. J., Moran C. P., Jr, Haldenwang W. G. The Bacillus subtilis spoIIG operon encodes both sigma E and a gene necessary for sigma E activation. J Bacteriol. 1988 Feb;170(2):507–511. doi: 10.1128/jb.170.2.507-511.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. 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]
  14. LaBell T. L., Trempy J. E., Haldenwang W. G. Sporulation-specific sigma factor sigma 29 of Bacillus subtilis is synthesized from a precursor protein, P31. Proc Natl Acad Sci U S A. 1987 Apr;84(7):1784–1788. doi: 10.1073/pnas.84.7.1784. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Losick R., Youngman P., Piggot P. J. Genetics of endospore formation in Bacillus subtilis. Annu Rev Genet. 1986;20:625–669. doi: 10.1146/annurev.ge.20.120186.003205. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. Mason J. M., Hackett R. H., Setlow P. Regulation of expression of genes coding for small, acid-soluble proteins of Bacillus subtilis spores: studies using lacZ gene fusions. J Bacteriol. 1988 Jan;170(1):239–244. doi: 10.1128/jb.170.1.239-244.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Panzer S., Losick R., Sun D., Setlow P. Evidence for an additional temporal class of gene expression in the forespore compartment of sporulating Bacillus subtilis. J Bacteriol. 1989 Jan;171(1):561–564. doi: 10.1128/jb.171.1.561-564.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Rong S., Rosenkrantz M. S., Sonenshein A. L. Transcriptional control of the Bacillus subtilis spoIID gene. J Bacteriol. 1986 Mar;165(3):771–779. doi: 10.1128/jb.165.3.771-779.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. Schmidt R., Margolis P., Duncan L., Coppolecchia R., Moran C. P., Jr, Losick R. Control of developmental transcription factor sigma F by sporulation regulatory proteins SpoIIAA and SpoIIAB in Bacillus subtilis. Proc Natl Acad Sci U S A. 1990 Dec;87(23):9221–9225. doi: 10.1073/pnas.87.23.9221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Stevens C. M., Errington J. Differential gene expression during sporulation in Bacillus subtilis: structure and regulation of the spoIIID gene. Mol Microbiol. 1990 Apr;4(4):543–551. doi: 10.1111/j.1365-2958.1990.tb00622.x. [DOI] [PubMed] [Google Scholar]
  23. Stragier P., Bonamy C., Karmazyn-Campelli C. Processing of a sporulation sigma factor in Bacillus subtilis: how morphological structure could control gene expression. Cell. 1988 Mar 11;52(5):697–704. doi: 10.1016/0092-8674(88)90407-2. [DOI] [PubMed] [Google Scholar]
  24. Stragier P., Bouvier J., Bonamy C., Szulmajster J. A developmental gene product of Bacillus subtilis homologous to the sigma factor of Escherichia coli. Nature. 1984 Nov 22;312(5992):376–378. doi: 10.1038/312376a0. [DOI] [PubMed] [Google Scholar]
  25. Stragier P., Losick R. Cascades of sigma factors revisited. Mol Microbiol. 1990 Nov;4(11):1801–1806. doi: 10.1111/j.1365-2958.1990.tb02028.x. [DOI] [PubMed] [Google Scholar]
  26. Sun D. X., Stragier P., Setlow P. Identification of a new sigma-factor involved in compartmentalized gene expression during sporulation of Bacillus subtilis. Genes Dev. 1989 Feb;3(2):141–149. doi: 10.1101/gad.3.2.141. [DOI] [PubMed] [Google Scholar]
  27. Trempy J. E., Bonamy C., Szulmajster J., Haldenwang W. G. Bacillus subtilis sigma factor sigma 29 is the product of the sporulation-essential gene spoIIG. Proc Natl Acad Sci U S A. 1985 Jun;82(12):4189–4192. doi: 10.1073/pnas.82.12.4189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Trempy J. E., Morrison-Plummer J., Haldenwang W. G. Synthesis of sigma 29, an RNA polymerase specificity determinant, is a developmentally regulated event in Bacillus subtilis. J Bacteriol. 1985 Jan;161(1):340–346. doi: 10.1128/jb.161.1.340-346.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. 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]
  30. de Lencastre H., Piggot P. J. Identification of different sites of expression for spo loci by transformation of Bacillus subtilis. J Gen Microbiol. 1979 Oct;114(2):377–389. doi: 10.1099/00221287-114-2-377. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES