Home LiteratureArticle Details
PMID: 9150232 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Disappearance of the sigma E transcription factor from the forespore and the SpoIIE phosphatase from the mother cell contributes to establishment of cell-specific gene expression during sporulation in Bacillus subtilis.

Journal of bacteriology ·Vol. 179 ·No. 10 ·1997-05-00 ·Pages 3331-41

Pogliano K, Hofmeister AE, Losick R

Abstract

We used immunofluorescence microscopy to investigate mechanisms governing the establishment of cell-specific gene transcription during sporulation in the bacterium Bacillus subtilis. The transcription factors sigma E and sigma F are synthesized shortly after the start of sporulation but do not become active in directing gene transcription until after polar division, when the activity of sigma E is confined to the mother cell and the activity of sigma F is restricted to the forespore. We show that shortly after septation, sigma E and its proprotein precursor pro-sigma E appear to be absent from the forespore and that a null mutation in spoIIIE, a gene known to be required for the translocation of a chromosome into the forespore, allows sigma E and/or pro-sigma E to persist and sigma E to become active in the forespore. These findings suggest that the loss of sigma E/pro-sigma E from the forespore contributes to the compartmentalization of sigma E-directed gene transcription. We also investigated the distribution of SpoIIE, a regulatory phosphatase required for the activation of sigma F which exhibits a bipolar pattern of localization shortly after the start of sporulation. Normally, SpoIIE rapidly disappears from the sporangium, first from the mother-cell pole and then from the forespore pole. Here we show that a null mutation in spoIIIE causes the SpoIIE phosphatase to persist at both poles. The persistence of the SpoIIE phosphatase at the mother-cell pole could explain the lack of compartmentalization of sigma F activity observed in a spoIIIE null mutant. We conclude that the establishment of cell-specific gene transcription involves the loss of sigma E/pro-sigma E from the forespore and the loss of the SpoIIE phosphatase from the mother-cell pole and that both processes are dependent upon the SpoIIIE protein.

MeSH Terms
Bacillus subtilis/enzymology,genetics,metabolism,physiology Bacterial Proteins/genetics Cell Compartmentation/genetics Gene Expression Regulation, Bacterial/physiology Mutagenesis, Insertional Phosphoprotein Phosphatases/genetics,metabolism Sigma Factor/genetics,physiology Spores, Bacterial/enzymology,genetics Transcription Factors/genetics,physiology
Chemicals
Bacterial Proteins Sigma Factor Transcription Factors spoIIR protein, Bacillus subtilis spore-specific proteins, Bacillus sporulation-specific sigma factors Phosphoprotein Phosphatases
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Pogliano K
Department of Molecular and Cellular Biology, Harvard University, Cambridge, Massachusetts 02138, USA.
Hofmeister A E
Losick R
References (39)
39 references, click to expand
  1. Analysis of the role of prespore gene expression in the compartmentalization of mother cell-specific gene expression during sporulation of Bacillus subtilis.
    J Bacteriol. 1996 May;178(10):2813-7 PMID: 8631668
  2. [MORPHOLOGIC STUDY OF THE SPORULATION OF BACILLUS SUBTILIS].
    Ann Inst Pasteur (Paris). 1965 Jan;108:40-60 PMID: 14289982
  3. Genetic aspects of bacterial endospore formation.
    Bacteriol Rev. 1976 Dec;40(4):908-62 PMID: 12736
  4. A novel method for the rapid cloning in Escherichia coli of Bacillus subtilis chromosomal DNA adjacent to Tn917 insertions.
    Mol Gen Genet. 1984;195(3):424-33 PMID: 6088944
  5. Synthesis of sigma 29, an RNA polymerase specificity determinant, is a developmentally regulated event in Bacillus subtilis.
    J Bacteriol. 1985 Jan;161(1):340-6 PMID: 3918005
  6. 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):1784-8 PMID: 3104904
  7. The Bacillus subtilis spoIIG operon encodes both sigma E and a gene necessary for sigma E activation.
    J Bacteriol. 1988 Feb;170(2):507-11 PMID: 2448286
  8. Processing of a sporulation sigma factor in Bacillus subtilis: how morphological structure could control gene expression.
    Cell. 1988 Mar 11;52(5):697-704 PMID: 3125985
  9. 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):461-73 PMID: 3135411
  10. Condensation of the forespore nucleoid early in sporulation of Bacillus species.
    J Bacteriol. 1991 Oct;173(19):6270-8 PMID: 1917859
  11. Crisscross regulation of cell-type-specific gene expression during development in B. subtilis.
    Nature. 1992 Feb 13;355(6361):601-4 PMID: 1538747
  12. SpoIIAB is an anti-sigma factor that binds to and inhibits transcription by regulatory protein sigma F from Bacillus subtilis.
    Proc Natl Acad Sci U S A. 1993 Mar 15;90(6):2325-9 PMID: 8460142
  13. Bacillus subtilis spoVE gene is transcribed by sigma E-associated RNA polymerase.
    J Bacteriol. 1993 Jul;175(13):4081-6 PMID: 8320224
  14. Sigma F, the first compartment-specific transcription factor of B. subtilis, is regulated by an anti-sigma factor that is also a protein kinase.
    Cell. 1993 Aug 27;74(4):735-42 PMID: 8358793
  15. Bacillus subtilis SpoIIIE protein required for DNA segregation during asymmetric cell division.
    Science. 1994 Apr 22;264(5158):572-5 PMID: 8160014
  16. An adenosine nucleotide switch controlling the activity of a cell type-specific transcription factor in B. subtilis.
    Cell. 1994 Apr 22;77(2):195-205 PMID: 8168129
  17. Sigma factors, asymmetry, and the determination of cell fate in Bacillus subtilis.
    Proc Natl Acad Sci U S A. 1994 Apr 26;91(9):3849-53 PMID: 8171000
  18. Role of interactions between SpoIIAA and SpoIIAB in regulating cell-specific transcription factor sigma F of Bacillus subtilis.
    Genes Dev. 1994 Nov 1;8(21):2653-63 PMID: 7958923
  19. Isolation of a Bacillus subtilis spoIIGA allele that suppresses processing-negative mutations in the Pro-sigma E gene (sigE).
    J Bacteriol. 1994 Dec;176(24):7763-6 PMID: 8002606
  20. Cell-cell signaling pathway activating a developmental transcription factor in Bacillus subtilis.
    Genes Dev. 1995 Feb 15;9(4):503-8 PMID: 7883171
  21. Identification of a gene, spoIIR, that links the activation of sigma E to the transcriptional activity of sigma F during sporulation in Bacillus subtilis.
    Proc Natl Acad Sci U S A. 1995 Mar 14;92(6):2012-6 PMID: 7892217
  22. Use of immunofluorescence to visualize cell-specific gene expression during sporulation in Bacillus subtilis.
    J Bacteriol. 1995 Jun;177(12):3386-93 PMID: 7768847
  23. A conjugation-like mechanism for prespore chromosome partitioning during sporulation in Bacillus subtilis.
    Genes Dev. 1995 Jun 1;9(11):1316-26 PMID: 7797072
  24. Extracellular signal protein triggering the proteolytic activation of a developmental transcription factor in B. subtilis.
    Cell. 1995 Oct 20;83(2):219-26 PMID: 7585939
  25. Localization of protein implicated in establishment of cell type to sites of asymmetric division.
    Science. 1995 Oct 27;270(5236):637-40 PMID: 7570022
  26. Activation of cell-specific transcription by a serine phosphatase at the site of asymmetric division.
    Science. 1995 Oct 27;270(5236):641-4 PMID: 7570023
  27. Transcription factor Spo0A switches the localization of the cell division protein FtsZ from a medial to a bipolar pattern in Bacillus subtilis.
    Genes Dev. 1996 Feb 15;10(4):478-88 PMID: 8600030
  28. Bifunctional protein required for asymmetric cell division and cell-specific transcription in Bacillus subtilis.
    Genes Dev. 1996 Apr 1;10(7):794-803 PMID: 8846916
  29. SpoIIE governs the phosphorylation state of a protein regulating transcription factor sigma F during sporulation in Bacillus subtilis.
    Proc Natl Acad Sci U S A. 1996 Apr 16;93(8):3238-42 PMID: 8622920
  30. Isolation of an ftsZ homolog from the archaebacterium Halobacterium salinarium: implications for the evolution of FtsZ and tubulin.
    J Bacteriol. 1996 Mar;178(5):1320-7 PMID: 8631708
  31. Cell cycle-controlled proteolysis of a flagellar motor protein that is asymmetrically distributed in the Caulobacter predivisional cell.
    EMBO J. 1996 May 15;15(10):2393-406 PMID: 8665847
  32. Structure and function of the Bacillus SpoIIE protein and its localization to sites of sporulation septum assembly.
    Mol Microbiol. 1996 Mar;19(5):1047-60 PMID: 8830262
  33. SpoIIAA governs the release of the cell-type specific transcription factor sigma F from its anti-sigma factor SpoIIAB.
    J Mol Biol. 1996 Jul 12;260(2):147-64 PMID: 8764397
  34. Visualization of the subcellular location of sporulation proteins in Bacillus subtilis using immunofluorescence microscopy.
    Mol Microbiol. 1995 Nov;18(3):459-70 PMID: 8748030
  35. FtsZ ring: the eubacterial division apparatus conserved in archaebacteria.
    Mol Microbiol. 1996 Jul;21(2):313-9 PMID: 8858586
  36. Molecular genetics of sporulation in Bacillus subtilis.
    Annu Rev Genet. 1996;30:297-41 PMID: 8982457
  37. Compartmentalized distribution of the proteins controlling the prespore-specific transcription factor sigmaF of Bacillus subtilis.
    Genes Cells. 1996 Oct;1(10):881-94 PMID: 9077448
  38. Septal localization of the SpoIIIE chromosome partitioning protein in Bacillus subtilis.
    EMBO J. 1997 Apr 15;16(8):2161-9 PMID: 9155041
  39. Commitment to sporulation in Bacillus subtilis and its relationship to development of actinomycin resistance.
    Biochem J. 1969 Jun;113(1):29-37 PMID: 4185146
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
1997-05-00
Pages
3331-41
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC179115
Subset
IM
Grants
NIGMS NIH HHS · GM18568 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]