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PMID: 12426398 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

MinCD-dependent regulation of the polarity of SpoIIIE assembly and DNA transfer.

The EMBO journal ·Vol. 21 ·No. 22 ·2002-11-15 ·Pages 6267-74

Sharp MD, Pogliano K

Abstract

During Bacillus subtilis sporulation, the SpoIIIE DNA translocase moves a trapped chromosome across the sporulation septum into the forespore. The direction of DNA translocation is controlled by the specific assembly of SpoIIIE in the mother cell and subsequent export of DNA into the forespore. We present evidence that the MinCD heterodimer, which spatially regulates cell division during vegetative growth, serves as a forespore-specific inhibitor of SpoIIIE assembly. The deletion of minCD increases the ability of forespore-expressed SpoIIIE to assemble and translocate DNA, and causes otherwise wild-type cells to reverse the direction of DNA transfer, producing anucleate forespores. We propose that two distinct mechanisms ensure the specific assembly of SpoIIIE in the mother cell, the partitioning of more SpoIIIE molecules into the larger mother cell by asymmetric cell division and the MinCD-dependent repression of SpoIIIE assembly in the forespore. Our results suggest that the ability of MinCD to sense positional information is utilized during sporulation to regulate protein assembly differentially on the two faces of the sporulation septum.

MeSH Terms
Adenosine Triphosphatases/deficiency,genetics,physiology Bacillus subtilis/genetics,physiology,ultrastructure Bacterial Proteins/genetics,metabolism,physiology Cell Division Cell Polarity/physiology Chromosomes, Bacterial Escherichia coli Proteins Macromolecular Substances Recombinant Fusion Proteins/metabolism Sequence Deletion Sigma Factor Spores, Bacterial Transcription Factors
Chemicals
Bacterial Proteins Escherichia coli Proteins Macromolecular Substances MinC protein, Bacteria Recombinant Fusion Proteins Sigma Factor Transcription Factors spoIIR protein, Bacillus subtilis spore-specific proteins, Bacillus Adenosine Triphosphatases MinD protein, E coli
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Sharp Marc D
Division of Biological Sciences, University of California, San Diego, 9500 Gilman Drive, La Jolla, CA 92093-0349, USA.
Pogliano Kit
References (42)
42 references, click to expand
  1. Identification of Bacillus subtilis genes for septum placement and shape determination.
    J Bacteriol. 1992 Nov;174(21):6717-28 PMID: 1400224
  2. A three-protein inhibitor of polar septation during sporulation in Bacillus subtilis.
    Mol Microbiol. 2001 Dec;42(5):1147-62 PMID: 11886548
  3. Cell division in Escherichia coli minB mutants.
    Mol Microbiol. 1992 Aug;6(15):2073-83 PMID: 1406249
  4. Bacillus subtilis SpoIIIE protein required for DNA segregation during asymmetric cell division.
    Science. 1994 Apr 22;264(5158):572-5 PMID: 8160014
  5. 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
  6. A conjugation-like mechanism for prespore chromosome partitioning during sporulation in Bacillus subtilis.
    Genes Dev. 1995 Jun 1;9(11):1316-26 PMID: 7797072
  7. Localization of protein implicated in establishment of cell type to sites of asymmetric division.
    Science. 1995 Oct 27;270(5236):637-40 PMID: 7570022
  8. 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
  9. 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
  10. FACS-optimized mutants of the green fluorescent protein (GFP).
    Gene. 1996;173(1 Spec No):33-8 PMID: 8707053
  11. Visualization of the subcellular location of sporulation proteins in Bacillus subtilis using immunofluorescence microscopy.
    Mol Microbiol. 1995 Nov;18(3):459-70 PMID: 8748030
  12. Plasmids for ectopic integration in Bacillus subtilis.
    Gene. 1996 Nov 21;180(1-2):57-61 PMID: 8973347
  13. Topological regulation of cell division in Escherichia coli involves rapid pole to pole oscillation of the division inhibitor MinC under the control of MinD and MinE.
    Mol Microbiol. 1999 Oct;34(1):82-90 PMID: 10540287
  14. An in vivo membrane fusion assay implicates SpoIIIE in the final stages of engulfment during Bacillus subtilis sporulation.
    Proc Natl Acad Sci U S A. 1999 Dec 7;96(25):14553-8 PMID: 10588743
  15. The MinC component of the division site selection system in Escherichia coli interacts with FtsZ to prevent polymerization.
    Proc Natl Acad Sci U S A. 1999 Dec 21;96(26):14819-24 PMID: 10611296
  16. The chromosomal location of the Bacillus subtilis sporulation gene spoIIR is important for its function.
    J Bacteriol. 2000 Aug;182(16):4425-9 PMID: 10913074
  17. Role of Bacillus subtilis SpoIIIE in DNA transport across the mother cell-prespore division septum.
    Science. 2000 Nov 3;290(5493):995-7 PMID: 11062134
  18. Chromosomal organization governs the timing of cell type-specific gene expression required for spore formation in Bacillus subtilis.
    Mol Microbiol. 2001 Mar;39(6):1471-81 PMID: 11260465
  19. DNA transport in bacteria.
    Nat Rev Mol Cell Biol. 2001 Jul;2(7):538-45 PMID: 11433368
  20. Division site selection protein DivIVA of Bacillus subtilis has a second distinct function in chromosome segregation during sporulation.
    Genes Dev. 2001 Jul 1;15(13):1662-73 PMID: 11445541
  21. Polar explorers: membrane proteins that determine division site placement.
    Cell. 2001 Jul 13;106(1):13-6 PMID: 11461697
  22. Differential gene expression governed by chromosomal spatial asymmetry.
    Cell. 2001 Nov 2;107(3):339-46 PMID: 11701124
  23. Spatial regulation of cytokinesis in bacteria.
    Curr Opin Microbiol. 2001 Dec;4(6):647-52 PMID: 11731315
  24. Role of cell-specific SpoIIIE assembly in polarity of DNA transfer.
    Science. 2002 Jan 4;295(5552):137-9 PMID: 11778051
  25. Partitioning of chromosomal DNA during establishment of cellular asymmetry in Bacillus subtilis.
    J Bacteriol. 2002 Mar;184(6):1743-9 PMID: 11872726
  26. Asymmetric cell division in B. subtilis involves a spiral-like intermediate of the cytokinetic protein FtsZ.
    Cell. 2002 Apr 19;109(2):257-66 PMID: 12007411
  27. Evidence from terminal recombination gradients that FtsK uses replichore polarity to control chromosome terminus positioning at division in Escherichia coli.
    J Bacteriol. 2002 Jul;184(14):3801-7 PMID: 12081949
  28. Commitment to sporulation in Bacillus subtilis and its relationship to development of actinomycin resistance.
    Biochem J. 1969 Jun;113(1):29-37 PMID: 4185146
  29. A division inhibitor and a topological specificity factor coded for by the minicell locus determine proper placement of the division septum in E. coli.
    Cell. 1989 Feb 24;56(4):641-9 PMID: 2645057
  30. The Escherichia coli minB mutation resembles gyrB in defective nucleoid segregation and decreased negative supercoiling of plasmids.
    Mol Gen Genet. 1990 Mar;221(1):87-93 PMID: 2183010
  31. 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.
    J Bacteriol. 1997 May;179(10):3331-41 PMID: 9150232
  32. Septal localization of the SpoIIIE chromosome partitioning protein in Bacillus subtilis.
    EMBO J. 1997 Apr 15;16(8):2161-9 PMID: 9155041
  33. The Bacillus subtilis DivIVA protein targets to the division septum and controls the site specificity of cell division.
    Mol Microbiol. 1997 Jun;24(5):905-15 PMID: 9219999
  34. Polar localization of the MinD protein of Bacillus subtilis and its role in selection of the mid-cell division site.
    Genes Dev. 1998 Nov 1;12(21):3419-30 PMID: 9808628
  35. A vital stain for studying membrane dynamics in bacteria: a novel mechanism controlling septation during Bacillus subtilis sporulation.
    Mol Microbiol. 1999 Feb;31(4):1149-59 PMID: 10096082
  36. Rapid pole-to-pole oscillation of a protein required for directing division to the middle of Escherichia coli.
    Proc Natl Acad Sci U S A. 1999 Apr 27;96(9):4971-6 PMID: 10220403
  37. Selection of the midcell division site in Bacillus subtilis through MinD-dependent polar localization and activation of MinC.
    Mol Microbiol. 1999 Jul;33(1):84-96 PMID: 10411726
  38. MinDE-dependent pole-to-pole oscillation of division inhibitor MinC in Escherichia coli.
    J Bacteriol. 1999 Oct;181(20):6419-24 PMID: 10515933
  39. [MORPHOLOGIC STUDY OF THE SPORULATION OF BACILLUS SUBTILIS].
    Ann Inst Pasteur (Paris). 1965 Jan;108:40-60 PMID: 14289982
  40. Condensation of the forespore nucleoid early in sporulation of Bacillus species.
    J Bacteriol. 1991 Oct;173(19):6270-8 PMID: 1917859
  41. Genetic analysis in Bacillus subtilis.
    Methods Enzymol. 1991;204:305-20 PMID: 1943780
  42. The divIVB region of the Bacillus subtilis chromosome encodes homologs of Escherichia coli septum placement (minCD) and cell shape (mreBCD) determinants.
    J Bacteriol. 1992 Nov;174(21):6729-42 PMID: 1400225
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
2002-11-15
Pages
6267-74
Language
English
Region
England
NLM ID
8208664
PMCID
PMC137189
Subset
IM
Grants
NIGMS NIH HHS · R01 GM057045 · United States
NIGMS NIH HHS · GM 57045 · United States
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