PMCCPMCCPMCC

Search tips
Search criteria 

Advanced

 
Logo of jbacterPermissionsJournals.ASM.orgJournalJB ArticleJournal InfoAuthorsReviewers
 
J Bacteriol. 1997 November; 179(21): 6788–6797.
PMCID: PMC179610

Interactions between heterologous FtsA and FtsZ proteins at the FtsZ ring.

Abstract

FtsZ and FtsA are essential for cell division in Escherichia coli and colocalize to the septal ring. One approach to determine what regions of FtsA and FtsZ are important for their interaction is to identify in vivo interactions between FtsA and FtsZ from different species. As a first step, the ftsA genes of Rhizobium meliloti and Agrobacterium tumefaciens were isolated and characterized. In addition, an FtsZ homolog that shared the unusual C-terminal extension of R. meliloti FtsZ1 was found in A. tumefaciens. In order to visualize their localization in cells, we tagged these proteins with green fluorescent protein (GFP). When R. meliloti FtsZ1-GFP or A. tumefaciens FtsZ-GFP was expressed at low levels in E. coli, they specifically localized only to the E. coli FtsZ ring, possibly by coassembly. When A. tumefaciens FtsA-GFP or R. meliloti FtsA-GFP was expressed in E. coli, they failed to localize detectably to the E. coli FtsZ ring. However, when R. meliloti FtsZ1 was coexpressed with them, fluorescence localized to a band at the midcell division site, strongly suggesting that FtsA from either A. tumefaciens or R. meliloti can bind directly to its cognate FtsZ. As expected, GFP-tagged FtsZ1 and FtsA from either R. meliloti or A. tumefaciens localized to the division site in A. tumefaciens cells. Therefore, the 61 amino acid changes between A. tumefaciens FtsA and R. meliloti FtsA do not prevent their direct interaction with FtsZ1 from either species, suggesting that those residues are not essential for protein-protein contacts. Moreover, the failure of the two non-E. coli FtsA derivatives to interact strongly with E. coli FtsZ in this in vivo system unless their cognate FtsZ was also present suggests that FtsA-FtsZ interactions have coevolved and that the residues which differ between the E. coli proteins and those of the two other species may be important for specific interactions.

Full Text

The Full Text of this article is available as a PDF (895K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Addinall SG, Bi E, Lutkenhaus J. FtsZ ring formation in fts mutants. J Bacteriol. 1996 Jul;178(13):3877–3884. [PMC free article] [PubMed]
  • Addinall SG, Lutkenhaus J. FtsA is localized to the septum in an FtsZ-dependent manner. J Bacteriol. 1996 Dec;178(24):7167–7172. [PMC free article] [PubMed]
  • Baumann P, Jackson SP. An archaebacterial homologue of the essential eubacterial cell division protein FtsZ. Proc Natl Acad Sci U S A. 1996 Jun 25;93(13):6726–6730. [PubMed]
  • Beall B, Lowe M, Lutkenhaus J. Cloning and characterization of Bacillus subtilis homologs of Escherichia coli cell division genes ftsZ and ftsA. J Bacteriol. 1988 Oct;170(10):4855–4864. [PMC free article] [PubMed]
  • Berger BR, Christie PJ. The Agrobacterium tumefaciens virB4 gene product is an essential virulence protein requiring an intact nucleoside triphosphate-binding domain. J Bacteriol. 1993 Mar;175(6):1723–1734. [PMC free article] [PubMed]
  • Bi EF, Lutkenhaus J. FtsZ ring structure associated with division in Escherichia coli. Nature. 1991 Nov 14;354(6349):161–164. [PubMed]
  • Bork P, Sander C, Valencia A. An ATPase domain common to prokaryotic cell cycle proteins, sugar kinases, actin, and hsp70 heat shock proteins. Proc Natl Acad Sci U S A. 1992 Aug 15;89(16):7290–7294. [PubMed]
  • Chen CY, Winans SC. Controlled expression of the transcriptional activator gene virG in Agrobacterium tumefaciens by using the Escherichia coli lac promoter. J Bacteriol. 1991 Feb;173(3):1139–1144. [PMC free article] [PubMed]
  • Cook WR, Rothfield LI. Development of the cell-division site in FtsA- filaments. Mol Microbiol. 1994 Nov;14(3):497–503. [PubMed]
  • Cormack BP, Valdivia RH, Falkow S. FACS-optimized mutants of the green fluorescent protein (GFP). Gene. 1996;173(1 Spec No):33–38. [PubMed]
  • Corton JC, Ward JE, Jr, Lutkenhaus J. Analysis of cell division gene ftsZ (sulB) from gram-negative and gram-positive bacteria. J Bacteriol. 1987 Jan;169(1):1–7. [PMC free article] [PubMed]
  • Dai K, Lutkenhaus J. ftsZ is an essential cell division gene in Escherichia coli. J Bacteriol. 1991 Jun;173(11):3500–3506. [PMC free article] [PubMed]
  • Dai K, Lutkenhaus J. The proper ratio of FtsZ to FtsA is required for cell division to occur in Escherichia coli. J Bacteriol. 1992 Oct;174(19):6145–6151. [PMC free article] [PubMed]
  • Dai K, Xu Y, Lutkenhaus J. Cloning and characterization of ftsN, an essential cell division gene in Escherichia coli isolated as a multicopy suppressor of ftsA12(Ts). J Bacteriol. 1993 Jun;175(12):3790–3797. [PMC free article] [PubMed]
  • de Boer P, Crossley R, Rothfield L. The essential bacterial cell-division protein FtsZ is a GTPase. Nature. 1992 Sep 17;359(6392):254–256. [PubMed]
  • Descoteaux A, Drapeau GR. Regulation of cell division in Escherichia coli K-12: probable interactions among proteins FtsQ, FtsA, and FtsZ. J Bacteriol. 1987 May;169(5):1938–1942. [PMC free article] [PubMed]
  • Devereux J, Haeberli P, Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. [PMC free article] [PubMed]
  • Dewar SJ, Begg KJ, Donachie WD. Inhibition of cell division initiation by an imbalance in the ratio of FtsA to FtsZ. J Bacteriol. 1992 Oct;174(19):6314–6316. [PMC free article] [PubMed]
  • Doi M, Wachi M, Ishino F, Tomioka S, Ito M, Sakagami Y, Suzuki A, Matsuhashi M. Determinations of the DNA sequence of the mreB gene and of the gene products of the mre region that function in formation of the rod shape of Escherichia coli cells. J Bacteriol. 1988 Oct;170(10):4619–4624. [PMC free article] [PubMed]
  • Donachie WD, Begg KJ, Lutkenhaus JF, Salmond GP, Martinez-Salas E, Vincente M. Role of the ftsA gene product in control of Escherichia coli cell division. J Bacteriol. 1979 Nov;140(2):388–394. [PMC free article] [PubMed]
  • Erickson HP, Taylor DW, Taylor KA, Bramhill D. Bacterial cell division protein FtsZ assembles into protofilament sheets and minirings, structural homologs of tubulin polymers. Proc Natl Acad Sci U S A. 1996 Jan 9;93(1):519–523. [PubMed]
  • Hale CA, de Boer PA. Direct binding of FtsZ to ZipA, an essential component of the septal ring structure that mediates cell division in E. coli. Cell. 1997 Jan 24;88(2):175–185. [PubMed]
  • Holmes KC, Sander C, Valencia A. A new ATP-binding fold in actin, hexokinase and Hsc70. Trends Cell Biol. 1993 Feb;3(2):53–59. [PubMed]
  • Latch JN, Margolin W. Generation of buds, swellings, and branches instead of filaments after blocking the cell cycle of Rhizobium meliloti. J Bacteriol. 1997 Apr;179(7):2373–2381. [PMC free article] [PubMed]
  • Ma X, Ehrhardt DW, Margolin W. Colocalization of cell division proteins FtsZ and FtsA to cytoskeletal structures in living Escherichia coli cells by using green fluorescent protein. Proc Natl Acad Sci U S A. 1996 Nov 12;93(23):12998–13003. [PubMed]
  • Margolin W, Corbo JC, Long SR. Cloning and characterization of a Rhizobium meliloti homolog of the Escherichia coli cell division gene ftsZ. J Bacteriol. 1991 Sep;173(18):5822–5830. [PMC free article] [PubMed]
  • Margolin W, Long SR. Rhizobium meliloti contains a novel second homolog of the cell division gene ftsZ. J Bacteriol. 1994 Apr;176(7):2033–2043. [PMC free article] [PubMed]
  • Margolin W, Wang R, Kumar M. Isolation of an ftsZ homolog from the archaebacterium Halobacterium salinarium: implications for the evolution of FtsZ and tubulin. J Bacteriol. 1996 Mar;178(5):1320–1327. [PMC free article] [PubMed]
  • Mukherjee A, Dai K, Lutkenhaus J. Escherichia coli cell division protein FtsZ is a guanine nucleotide binding protein. Proc Natl Acad Sci U S A. 1993 Feb 1;90(3):1053–1057. [PubMed]
  • Pla J, Dopazo A, Vicente M. The native form of FtsA, a septal protein of Escherichia coli, is located in the cytoplasmic membrane. J Bacteriol. 1990 Sep;172(9):5097–5102. [PMC free article] [PubMed]
  • RayChaudhuri D, Park JT. Escherichia coli cell-division gene ftsZ encodes a novel GTP-binding protein. Nature. 1992 Sep 17;359(6392):251–254. [PubMed]
  • Sánchez M, Valencia A, Ferrándiz MJ, Sander C, Vicente M. Correlation between the structure and biochemical activities of FtsA, an essential cell division protein of the actin family. EMBO J. 1994 Oct 17;13(20):4919–4925. [PubMed]
  • Tormo A, Vicente M. The ftsA gene product participates in formation of the Escherichia coli septum structure. J Bacteriol. 1984 Mar;157(3):779–784. [PMC free article] [PubMed]
  • Vieira J, Messing J. Production of single-stranded plasmid DNA. Methods Enzymol. 1987;153:3–11. [PubMed]
  • Wang HC, Gayda RC. High-level expression of the FtsA protein inhibits cell septation in Escherichia coli K-12. J Bacteriol. 1990 Aug;172(8):4736–4740. [PMC free article] [PubMed]
  • Wang H, Gayda RC. Quantitative determination of FtsA at different growth rates in Escherichia coli using monoclonal antibodies. Mol Microbiol. 1992 Sep;6(17):2517–2524. [PubMed]
  • Wang X, Lutkenhaus J. FtsZ ring: the eubacterial division apparatus conserved in archaebacteria. Mol Microbiol. 1996 Jul;21(2):313–319. [PubMed]
  • Yi QM, Rockenbach S, Ward JE, Jr, Lutkenhaus J. Structure and expression of the cell division genes ftsQ, ftsA and ftsZ. J Mol Biol. 1985 Aug 5;184(3):399–412. [PubMed]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)