Ordered expression of ftsQA and ftsZ during the Caulobacter crescentus cell cycle

The mechanisms by which bacterial cell division and DNA replication are co‐ordinated are still unknown. We have used the easily synchronizable bacterium Caulobacter crescentus to determine when the cell division genes ftsQ and ftsA are transcribed during the DNA replication cycle and to compare their transcription with that of ftsZ. Unlike the situation in Escherichia coli, transcription of ftsQ and ftsA does not extend into ftsZ in Caulobacter. ftsQ and ftsA are co‐transcribed by a strong promoter, PQA, present within the end of the ddl gene upstream of ftsQ. Transcription of PQA is turned on at the end of the DNA replication period, coincident with the end of the ftsZ transcription period. ftsA is also transcribed by another promoter, PA, present between ftsQ and ftsA. PA transcription is ≈10 times weaker than PQA and occurs during the DNA replication period. Transcription of ftsA by PA is sufficient for cell viability, but is not sufficient for normal cell division. When the transcription of ftsA is increased constitutively, cell division is inhibited and stalks are synthesized at aberrant positions. Thus, transcription of ftsA and ftsZ mimics their order of action in Caulobacter and proper transcription of ftsA has to be maintained for normal cell division and differentiation.

[1]  J. Wingrove,et al.  Spatial and temporal phosphorylation of a transcriptional activator regulates pole-specific gene expression in Caulobacter. , 1993, Genes & development.

[2]  J. Jessee,et al.  DH11S: an Escherichia coli strain for preparation of single-stranded DNA from phagemid vectors. , 1992, BioTechniques.

[3]  R. C. Johnson,et al.  Isolation of spontaneously derived mutants of Caulobacter crescentus. , 1977, Genetics.

[4]  B. Ely DNA sequence of the 3' end of the Caulobacter crescentus 16S rRNA gene. , 1992, Nucleic Acids Research.

[5]  N. Agabian,et al.  Envelope-associated nucleoid from Caulobacter crescentus stalked and swarmer cells , 1977, Journal of bacteriology.

[6]  P. Taschner,et al.  Division behavior and shape changes in isogenic ftsZ, ftsQ, ftsA, pbpB, and ftsE cell division mutants of Escherichia coli during temperature shift experiments , 1988, Journal of bacteriology.

[7]  A. Newton,et al.  Localization of surface structures during procaryotic differentiation: role of cell division in Caulobacter crescentus. , 1982, Differentiation; research in biological diversity.

[8]  J. Lutkenhaus,et al.  FtsA is localized to the septum in an FtsZ-dependent manner , 1996, Journal of bacteriology.

[9]  E. Bi,et al.  FtsZ ring formation in fts mutants , 1996, Journal of bacteriology.

[10]  H. Erickson,et al.  FtsZ, a prokaryotic homolog of tubulin? , 1995, Cell.

[11]  W. Margolin,et al.  Interactions between heterologous FtsA and FtsZ proteins at the FtsZ ring , 1997, Journal of bacteriology.

[12]  R. Losick,et al.  Cell division gene ftsQ is required for efficient sporulation but not growth and viability in Streptomyces coelicolor A3(2) , 1996, Journal of bacteriology.

[13]  R. Spiegelberg,et al.  DNA sequence and transcriptional organization of essential cell division genes ftsQ and ftsA of Escherichia coli: evidence for overlapping transcriptional units , 1984, Journal of bacteriology.

[14]  L. Shapiro,et al.  A developmentally regulated Caulobacter flagellar promoter is activated by 3' enhancer and IHF binding elements. , 1992, Molecular biology of the cell.

[15]  J. Lutkenhaus,et al.  Overproduction of FtsZ induces minicell formation in E. coli , 1985, Cell.

[16]  Y. Brun,et al.  Cell cycle regulation and cell type-specific localization of the FtsZ division initiation protein in Caulobacter. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[17]  H. Krisch,et al.  In vitro insertional mutagenesis with a selectable DNA fragment. , 1984, Gene.

[18]  J. Devereux,et al.  A comprehensive set of sequence analysis programs for the VAX , 1984, Nucleic Acids Res..

[19]  M. Aldea,et al.  Division genes in Escherichia coli are expressed coordinately to cell septum requirements by gearbox promoters. , 1990, The EMBO journal.

[20]  A. Weiss,et al.  Conservation of the 168 divIB gene in Bacillus subtilis W23 and B. licheniformis, and evidence for homology to ftsQ of Escherichia coli. , 1994, Gene.

[21]  E. Martínez-Salas,et al.  Involvement of the ftsA gene product in late stages of the Escherichia coli cell cycle , 1980, Journal of bacteriology.

[22]  M. Osley,et al.  Mutational analysis of developmental control in Caulobacter crescentus. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[23]  J. Poindexter BIOLOGICAL PROPERTIES AND CLASSIFICATION OF THE CAULOBACTER GROUP , 1964, Bacteriological reviews.

[24]  T. Baldwin,et al.  Control of cell division in Escherichia coli: regulation of transcription of ftsQA involves both rpoS and SdiA-mediated autoinduction. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[25]  L. Shapiro,et al.  Isolation and characterization of a xylose-dependent promoter from Caulobacter crescentus , 1997, Journal of bacteriology.

[26]  L. Shapiro,et al.  A temporally controlled sigma-factor is required for polar morphogenesis and normal cell division in Caulobacter. , 1992, Genes & development.

[27]  W. Donachie,et al.  Inhibition of cell division initiation by an imbalance in the ratio of FtsA to FtsZ , 1992, Journal of bacteriology.

[28]  A. Pühler,et al.  A Broad Host Range Mobilization System for In Vivo Genetic Engineering: Transposon Mutagenesis in Gram Negative Bacteria , 1983, Bio/Technology.

[29]  L. Shapiro,et al.  The expression of asymmetry during Caulobacter cell differentiation. , 1994, Annual review of biochemistry.

[30]  D. Ehrhardt,et al.  Colocalization of cell division proteins FtsZ and FtsA to cytoskeletal structures in living Escherichia coli cells by using green fluorescent protein. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[31]  B. Ely,et al.  Organization of the flaFG gene cluster and identification of two additional genes involved in flagellum biogenesis in Caulobacter crescentus , 1989, Journal of bacteriology.

[32]  N. Ohta,et al.  Signal transduction in the cell cycle regulation of Caulobacter differentiation. , 1996, Trends in microbiology.

[33]  R. A. Gustafson,et al.  Regulation of bacterial cell division: temperature-sensitive mutants of Escherichia coli that are defective in septum formation , 1975, Journal of bacteriology.

[34]  M. Winkler,et al.  Nucleotide sequence of the Caulobacter crescentus flaF and flbT genes and an analysis of codon usage in organisms with G + C-rich genomes. , 1990, Gene.

[35]  J. Beckwith,et al.  The FtsQ protein of Escherichia coli: membrane topology, abundance, and cell division phenotypes due to overproduction and insertion mutations , 1991, Journal of bacteriology.

[36]  K. Flärdh,et al.  Contribution of individual promoters in the ddlB–ftsZ region to the transcription of the essential cell‐division gene ftsZ in Escherichia coli , 1997, Molecular microbiology.

[37]  B. Spratt Temperature-Sensitive Cell Division Mutants of Escherichia coli with Thermolabile Penicillin-Binding Proteins , 1977, Journal of bacteriology.

[38]  J. Lutkenhaus,et al.  The proper ratio of FtsZ to FtsA is required for cell division to occur in Escherichia coli , 1992, Journal of bacteriology.

[39]  Y. Brun,et al.  Cell cycle-dependent transcriptional and proteolytic regulation of FtsZ in Caulobacter. , 1998, Genes & development.

[40]  B. Spratt,et al.  Kanamycin-resistant vectors that are analogues of plasmids pUC8, pUC9, pEMBL8 and pEMBL9. , 1986, Gene.

[41]  Y. Brun,et al.  Dominant C‐terminal deletions of FtsZ that affect its ability to localize in Caulobacter and its interaction with FtsA , 1998, Molecular microbiology.

[42]  W. Margolin,et al.  Generation of buds, swellings, and branches instead of filaments after blocking the cell cycle of Rhizobium meliloti , 1997, Journal of bacteriology.

[43]  C. Sander,et al.  Correlation between the structure and biochemical activities of FtsA, an essential cell division protein of the actin family. , 1994, The EMBO journal.

[44]  E. Bi,et al.  FtsZ ring structure associated with division in Escherichia coli , 1991, Nature.

[45]  W. Donachie,et al.  Morphogenes of Escherichia coli , 1984 .

[46]  E. Harry,et al.  The membrane‐bound cell division protein DivIB is localized to the division site in Bacillus subtilis , 1997, Molecular microbiology.

[47]  B Ely,et al.  A consensus promoter sequence for Caulobacter crescentus genes involved in biosynthetic and housekeeping functions , 1995, Journal of bacteriology.

[48]  W. Donachie,et al.  Cell shape and division in Escherichia coli: experiments with shape and division mutants , 1985, Journal of bacteriology.

[49]  Y. Hirota,et al.  On the process of cellular division in Escherichia coli: a series of mutants of E. coli altered in the penicillin-binding proteins. , 1978, Proceedings of the National Academy of Sciences of the United States of America.

[50]  J. Gober,et al.  Regulation of cellular differentiation in Caulobacter crescentus , 1995, Microbiological reviews.

[51]  F. Sanger,et al.  DNA sequencing with chain-terminating inhibitors. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[52]  R. Gayda,et al.  High-level expression of the FtsA protein inhibits cell septation in Escherichia coli K-12 , 1990, Journal of bacteriology.

[53]  Jeffrey H. Miller Experiments in molecular genetics , 1972 .

[54]  L. Shapiro,et al.  Expression of positional information during cell differentiation in caulobacter , 1991, Cell.

[55]  A. Ninfa,et al.  Identification, characterization, and chromosomal organization of cell division cycle genes in Caulobacter crescentus , 1997, Journal of bacteriology.

[56]  M. de Pedro,et al.  Interaction of FtsA and PBP3 proteins in the Escherichia coli septum , 1986, Journal of bacteriology.

[57]  J. Lutkenhaus,et al.  Bacterial cell division and the Z ring. , 1997, Annual review of biochemistry.