SpringerLink
Log in

Temporal Control of Promoter Activity During the Caulobacter Cell Cycle

  • Chapter
  • First Online:
Cell Cycle Regulation and Development in Alphaproteobacteria

  • 282 Accesses

Abstract

A cascade of cellular events must occur to allow cells to complete one round of cell division. Such a successful cell division cycle relies on the predetermined and sequential production of specific proteins that execute dedicated functions. Protein production is typically governed by transcriptional control occurring at the promoter of the genes encoding the proteins whose function are needed at a specific time in the cell cycle. Here we review the basis for the cell-cycle-controlled promoter activation in the synchronizable model bacterium Caulobacter crescentus, a Gram-negative alpha-proteobacterium. We detail which promoters fire at the same time and we reason why this is the case.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Chapter
EUR 29.95
Price includes VAT (Germany)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
EUR 139.09
Price includes VAT (Germany)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
EUR 181.89
Price includes VAT (Germany)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info
Hardcover Book
EUR 181.89
Price includes VAT (Germany)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  • Anderson PE, Gober JW (2000) FlbT, the post-transcriptional regulator of flagellin synthesis in Caulobacter crescentus, interacts with the 5′ untranslated region of flagellin mRNA. Mol Microbiol 38:41–52

    CAS  PubMed  Google Scholar 

  • Ardissone S, Viollier PH (2015) Interplay between flagellation and cell cycle control in Caulobacter. Curr Opin Microbiol 28:83–92

    CAS  PubMed  Google Scholar 

  • Ardissone S et al (2014) Cell cycle constraints on capsulation and bacteriophage susceptibility. elife 3:e03587

    PubMed Central  Google Scholar 

  • Ardissone S et al (2016) Cell cycle constraints and environmental control of local DNA hypomethylation in α-proteobacteria. PLoS Genet 12:e1006499

    PubMed  PubMed Central  Google Scholar 

  • Ardissone S, Kint N, Petrignani B, Panis G, Viollier PH (2020) Secretion relieves translational co-repression by a specialized flagellin paralog. Dev Cell 55(4):500–513.e4. https://doi.org/10.1016/j.devcel.2020.10.005

  • Arias-Cartin R et al (2017) Replication fork passage drives asymmetric dynamics of a critical nucleoid-associated protein in Caulobacter. EMBO J 36:301–318

    CAS  PubMed  Google Scholar 

  • Beaufay F et al (2015) A NAD-dependent glutamate dehydrogenase coordinates metabolism with cell division in Caulobacter crescentus. EMBO J 34:1786–1800

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bergkessel M, Basta DW, Newman DK (2016) The physiology of growth arrest: uniting molecular and environmental microbiology. Nat Rev Microbiol 14:549–562

    CAS  PubMed  Google Scholar 

  • Berne C et al (2018) Feedback regulation of Caulobacter crescentus holdfast synthesis by flagellum assembly via the holdfast inhibitor HfiA. Mol Microbiol 110:219–238

    CAS  PubMed  PubMed Central  Google Scholar 

  • Biondi EG et al (2006a) Regulation of the bacterial cell cycle by an integrated genetic circuit. Nature 444:899–904

    CAS  PubMed  Google Scholar 

  • Biondi EG et al (2006b) A phosphorelay system controls stalk biogenesis during cell cycle progression in Caulobacter crescentus. Mol Microbiol 59:386–401

    CAS  PubMed  Google Scholar 

  • Bodenmiller D, Toh E, Brun YV (2004) Development of surface adhesion in Caulobacter crescentus. J Bacteriol 186:1438–1447

    CAS  PubMed  PubMed Central  Google Scholar 

  • Boutte CC, Crosson S (2011) The complex logic of stringent response regulation in Caulobacter crescentus: starvation signaling in an oligotrophic environment. Mol Microbiol 80:695–714

    CAS  PubMed  PubMed Central  Google Scholar 

  • Boutte CC, Henry JT, Crosson S (2012) ppGpp and Polyphosphate Modulate Cell Cycle Progression in Caulobacter crescentus. J Bacteriol 194:28–35

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brown PJB, Hardy GG, Trimble MJ, Brun YV (2009) Complex regulatory pathways coordinate cell-cycle progression and development in Caulobacter crescentus. Adv Microb Physiol 54:1–101

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brun YV (2001) Global analysis of a bacterial cell cycle: tracking down necessary functions and their regulators. Trends Microbiol 9:405–407

    CAS  PubMed  Google Scholar 

  • Camara JE et al (2005) Hda inactivation of DnaA is the predominant mechanism preventing hyperinitiation of Escherichia coli DNA replication. EMBO Rep 6:736–741

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng Z, Miura K, Popov VL, Kumagai Y, Rikihisa Y (2011) Insights into the CtrA regulon in development of stress resistance in obligatory intracellular pathogen Ehrlichia chaffeensis. Mol Microbiol 82:1217–1234

    CAS  PubMed  PubMed Central  Google Scholar 

  • Collier J, Shapiro L (2009) Feedback control of DnaA-mediated replication initiation by replisome-associated HdaA protein in Caulobacter. J Bacteriol 191:5706–5716

    CAS  PubMed  PubMed Central  Google Scholar 

  • Collier J, Murray SR, Shapiro L (2006) DnaA couples DNA replication and the expression of two cell cycle master regulators. EMBO J 25:346–356

    CAS  PubMed  PubMed Central  Google Scholar 

  • Collier J, McAdams HH, Shapiro L (2007) A DNA methylation ratchet governs progression through a bacterial cell cycle. Proc Natl Acad Sci U S A 104:17111–17116

    CAS  PubMed  PubMed Central  Google Scholar 

  • Costa TRD et al (2015) Secretion systems in Gram-negative bacteria: structural and mechanistic insights. Nat Rev Microbiol 13:343–359

    CAS  PubMed  Google Scholar 

  • Craig L, Pique ME, Tainer JA (2004) Type IV pilus structure and bacterial pathogenicity. Nat Rev Microbiol 2:363–378

    CAS  PubMed  Google Scholar 

  • Davis NJ et al (2013) De- and repolarization mechanism of flagellar morphogenesis during a bacterial cell cycle. Genes Dev 27:2049–2062

    CAS  PubMed  PubMed Central  Google Scholar 

  • Delaby M, Panis G, Viollier PH (2019) Bacterial cell cycle and growth phase switch by the essential transcriptional regulator CtrA. Nucleic Acids Res 47(20):10628–10644. https://doi.org/10.1093/nar/gkz846

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Domian IJ, Reisenauer A, Shapiro L (1999) Feedback control of a master bacterial cell-cycle regulator. Proc Natl Acad Sci U S A 96:6648–6653

    CAS  PubMed  PubMed Central  Google Scholar 

  • Duderstadt KE, Chuang K, Berger JM (2011) DNA stretching by bacterial initiators promotes replication origin opening. Nature 478:209–213

    CAS  PubMed  PubMed Central  Google Scholar 

  • Duerig A et al (2009) Second messenger-mediated spatiotemporal control of protein degradation regulates bacterial cell cycle progression. Genes Dev 23:93–104

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ellison CK et al (2017) Obstruction of pilus retraction stimulates bacterial surface sensing. Science 358:535–538

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ely B, Ely TW (1989) Use of pulsed field gel electrophoresis and transposon mutagenesis to estimate the minimal number of genes required for motility in Caulobacter crescentus. Genetics 123:649–654

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ely B et al (1986) General nonchemotactic mutants of Caulobacter crescentus. Genetics 114:717–730

    CAS  PubMed  PubMed Central  Google Scholar 

  • Entcheva-Dimitrov P, Spormann AM (2004) Dynamics and control of biofilms of the oligotrophic bacterium Caulobacter crescentus. J Bacteriol 186:8254–8266

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fang G et al (2013) Transcriptomic and phylogenetic analysis of a bacterial cell cycle reveals strong associations between gene co-expression and evolution. BMC Genomics 14:450

    PubMed  PubMed Central  Google Scholar 

  • Felletti M, Omnus DJ, Jonas K (2019) Regulation of the replication initiator DnaA in Caulobacter crescentus. Biochim Biophys Acta Gene Regul Mech 1862(7):697–705. https://doi.org/10.1016/j.bbagrm.2018.01.004

    Article  CAS  PubMed  Google Scholar 

  • Fernandez-Fernandez C, Gonzalez D, Collier J (2011) Regulation of the Activity of the Dual-Function DnaA Protein in Caulobacter crescentus. PLoS One 6:e26028

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fiebig A et al (2014) A cell cycle and nutritional checkpoint controlling bacterial surface adhesion. PLoS Genet 10:e1004101

    PubMed  PubMed Central  Google Scholar 

  • Fioravanti A et al (2013) DNA binding of the cell cycle transcriptional regulator GcrA depends on N6-adenosine methylation in Caulobacter crescentus and other alphaproteobacteria. PLoS Genet 9:e1003541

    CAS  PubMed  PubMed Central  Google Scholar 

  • Foreman R, Fiebig A, Crosson S (2012) The LovK-LovR two-component system is a regulator of the general stress pathway in Caulobacter crescentus. J Bacteriol 194:3038–3049

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fumeaux C et al (2014) Cell cycle transition from S-phase to G1 in Caulobacter is mediated by ancestral virulence regulators. Nat Commun 5

    Google Scholar 

  • Gonzalez D, Collier J (2013) DNA methylation by CcrM activates the transcription of two genes required for the division of Caulobacter crescentus. Mol Microbiol 88:203–218

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gora KG et al (2010) A cell-type-specific protein-protein interaction modulates transcriptional activity of a master regulator in Caulobacter crescentus. Mol Cell 39:455–467

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gora KG et al (2013) Regulated proteolysis of a transcription factor complex is critical to cell cycle progression in Caulobacter crescentus. Mol Microbiol 87:1277–1289

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guo MS, Haakonsen DL, Zeng W, Schumacher MA, Laub MT (2018) A bacterial chromosome structuring protein binds overtwisted DNA to stimulate type II topoisomerases and enable DNA replication. Cell 175:583–597.e23

    CAS  PubMed  PubMed Central  Google Scholar 

  • Haakonsen DL, Yuan AH, Laub MT (2015) The bacterial cell cycle regulator GcrA is a σ70 cofactor that drives gene expression from a subset of methylated promoters. Genes Dev 29:2272–2286

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hallez R, Bellefontaine A-F, Letesson J-J, De Bolle X (2004) Morphological and functional asymmetry in alpha-proteobacteria. Trends Microbiol 12:361–365

    CAS  PubMed  Google Scholar 

  • Hallez R, Delaby M, Sanselicio S, Viollier PH (2017) Hit the right spots: cell cycle control by phosphorylated guanosines in alphaproteobacteria. Nat Rev Microbiol 15:137–148

    CAS  PubMed  Google Scholar 

  • Hickman JW, Harwood CS (2008) Identification of FleQ from Pseudomonas aeruginosa as a c-di-GMP-responsive transcription factor. Mol Microbiol 69:376–389

    CAS  PubMed  PubMed Central  Google Scholar 

  • Holtzendorff J et al (2004) Oscillating global regulators control the genetic circuit driving a bacterial cell cycle. Science 304:983–987

    CAS  PubMed  Google Scholar 

  • Hottes AK, Shapiro L, McAdams HH (2005) DnaA coordinates replication initiation and cell cycle transcription in Caulobacter crescentus. Mol Microbiol 58:1340–1353

    CAS  PubMed  Google Scholar 

  • Huitema E, Pritchard S, Matteson D, Radhakrishnan SK, Viollier PH (2006) Bacterial birth scar proteins mark future flagellum assembly site. Cell 124:1025–1037

    CAS  PubMed  Google Scholar 

  • Iniesta AA, McGrath PT, Reisenauer A, McAdams HH, Shapiro L (2006) A phospho-signaling pathway controls the localization and activity of a protease complex critical for bacterial cell cycle progression. Proc Natl Acad Sci U S A 103:10935–10940

    CAS  PubMed  PubMed Central  Google Scholar 

  • Janakiraman RS, Brun YV (1999) Cell cycle control of a holdfast attachment gene in Caulobacter crescentus. J Bacteriol 181:1118–1125

    CAS  PubMed  PubMed Central  Google Scholar 

  • Janakiraman B, Mignolet J, Narayanan S, Viollier PH, Radhakrishnan SK (2016) In-phase oscillation of global regulons is orchestrated by a pole-specific organizer. Proc Natl Acad Sci U S A 113:12550–12555

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jenal U, Fuchs T (1998) An essential protease involved in bacterial cell-cycle control. EMBO J 17:5658–5669

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jonas K, Chen YE, Laub MT (2011) Modularity of the bacterial cell cycle enables independent spatial and temporal control of DNA replication. Curr Biol 21:1092–1101

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jonas K, Liu J, Chien P, Laub MT (2013) Proteotoxic stress induces a cell-cycle arrest by stimulating Lon to degrade the replication initiator DnaA. Cell 154:623–636

    CAS  PubMed  PubMed Central  Google Scholar 

  • Joshi KK, Bergé M, Radhakrishnan SK, Viollier PH, Chien P (2015) An adaptor hierarchy regulates proteolysis during a bacterial cell cycle. Cell 163:419–431

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kaczmarczyk A, Hempel AM, von Arx C, Böhm R, Dubey BN, Nesper J, Schirmer T, Hiller S, Jenal U (2020) Precise timing of transcription by c-di-GMP coordinates cell cycle and morphogenesis in Caulobacter. Nat Commun 11(1):816. https://doi.org/10.1038/s41467-020-14585-6

  • Katayama T, Ozaki S, Keyamura K, Fujimitsu K (2010) Regulation of the replication cycle: conserved and diverse regulatory systems for DnaA and oriC. Nat Rev Microbiol 8:163–170

    CAS  PubMed  Google Scholar 

  • Kelly AJ, Sackett MJ, Din N, Quardokus E, Brun YV (1998) Cell cycle-dependent transcriptional and proteolytic regulation of FtsZ in Caulobacter. Genes Dev 12:880–893

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kiekebusch D, Michie KA, Essen L-O, Löwe J, Thanbichler M (2012) Localized dimerization and nucleoid binding drive gradient formation by the bacterial cell division inhibitor MipZ. Mol Cell 46:245–259

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lam H, Schofield WB, Jacobs-Wagner C (2006) A landmark protein essential for establishing and perpetuating the polarity of a bacterial cell. Cell 124:1011–1023

    CAS  PubMed  Google Scholar 

  • Laub MT, McAdams HH, Feldblyum T, Fraser CM, Shapiro L (2000) Global analysis of the genetic network controlling a bacterial cell cycle. Science 290:2144–2148

    CAS  PubMed  Google Scholar 

  • Laub MT, Chen SL, Shapiro L, McAdams HH (2002) Genes directly controlled by CtrA, a master regulator of the Caulobacter cell cycle. Proc Natl Acad Sci U S A 99:4632–4637

    CAS  PubMed  PubMed Central  Google Scholar 

  • Laub MT, Shapiro L, McAdams HH (2007) Systems biology of Caulobacter. Annu Rev Genet 41:429–441

    CAS  PubMed  Google Scholar 

  • Lesley JA, Shapiro L (2008) SpoT regulates DnaA stability and initiation of DNA replication in carbon-starved Caulobacter crescentus. J Bacteriol 190:6867–6880

    CAS  PubMed  PubMed Central  Google Scholar 

  • Leslie DJ et al (2015) Nutritional control of DNA replication initiation through the proteolysis and regulated translation of DnaA. PLoS Genet 11:e1005342

    PubMed  PubMed Central  Google Scholar 

  • Levi A, Jenal U (2006) Holdfast formation in motile swarmer cells optimizes surface attachment during Caulobacter crescentus development. J Bacteriol 188:5315–5318

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li S, Brazhnik P, Sobral B, Tyson JJ (2009) Temporal controls of the asymmetric cell division cycle in Caulobacter crescentus. PLoS Comput Biol 5

    Google Scholar 

  • Liu J, Francis LI, Jonas K, Laub MT, Chien P (2016) ClpAP is an auxiliary protease for DnaA degradation in Caulobacter crescentus. Mol Microbiol 102:1075–1085

    CAS  PubMed  PubMed Central  Google Scholar 

  • Llewellyn M, Dutton RJ, Easter J, O’Donnol D, Gober JW (2005) The conserved flaF gene has a critical role in coupling flagellin translation and assembly in Caulobacter crescentus. Mol Microbiol 57:1127–1142

    CAS  PubMed  Google Scholar 

  • Mangan EK et al (1999) FlbT couples flagellum assembly to gene expression in Caulobacter crescentus. J Bacteriol 181:6160–6170

    CAS  PubMed  PubMed Central  Google Scholar 

  • McGrath PT, Iniesta AA, Ryan KR, Shapiro L, McAdams HH (2006) A dynamically localized protease complex and a polar specificity factor control a cell cycle master regulator. Cell 124:535–547

    CAS  PubMed  Google Scholar 

  • McGrath PT et al (2007) High-throughput identification of transcription start sites, conserved promoter motifs and predicted regulons. Nat Biotechnol 25:584–592

    CAS  PubMed  Google Scholar 

  • Melville S, Craig L (2013) Type IV pili in Gram-positive bacteria. Microbiol Mol Biol Rev 77:323–341

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mignolet J et al (2016) Functional dichotomy and distinct nanoscale assemblies of a cell cycle-controlled bipolar zinc-finger regulator. elife 5

    Google Scholar 

  • Mignolet J, Panis G, Viollier PH (2018) More than a Tad: spatiotemporal control of Caulobacter pili. Curr Opin Microbiol 42:79–86

    CAS  PubMed  Google Scholar 

  • Mohr CD, MacKichan JK, Shapiro L (1998) A membrane-associated protein, FliX, is required for an early step in Caulobacter flagellar assembly. J Bacteriol 180:2175–2185

    CAS  PubMed  PubMed Central  Google Scholar 

  • Möll A, Thanbichler M (2009) FtsN-like proteins are conserved components of the cell division machinery in proteobacteria. Mol Microbiol 72:1037–1053

    PubMed  Google Scholar 

  • Muir RE, Gober JW (2002) Mutations in FlbD that relieve the dependency on flagellum assembly alter the temporal and spatial pattern of developmental transcription in Caulobacter crescentus. Mol Microbiol 43:597–615

    CAS  PubMed  Google Scholar 

  • Muir RE, O’Brien TM, Gober JW (2001) The Caulobacter crescentus flagellar gene, fliX, encodes a novel trans-acting factor that couples flagellar assembly to transcription. Mol Microbiol 39:1623–1637

    CAS  PubMed  Google Scholar 

  • Mullin DA, Newton A (1989) Ntr-like promoters and upstream regulatory sequence ftr are required for transcription of a developmentally regulated Caulobacter crescentus flagellar gene. J Bacteriol 171:3218–3227

    CAS  PubMed  PubMed Central  Google Scholar 

  • Murray SM, Panis G, Fumeaux C, Viollier PH, Howard M (2013) Computational and genetic reduction of a cell cycle to its simplest, primordial components. PLoS Biol 11:e1001749

    PubMed  PubMed Central  Google Scholar 

  • Nesper J et al (2017) Cyclic di-GMP differentially tunes a bacterial flagellar motor through a novel class of CheY-like regulators. elife 6:e28842

    PubMed  PubMed Central  Google Scholar 

  • Nierman WC et al (2001) Complete genome sequence of Caulobacter crescentus. Proc Natl Acad Sci U S A 98:4136–4141

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ouimet M-C, Marczynski GT (2000) Analysis of a cell-cycle promoter bound by a response regulator11Edited by M. Yaniv. J Mol Biol 302:761–775

    CAS  PubMed  Google Scholar 

  • Panis G, Murray SR, Viollier PH (2015) Versatility of global transcriptional regulators in alpha-Proteobacteria: from essential cell cycle control to ancillary functions. FEMS Microbiol Rev 39:120–133

    CAS  PubMed  Google Scholar 

  • Potrykus K, Cashel M (2008) (p)ppGpp: still magical? Annu Rev Microbiol 62:35–51

    CAS  PubMed  Google Scholar 

  • Purcell EB, Boutte CC, Crosson S (2008) Two-component signaling systems and cell cycle control in Caulobacter crescentus. Adv Exp Med Biol 631:122–130

    CAS  PubMed  Google Scholar 

  • Quon KC, Marczynski GT, Shapiro L (1996) Cell cycle control by an essential bacterial two-component signal transduction protein. Cell 84:83–93

    CAS  PubMed  Google Scholar 

  • Quon KC, Yang B, Domian IJ, Shapiro L, Marczynski GT (1998) Negative control of bacterial DNA replication by a cell cycle regulatory protein that binds at the chromosome origin. Proc Natl Acad Sci U S A 95:120–125

    CAS  PubMed  PubMed Central  Google Scholar 

  • Radhakrishnan SK, Thanbichler M, Viollier PH (2008) The dynamic interplay between a cell fate determinant and a lysozyme homolog drives the asymmetric division cycle of Caulobacter crescentus. Genes Dev 22:212–225

    CAS  PubMed  PubMed Central  Google Scholar 

  • Radhakrishnan SK, Pritchard S, Viollier PH (2010) Coupling prokaryotic cell fate and division control with a bifunctional and oscillating oxidoreductase homolog. Dev Cell 18:90–101

    CAS  PubMed  Google Scholar 

  • Ramakrishnan G, Newton A (1990) FlbD of Caulobacter crescentus is a homologue of the NtrC (NRI) protein and activates sigma 54-dependent flagellar gene promoters. Proc Natl Acad Sci U S A 87:2369–2373

    CAS  PubMed  PubMed Central  Google Scholar 

  • Reisenauer A, Quon K, Shapiro L (1999) The CtrA response regulator mediates temporal control of gene expression during the caulobacter cell cycle. J Bacteriol 181:2430–2439

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ricci DP et al (2016) Cell cycle progression in Caulobacter requires a nucleoid-associated protein with high AT sequence recognition. Proc Natl Acad Sci U S A 113:E5952–E5961

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rikihisa Y (2015) Molecular pathogenesis of Ehrlichia chaffeensis infection. Annu Rev Microbiol 69:283–304

    CAS  PubMed  Google Scholar 

  • Ronneau S, Petit K, De Bolle X, Hallez R (2016) Phosphotransferase-dependent accumulation of (p)ppGpp in response to glutamine deprivation in Caulobacter crescentus. Nat Commun 7:11423

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ronneau S et al (2019) Regulation of (p)ppGpp hydrolysis by a conserved archetypal regulatory domain. Nucleic Acids Res 47:843–854

    CAS  PubMed  Google Scholar 

  • Sackett MJ, Kelly AJ, Brun YV (1998) Ordered expression of ftsQA and ftsZ during the Caulobacter crescentus cell cycle. Mol Microbiol 28:421–434

    CAS  PubMed  Google Scholar 

  • Sanselicio S, Viollier PH (2015) Convergence of alarmone and cell cycle signaling from trans-encoded sensory domains. mBio 6:e01415-15

    PubMed  PubMed Central  Google Scholar 

  • Sanselicio S, Bergé M, Théraulaz L, Radhakrishnan SK, Viollier PH (2015) Topological control of the Caulobacter cell cycle circuitry by a polarized single-domain PAS protein. Nat Commun 6:7005

    CAS  PubMed  Google Scholar 

  • Schrader JM et al (2016) Dynamic translation regulation in Caulobacter cell cycle control. Proc Natl Acad Sci U S A 113:E6859–E6867

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shaheen SM, Ouimet M-C, Marczynski GT (2009) Comparative analysis of Caulobacter chromosome replication origins. Microbiol Read Engl 155:1215–1225

    CAS  Google Scholar 

  • Siwach M, Kumar L, Palani S, Muraleedharan S, Panis G, Fumeaux C, Mony BM, Sanyal S, Viollier PH, Radhakrishnan SK (2021) An organelle-tethering mechanism couples flagellation to cell division in bacteria. Dev Cell 56(5):657–670.e4. https://doi.org/10.1016/j.devcel.2021.01.013

    Article  CAS  PubMed  Google Scholar 

  • Skarstad K, Katayama T (2013) Regulating DNA replication in bacteria. Cold Spring Harb Perspect Biol 5:a012922

    PubMed  PubMed Central  Google Scholar 

  • Skerker JM, Laub MT (2004) Cell-cycle progression and the generation of asymmetry in Caulobacter crescentus. Nat Rev Microbiol 2:325–337

    CAS  PubMed  Google Scholar 

  • Skerker JM, Shapiro L (2000) Identification and cell cycle control of a novel pilus system in Caulobacter crescentus. EMBO J 19:3223–3234

    CAS  PubMed  PubMed Central  Google Scholar 

  • Skerker JM, Prasol MS, Perchuk BS, Biondi EG, Laub MT (2005) Two-component signal transduction pathways regulating growth and cell cycle progression in a bacterium: a system-level analysis. PLoS Biol 3:e334

    PubMed  PubMed Central  Google Scholar 

  • Smith SC et al (2014) Cell cycle-dependent adaptor complex for ClpXP-mediated proteolysis directly integrates phosphorylation and second messenger signals. Proc Natl Acad Sci U S A 111:14229–14234

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tan MH, Kozdon JB, Shen X, Shapiro L, McAdams HH (2010) An essential transcription factor, SciP, enhances robustness of Caulobacter cell cycle regulation. Proc Natl Acad Sci U S A 107:18985–18990

    CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor JA, Ouimet M-C, Wargachuk R, Marczynski GT (2011) The Caulobacter crescentus chromosome replication origin evolved two classes of weak DnaA binding sites. Mol Microbiol 82:312–326

    CAS  PubMed  Google Scholar 

  • Taylor JA, Panis G, Viollier PH, Marczynski GT (2017) A novel nucleoid-associated protein coordinates chromosome replication and chromosome partition. Nucleic Acids Res 45:8916–8929

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thanbichler M, Shapiro L (2006) MipZ, a spatial regulator coordinating chromosome segregation with cell division in Caulobacter. Cell 126:147–162

    CAS  PubMed  Google Scholar 

  • Tsokos CG, Perchuk BS, Laub MT (2011) A dynamic complex of signaling proteins uses polar localization to regulate cell-fate asymmetry in Caulobacter crescentus. Dev Cell 20:329–341

    CAS  PubMed  PubMed Central  Google Scholar 

  • Viollier PH, Sternheim N, Shapiro L (2002a) Identification of a localization factor for the polar positioning of bacterial structural and regulatory proteins. Proc Natl Acad Sci U S A 99:13831–13836

    CAS  PubMed  PubMed Central  Google Scholar 

  • Viollier PH, Sternheim N, Shapiro L (2002b) A dynamically localized histidine kinase controls the asymmetric distribution of polar pili proteins. EMBO J 21:4420–4428

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wortinger MA, Quardokus EM, Brun YV (1998) Morphological adaptation and inhibition of cell division during stationary phase in Caulobacter crescentus. Mol Microbiol 29:963–973

    CAS  PubMed  Google Scholar 

  • Wortinger M, Sackett MJ, Brun YV (2000) CtrA mediates a DNA replication checkpoint that prevents cell division in Caulobacter crescentus. EMBO J 19:4503–4512

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu J, Benson AK, Newton A (1995) Global regulation of a sigma 54-dependent flagellar gene family in Caulobacter crescentus by the transcriptional activator FlbD. J Bacteriol 177:3241–3250

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu J, Ohta N, Newton A (1998) An essential, multicomponent signal transduction pathway required for cell cycle regulation in Caulobacter. Proc Natl Acad Sci U S A 95:1443–1448

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu J, Ohta N, Zhao J-L, Newton A (1999) A novel bacterial tyrosine kinase essential for cell division and differentiation. Proc Natl Acad Sci U S A 96:13068–13073

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu X et al (2018) Structural insights into the unique mechanism of transcription activation by Caulobacter crescentus GcrA. Nucleic Acids Res 46:3245–3256

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou B et al (2015) The global regulatory architecture of transcription during the Caulobacter cell cycle. PLoS Genet 11:e1004831

    PubMed  PubMed Central  Google Scholar 

  • Zweiger G, Marczynski G, Shapiro L (1994) A Caulobacter DNA methyltransferase that functions only in the predivisional cell. J Mol Biol 235:472–485

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Faculty of Medicine, Department of Microbiology and Molecular Medicine/Centre Médical Universitaire, University of Geneva, Genève 4, Switzerland

    Marie Delaby & Patrick H. Viollier

Authors
  1. Marie Delaby
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Patrick H. Viollier
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Patrick H. Viollier .

Editor information

Editors and Affiliations

  1. CNRS, Institute for Integrative Biology of the Cell, Gif sur Yvette, France

    Emanuele Biondi

Rights and permissions

Reprints and permissions

Copyright information

© 2022 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Delaby, M., Viollier, P.H. (2022). Temporal Control of Promoter Activity During the Caulobacter Cell Cycle. In: Biondi, E. (eds) Cell Cycle Regulation and Development in Alphaproteobacteria. Springer, Cham. https://doi.org/10.1007/978-3-030-90621-4_2

Download citation

Publish with us

Policies and ethics

Search

Navigation