Turning off flagellum rotation requires the pleiotropic gene pleD: pleA, pleC, and pleD define two morphogenic pathways in Caulobacter crescentus

Sommer, Jürg M.; Newton, Austin

doi:10.1128/jb.171.1.392-401.1989

Cited by 88 publications

(110 citation statements)

References 26 publications

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“…When PflI is overproduced, it localizes ectopically to the stalked pole, and this correlates with a considerable increase in ectopic flagellar synthesis at that site. C. crescentus populations carrying tipN, podJ, pleC, or pleD mutations also have a proportion of cells with a flagellum at the stalked pole or at the stalk itself, but these mutations also alter many aspects of cell polarity and polar morphogenesis (1,20,21,27,47,49). On the other hand, we found no evidence of defects in cell polarization or polar morphogenesis in the ⌬pflI or pflI-overexpressing strains, apart from a high frequency of flagellum misplacement.…”

Section: Discussioncontrasting

confidence: 53%

“…Our data argue that the presence and proper localization of PflI are important for positioning the flagellum at the correct pole. It is known that mutations in genes involved in multiple aspects of cell polarity or polar morphogenesis can result in flagellar placement defects (1,20,21,27,47,49). Unlike some of these genes with pleiotropic functions, pflI does not affect cell division or stalk biogenesis, as judged by the normal cell and stalk morphology of ⌬pflI and pflI-overexpressing cells (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…The sessile stalked cells then begin expressing flagellar genes in a stepwise, hierarchical manner, and a new flagellum is formed at the pole opposite the stalk (28,35,52). Division yields a flagellated swarmer progeny for dispersal and a sessile stalked progeny for local colonization.Defects in flagellar placement have been observed in several C. crescentus mutants, but the mutations lie in genes that have pleiotropic functions in cell polarization and polar morphogenesis (1,20,21,27,47,49). In this study, we identify CC_2060, renamed pflI (the polar-flagellum-linked gene), as one of the genes specifically associated with flagellar positioning.…”

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confidence: 95%

“…Defects in flagellar placement have been observed in several C. crescentus mutants, but the mutations lie in genes that have pleiotropic functions in cell polarization and polar morphogenesis (1,20,21,27,47,49). In this study, we identify CC_2060, renamed pflI (the polar-flagellum-linked gene), as one of the genes specifically associated with flagellar positioning.…”

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confidence: 95%

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PflI, a Protein Involved in Flagellar Positioning in Caulobacter crescentus

Obuchowski

Jacobs‐Wagner

2008

J Bacteriol

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The bacterial flagellum is important for motility and adaptation to environmental niches. The sequence of events required for the synthesis of the flagellar apparatus has been extensively studied, yet the events that dictate where the flagellum is placed at the onset of flagellar biosynthesis remain largely unknown. We addressed this question for alphaproteobacteria by using the polarly flagellated alphaproteobacterium Caulobacter crescentus as an experimental model system. To identify candidates for a role in flagellar placement, we searched all available alphaproteobacterial genomes for genes of unknown function that cluster with early flagellar genes and that are present in polarly flagellated alphaproteobacteria while being absent in alphaproteobacteria with other flagellation patterns. From this in silico screen, we identified pflI. Loss of PflI function in C. crescentus results in an abnormally high frequency of cells with a randomly placed flagellum, while other aspects of cell polarization remain normal. In a wild-type background, a fusion of green fluorescent protein (GFP) and PflI localizes to the pole where the flagellum develops. This polar localization is independent of the flagellar protein FliF, whose oligomerization into the MS ring is thought to define the site of flagellar synthesis, suggesting that PflI acts before or independently of this event. Overproduction of PflI-GFP often leads to ectopic localization at the wrong, stalked pole. This is accompanied by a high frequency of flagellum formation at this ectopic site, suggesting that the location of PflI is a sufficient marker for a site for flagellar assembly.Flagellar arrangement has long been used as a defining characteristic in bacterial taxonomy. Bacteria can have flagella emerging from a specific site, such as the cell pole, or from seemingly random positions along the cell body (as in peritrichously flagellated bacteria). Differences in flagellar distribution can be important for how various species adapt to specific environments. While the biosynthesis of the flagellum and the temporal regulation of its assembly have been extensively studied (5, 32), we know little about what controls the cellular position of flagellar assembly. The distribution of flagella in peritrichous bacteria may be random and stochastically driven, but spatial mechanisms must exist in polarly flagellated bacteria to ensure that flagellar assembly takes place at the right location.It has been shown that in several polarly flagellated species of gammaproteobacteria, the flhF gene product is necessary for restricting the flagellum to a polar position (38, 41). flhF encodes a GTP-binding protein homologous to components of the signal recognition particle (SRP) pathway; in its absence, Pseudomonas putida and Pseudomonas aeruginosa have reduced motility and randomly placed flagella on the cell surface (25,38,41). Surprisingly, flhF homologs are also found in species with multiple, randomly placed flagella, indicating that FlhF is not a defining component of polarly f...

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Section: Discussioncontrasting

confidence: 53%

Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 95%

mentioning

confidence: 95%

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PflI, a Protein Involved in Flagellar Positioning in Caulobacter crescentus

Obuchowski

Jacobs‐Wagner

2008

J Bacteriol

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“…The ⌬pleC mutant is viable but lacks a stalk and pili and has bipolar, nonfunctional flagella (30,31). ⌬pleC cells contain elevated levels of DivKϳP (28) and cannot release localized DivK from the swarmer cell pole (27).…”

Section: Polar Localization Of Divk Is Not Required For Ctra Recruitmmentioning

confidence: 99%

Recruitment of a cytoplasmic response regulator to the cell pole is linked to its cell cycle-regulated proteolysis

Ryan

Huntwork

Shapiro

2004

Proc. Natl. Acad. Sci. U.S.A.

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The response regulator CtrA, which silences the Caulobacter origin of replication and controls multiple cell cycle events, is specifically proteolyzed in cells preparing to initiate DNA replication. At the swarmer-to-stalked cell transition and in the stalked compartment of the predivisional cell, CtrA is localized to the cell pole just before its degradation. Analysis of the requirements for CtrA polar localization and CtrA proteolysis revealed that both processes require a motif within amino acids 1-56 of the CtrA receiver domain, and neither process requires CtrA phosphorylation. These results strongly suggest that CtrA polar localization is coupled to its cell cycle-regulated proteolysis. The polarly localized DivK response regulator promotes CtrA localization and proteolysis, but it does not directly recruit CtrA to the cell pole. Mutations in the divJ and pleC histidine kinases perturb the characteristic asymmetry of CtrA localization and proteolysis in the predivisional cell. We propose that polar recruitment of CtrA evolved to ensure that CtrA is degraded only in the stalked half of the predivisional cell, perhaps by localizing a proteolytic adaptor protein to the stalked pole. This is an example of controlled proteolysis of a cytoplasmic protein that is associated with its active recruitment to a specific subcellular address.Caulobacter ͉ CtrA ͉ ClpXP I n Caulobacter crescentus, DNA replication occurs once per cell division, and the phases of the cell cycle are linked to observable morphological changes (reviewed in refs. 1 and 2). Motile swarmer cells (Fig. 1) in the G 1 phase of the cell cycle develop into stalked cells ( Fig. 1) and initiate chromosome replication. During the swarmer-to-stalked cell (SW-ST) (or G 1 -S) transition, each cell sheds its polar flagellum and builds a stalk at the same site. As DNA replication proceeds, stalked cells elongate and become predivisional cells with distinct poles. A new flagellum is built at the pole opposite the stalk, so that each cell division produces a motile swarmer cell and a stalked cell. Before cell separation, a diffusion barrier is established between the swarmer and stalked compartments of the predivisional cell so that they contain distinct sets of signal transduction proteins that yield progeny with different replicative fates (3): the stalked progeny can initiate DNA replication immediately, whereas the swarmer cell must first differentiate into a new stalked cell.A key signal transduction protein that regulates Caulobacter cell cycle progression is the essential response regulator CtrA (4). CtrA directly induces or represses the transcription of Ϸ55 operons in the Caulobacter genome, including genes needed for flagellum and pili biosynthesis, DNA methylation, cell division, chemotaxis, and metabolism (5, 6). However, CtrA also represses chromosome replication by binding to five sites within the replication origin (7). Because CtrA has multiple functions, its activity is tightly controlled by three mechanisms: cell cycleregulated transcription (...

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