Activation of Cell-Specific Transcription by a Serine Phosphatase at the Site of Asymmetric Division

Duncan, Leonard; Alper, Scott; Arigoni, Fabrizio; Losick, Richard; Stragier, Patrick

doi:10.1126/science.270.5236.641

Cited by 230 publications

(286 citation statements)

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“…The functions of the microbial PPMs that have been characterized include regulation of spore formation, stress response, cell density during stationary phase, carbon and nitrogen assimilation, vegetative growth, development of fruiting bodies and cell segregation (Beuf et al, 1994;Duncan et al, 1995;Gaidenko et al, 2002;Irmler & Forchhammer, 2001;Rajagopal et al, 2003;Shi et al, 1999;Treuner-Lange et al, 2001;Yang et al, 1996). It is notable that most bacterial species containing relatively large numbers of PPMencoding genes, such as Anabaena sp.…”

Section: Discussionmentioning

confidence: 99%

Evolution of the PPM-family protein phosphatases in Streptomyces: duplication of catalytic domain and lateral recruitment of additional sensory domains

Zhang

Shi

2004

Microbiology

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Originally identified from eukaryotes, the Mg 2+ -or Mn 2+ -dependent protein phosphatases (PPMs) are a diverse group of enzymes whose members include eukaryotic PP2C and some prokaryotic serine/threonine phosphatases. In a previous study, unexpectedly large numbers of PPMs were identified in two Streptomyces genomes. In this work, a phylogenetic analysis was performed with all the PPMs available from a wide variety of microbial sources to determine the evolutionary origin of the Streptomyces PPM proteins. Consistent with earlier hypotheses, the results suggested that the microbial PPMs were relatively recent additions from eukaryotic sources. Results also indicated that the Streptomyces PPMs were divided into two major subfamilies at an early stage of their emergence in Streptomyces genomes. The first subfamily, which contains only six Streptomyces PPMs, possesses a catalytic domain whose sequence and architecture are similar to that of eukaryotic PPMs; the second subfamily contains 89 Streptomyces PPMs that lack the 5a and 5b catalytic domain motifs, similar to the PPMs SpoIIE and RsbU of Bacillus subtilis. Significant gene duplication was observed for the PPMs in the second subfamily. In addition, more than half (54 %) of the Streptomyces PPMs from the second subfamily were found to have at least one additional sensory domain, most commonly the PAS or the GAF domain. Phylogenetic analysis showed that these domains tended to be clustered according to the putative physiological functions rather than taxonomic relationship, implying that they might have arisen as a result of domain recruitment in a late evolutionary stage. This study provides an insight into how Streptomyces spp. may have expanded their PPM-based signal transduction networks to enable them to respond to a greater range of environmental changes.

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Section: Discussionmentioning

confidence: 99%

Evolution of the PPM-family protein phosphatases in Streptomyces: duplication of catalytic domain and lateral recruitment of additional sensory domains

Zhang

Shi

2004

Microbiology

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“…One possibility is that SpoIIE is displayed on both faces of the polar septum but because the forespore is much smaller than the mother cell, the ratio of phosphatase (SpoIIE) to kinase (SpoIIAB) would be substantially higher in the forespore than in the mother cell ( Fig. 1B; Duncan et al 1995). Other possibilities are that SpoIIE is present on both faces of the septum but only active on the forespore face (Duncan et al 1995;Arigoni et al 1999), that SpoIIE is sequestered entirely to the forespore (Feucht et al 1996;Fig.…”

mentioning

confidence: 99%

“…1B; Duncan et al 1995). Other possibilities are that SpoIIE is present on both faces of the septum but only active on the forespore face (Duncan et al 1995;Arigoni et al 1999), that SpoIIE is sequestered entirely to the forespore (Feucht et al 1996;Fig. 1B), or that the compartmentalization of F activity is the product of some combination of the above mechanisms.…”

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confidence: 99%

“…SpoIIAA is an anti-anti-factor that induces the release of F from the SpoIIAB-F complex (Min et al 1993;Alper et al 1994;Diederich et al 1994;Duncan et al 1996;Garsin et al 1998). Finally, SpoIIE is a phosphatase responsible for converting the inactive, phosphorylated form of SpoIIAA (SpoIIAA-P) to the active, dephosphorylated form (Duncan et al 1995;Arigoni et al 1996;Feucht et al 1996). Therefore, SpoIIE indirectly activates F through the dephosphorylation of SpoIIAA-P.…”

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confidence: 99%

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Septation, dephosphorylation, and the activation of sigma F during sporulation in Bacillus subtilis

King

Dreesen²,

Stragier³

et al. 1999

Genes & Development

124

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Cell-specific activation of transcription factor F during sporulation in Bacillus subtilis requires the formation of the polar septum and the activity of a serine phosphatase (SpoIIE) located in the septum. The SpoIIE phosphatase indirectly activates F by dephosphorylating a protein (SpoIIAA-P) in the pathway that controls the activity of the transcription factor. By use of a SpoIIE-GFP fusion protein in time-course and time-lapse experiments and by direct visualization of septa in living cells, we show that SpoIIE is present in the predivisional sporangium, where it often localizes near both cell poles in structures known as E-rings. We also present evidence consistent with the view that SpoIIE is present in both progeny cells after polar division. These findings are incompatible with a model for the control of F activity in which the phosphatase is simply sequestered to one cell. Instead, we conclude that the function of SpoIIE is subject to regulation, and we present evidence that this occurs in two stages. The first stage, which involves the phosphatase function of SpoIIE, depends on the cell division protein FtsZ and could correspond to the FtsZ-dependent assembly of SpoIIE into E-rings. The second stage occurs after the dephosphorylation of SpoIIAA-P and is dependent on the later-acting, cell-division protein DivIC. Evidence based on the use of modified and mutant forms of the phosphatase protein indicates that SpoIIE blocks the capacity of unphosphorylated SpoIIAA to activate F until formation of the polar septum is completed.

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“…The transcription factor F is activated in a cellspecific manner that limits its activity to the forespore compartment of the sporangium (3). The activity of F is governed by a pathway involving the proteins SpoIIAB, SpoIIAA, and SpoIIE (3)(4)(5)(6)(7)(8)(9)(10). SpoIIAB (henceforth abbreviated AB) is an anti-F factor that binds to F , trapping it in an inactive complex.…”

mentioning

confidence: 99%

Evidence in Support of a Docking Model for the Release of the Transcription Factor σF from the Antisigma Factor SpoIIAB in Bacillus subtilis

Carniol

Losick

2003

Journal of Biological Chemistry

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Cell-specific activation of the transcription factor F during the process of sporulation in Bacillus subtilis is governed by an antisigma factor SpoIIAB and an antiantisigma factor SpoIIAA. SpoIIAB, which exists as a dimer, binds to F in a complex of stoichiometry F ⅐SpoIIAB 2 . Escape from the complex is mediated by SpoIIAA, which reacts with the complex to cause the release of free F . Previous evidence indicated that Arg-20 in SpoIIAB is a contact site for both F and SpoIIAA and that contact with F is mediated by Arg-20 on only one of the two subunits in the F ⅐SpoIIAB 2 complex. Here we report the construction of heterodimers of SpoIIAB in which one subunit is wild type and the other subunit is a mutant for Arg-20. We show that the dissociation constant for the binding of F to the heterodimer was similar to that for the wild type, a finding consistent with the idea that F contacts Arg-20 on only one of the two subunits. Although SpoIIAA was highly effective in causing the release of F from the wild type homodimer, the anti-antisigma factor had little effect on the release of F from the heterodimer. This finding is consistent with a model in which SpoIIAA docks on the F ⅐SpoIIAB 2 complex, making contact with the subunit in which Arg-20 is not in contact with F . SpoIIAB is both an anti-F factor and a protein kinase that phosphorylates and thereby inactivates SpoIIAA. We show that SpoIIAA effectively displaces F from a complex of F with a mutant (SpoIIAB R105A ) that is impaired in the kinase function of SpoIIAB. This result shows that SpoIIAAmediated displacement of F from SpoIIAB does not require concomitant phosphorylation of SpoIIAA.

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Activation of Cell-Specific Transcription by a Serine Phosphatase at the Site of Asymmetric Division

Cited by 230 publications

References 22 publications

Evolution of the PPM-family protein phosphatases in Streptomyces: duplication of catalytic domain and lateral recruitment of additional sensory domains

Evolution of the PPM-family protein phosphatases in Streptomyces: duplication of catalytic domain and lateral recruitment of additional sensory domains

Septation, dephosphorylation, and the activation of sigma F during sporulation in Bacillus subtilis

Evidence in Support of a Docking Model for the Release of the Transcription Factor σF from the Antisigma Factor SpoIIAB in Bacillus subtilis

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