<i>spoIIQ</i>, a forespore‐expressed gene required for engulfment in <i>Bacillus subtilis</i>

Ja, Londoño-Vallejo; Fréhel, Claude; Stragier, Patrick

doi:10.1046/j.1365-2958.1997.3181680.x

Cited by 129 publications

(151 citation statements)

References 37 publications

(59 reference statements)

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“…Class 2 included 19 genes whose main period of expression was centred 270 min after the onset of sporulation. The spoIIR, spoIIQ, lonB and rsfA genes were assigned to class 1, in agreement with experimental data Londono-Vallejo & Stragier, 1995;Londono-Vallejo et al, 1997;Serrano et al, 2001;Wu & Errington, 2000), whereas dacF, gpr, spIVB, sspN and tlp (Cabrera-Hernandez et al, 1999;Schuch & Piggot, 1994;Sussman & Setlow, 1991) were assigned to class 2 (Supplementary Table S1). s F and s G have overlapping promoter specificities, and therefore some s F -dependent genes are only recognized by s F , whereas other genes are recognized by both s F and s G (Amaya et al, 2001;Haldenwang, 1995;Helmann & Moran, 2002).…”

Section: Differentiation Of the Compartment-specific Sporulation Regusupporting

confidence: 67%

“…For example, some s F -dependent genes are expressed soon after asymmetric division of the sporangial cell and the concomitant prespore-specific activation of s F Londono-Vallejo & Stragier, 1995;Londono-Vallejo et al, 1997;Wu & Errington, 2003), while expression of the dacF or spoIIIG genes, for example, appears delayed relative to the first wave of s F -directed genes Partridge & Errington, 1993;Schuch & Piggot, 1994;see below). Therefore, we wanted to test whether or not, based on our data, we could discriminate between groups of genes with a common expression profile within each of the main regulons.…”

Section: Differentiation Of the Compartment-specific Sporulation Regumentioning

confidence: 99%

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Genome-wide analysis of temporally regulated and compartment-specific gene expression in sporulating cells of Bacillus subtilis

et al. 2005

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Temporal and compartment-specific control of gene expression during sporulation in Bacillus subtilis is governed by a cascade of four RNA polymerase subunits. s F in the prespore and s E in the mother cell control early stages of development, and are replaced at later stages by s G and s K , respectively. Ultimately, a comprehensive description of the molecular mechanisms underlying spore morphogenesis requires the knowledge of all the intervening genes and their assignment to specific regulons. Here, in an extension of earlier work, DNA macroarrays have been used, and members of the four compartment-specific sporulation regulons have been identified. Genes were identified and grouped based on: i) their temporal expression profile and ii) the use of mutants for each of the four sigma factors and a bofA allele, which allows s K activation in the absence of s G . As a further test, artificial production of active alleles of the sigma factors in non-sporulating cells was employed. A total of 439 genes were found, including previously characterized genes whose transcription is induced during sporulation: 55 in the s F regulon, 154 s E -governed genes, 113 s G -dependent genes, and 132 genes under s K control. The results strengthen the view that the activities of s F , s E , s G and s K are largely compartmentalized, both temporally as well as spatially, and that the major vegetative sigma factor (s A ) is active throughout sporulation. The results provide a dynamic picture of the changes in the overall pattern of gene expression in the two compartments of the sporulating cell, and offer insight into the roles of the prespore and the mother cell at different times of spore morphogenesis.

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Section: Differentiation Of the Compartment-specific Sporulation Regusupporting

confidence: 67%

Section: Differentiation Of the Compartment-specific Sporulation Regumentioning

confidence: 99%

Genome-wide analysis of temporally regulated and compartment-specific gene expression in sporulating cells of Bacillus subtilis

et al. 2005

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“…Both strains bearing the wild-type or spoIIIGE156K allele under the control of the spoIIQ promoter presented a high background of G activity starting at the onset of sporulation. The reason for this behavior is not known, but it could be the result of high levels of expression of spoIIIG or spoIIIGE156K from the strong spoIIQ promoter (24). In any event, we note that expression of spoIIIGE156K does not result in a higher background relative to expression of the wild-type spoIIIG gene (Fig.…”

Section: Vol 186 2004 Regulation Of G 4005mentioning

confidence: 85%

“…Transcription of the spoIIIG gene by G is delayed by an unknown mechanism towards the end of the engulfment process relative to the transcription of the first class of F -dependent genes, which includes the spoIIQ gene (24). We fused the coding region of spoIIIGE156K to the early F -dependent spoIIQ promoter, reasoning that the fusion allele would bypass both the mechanism that delays transcription of spoIIIG and a possible negative effect of SpoIIAB prior to engulfment.…”

Section: Vol 186 2004 Regulation Of G 4005mentioning

confidence: 99%

Role of the Anti-Sigma Factor SpoIIAB in Regulation of σ ^G during Bacillus subtilis Sporulation

et al. 2004

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RNA polymerase sigma factor F initiates the prespore-specific program of gene expression during Bacillus subtilis sporulation. F governs transcription of spoIIIG, encoding the late prespore-specific regulator G . However, transcription of spoIIIG is delayed relative to other genes under the control of F , and after synthesis, G is initially kept in an inactive form. Activation of G requires the complete engulfment of the prespore by the mother cell and expression of the spoIIIA and spoIIIJ loci. We screened for random mutations in spoIIIG that bypassed the requirement for spoIIIA for the activation of G . We found a mutation (spoIIIGE156K) that resulted in an amino acid substitution at position 156, which is adjacent to the position of a mutation (E155K) previously shown to prevent interaction of SpoIIAB with G . Comparative modelling techniques and in vivo studies suggested that the spoIIIGE156K mutation interferes with the interaction of SpoIIAB with G . The GE156K isoform restored G -directed gene expression to spoIIIA mutant cells. However, expression of sspElacZ in the spoIIIA spoIIIGE156K double mutant was delayed relative to completion of the engulfment process and was not confined to the prespore. Rather, ␤-galactosidase accumulated throughout the entire cell at late times in development. This suggests that the activity of GE156K is still regulated in the prespore of a spoIIIA mutant, but not by SpoIIAB. In agreement with this suggestion, we also found that expression of spoIIIGE156K from the promoter for the early prespore-specific gene spoIIQ still resulted in sspE-lacZ induction at the normal time during sporulation, coincidently with completion of the engulfment process. In contrast, transcription of spoIIIGE156K, but not of the wild-type spoIIIG gene, from the mother cell-specific spoIID promoter permitted the rapid induction of sspE-lacZ expression. Together, the results suggest that SpoIIAB is either redundant or has no role in the regulation of G in the prespore.Gene expression in the prespore and mother cell chambers of sporulating Bacillus subtilis is controlled by RNA polymerase sigma subunits whose activity is restricted to a specific cell type (22,31,37,46). The activation of the sporulation-specific sigma factors is tightly coupled to the completion of key morphological intermediates in the process and also relies on signaling pathways that operate between the two cell types and that keep the prespore and mother cell lines of gene expression in close register (22,31,37,46). Soon after the asymmetric division of the sporangial cell, an event that creates the prespore and the much larger mother cell, the first compartmentspecific sigma factor F becomes active in the prespore (22,31,37,46

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“…First, SpoIIQ is essential for the engulfment-dependent activation of G (20,21), although its precise role in this process remains unclear. Second, SpoIIQ participates in engulfment, providing a secondary mechanism that is necessary for membrane migration when the activity of the primary engulfment machinery is compromised (22).…”

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confidence: 99%

Impact of Membrane Fusion and Proteolysis on SpoIIQ Dynamics and Interaction with SpoIIIAH

Chiba¹,

Coleman

Pogliano

2007

Journal of Biological Chemistry

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The onset of engulfment-dependent gene expression during Bacillus subtilis sporulation requires the forespore membrane protein SpoIIQ, which recruits mother cell proteins involved in late gene expression to the outer forespore membrane. Engulfment activates the late forespore transcription factor G , which produces high levels of the secreted SpoIVB protease that is required for activation of the late mother cell transcription factor K . Engulfment also triggers the proteolytic cleavage of SpoIIQ, an event that depends on the SpoIVB protease but not on G activity. To determine if SpoIVB directly cleaves SpoIIQ and to determine if this event participates in the onset of late gene expression, we purified SpoIVB, SpoIIQ, and SpoIVFA (another SpoIVB substrate). SpoIVB directly cleaved SpoIIQ at the same site in vitro and in vivo and cleaved SpoIVFA in at least three different locations. SpoIIQ cleavage depends on membrane fusion, but not on G activity, suggesting that the ability of SpoIVB to cleave substrates is regulated by membrane fusion. We isolated SpoIVB-resistant SpoIIQ proteins by random mutagenesis of codons at the cleavage site and demonstrated that SpoIIQ processing is dispensable for spore formation and for activation of late forespore and mother cell gene expression. Fluorescence recovery after photobleaching analysis demonstrated that membrane fusion releases SpoIIQ from an immobile complex, an event that could allow SpoIVB to cleave SpoIIQ. We propose that this membrane fusion-dependent reorganization in the complex, rather than SpoIIQ proteolysis itself, is necessary for the onset of late transcription.Endospore formation in Bacillus subtilis and its relatives depends on engulfment, a phagocytosis-like process that mediates a dramatic rearrangement of the sporangium from two adjacent daughter cells, to an endospore in which the forespore lies within the cytoplasm of the larger mother cell (see Fig. 1; reviewed by Refs. 1 and 2). Engulfment is critical for sporulation, because it allows spore assembly to occur in a protected environment. It also serves as a morphological checkpoint for activation of the late forespore and mother cell transcription factors G and K , respectively (reviewed by Refs. 1-4). The endospore-forming bacteria must therefore have some mechanism to sense the completion of engulfment and to couple this morphological event to the onset of late gene expression.The forespore transcription factor G is the first to become active after engulfment, but it remains unclear how G is held inactive during engulfment or activated after engulfment. More is known about the regulation of the second late transcription factor, K , which becomes active in the mother cell (summarized in Fig. 1B and reviewed by Refs. 1-4). The K factor is initially synthesized as an inactive pro-protein containing a hydrophobic leader sequence, which functions as a covalently attached anti-sigma factor (5). This leader sequence is removed by the intramembrane protease SpoIVFB, which cleaves pro-K within the membrane ...

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spoIIQ, a forespore‐expressed gene required for engulfment in Bacillus subtilis

Cited by 129 publications

References 37 publications

Genome-wide analysis of temporally regulated and compartment-specific gene expression in sporulating cells of Bacillus subtilis

Genome-wide analysis of temporally regulated and compartment-specific gene expression in sporulating cells of Bacillus subtilis

Role of the Anti-Sigma Factor SpoIIAB in Regulation of σ ^G during Bacillus subtilis Sporulation

Impact of Membrane Fusion and Proteolysis on SpoIIQ Dynamics and Interaction with SpoIIIAH

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spoIIQ, a forespore‐expressed gene required for engulfment in Bacillus subtilis

Cited by 129 publications

References 37 publications

Genome-wide analysis of temporally regulated and compartment-specific gene expression in sporulating cells of Bacillus subtilis

Genome-wide analysis of temporally regulated and compartment-specific gene expression in sporulating cells of Bacillus subtilis

Role of the Anti-Sigma Factor SpoIIAB in Regulation of σ G during Bacillus subtilis Sporulation

Impact of Membrane Fusion and Proteolysis on SpoIIQ Dynamics and Interaction with SpoIIIAH

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Role of the Anti-Sigma Factor SpoIIAB in Regulation of σ ^G during Bacillus subtilis Sporulation