A developmental gene product of Bacillus subtilis homologous to the sigma factor of Escherichia coli

Stragier, Patrick; Bouvier, Jean; Bonamy, Celine; Szulmajster, Jekisiel

doi:10.1038/312376a0

Cited by 96 publications

(90 citation statements)

References 24 publications

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“…In their recent article, Errington et al [2] identify in the previously published sequence of the B. subtilis spoIIAC gene [3] a region exhibiting homology with known sigma factors. This region corresponds to the internal domain conserved in bacterial sigma factors [l] which was also the first one to be noticed in the SpoIIG sequence [4]. However, no homology can be found in the carboxy-terminal region of the spoIIAC product with the postulated DNAbinding domain of the other sigma factors, a serious discrepancy with our model.…”

contrasting

confidence: 54%

Comment on ‘Duplicated sporulation genes in bacteria’ by J. Errington, P. Fort and J. Mandelstam (FEBS Letters 188 (1985) 184‐188)

Stragier

1986

FEBS Letters

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We recently presented a model for the structural organization of bacterial sigma factors based on a thorough comparison of available sequences [ 11. The major sigma factor of Escherichia coli, a", its Bacillus subtilis vegetative counterpart, t3, the E. coli heat shock regulatory protein encoded by the htpR gene and the product of the B. subtilis sporulation-essential spoIIG gene, share common characteristics: a highly conserved internal domain proposed to interact with core RNA polymerase and a carboxy-terminal region postulated to be involved in promoter recognition. In their recent article, Errington et al. [2] identify in the previously published sequence of the B. subtilis spoIIAC gene [3] a region exhibiting homology with known sigma factors. This region corresponds to the internal domain conserved in bacterial sigma factors [l] which was also the first one to be noticed in the SpoIIG sequence [4]. However, no homology can be found in the carboxy-terminal region of the spoIIAC product with the postulated DNAbinding domain of the other sigma factors, a serious discrepancy with our model. Therefore we undertook a careful examination of the published spoIIAC sequence [3]. This study revealed that shifting the reading frame in the distal part of the spoIIAC sequence by addition of one extra nucleotide at two different locations extended the spoIIAC coding sequence by 60 amino acids and restored the missing homologous domain. In fact the homology created with the carboxy-terminal part of the spoIIG product was so striking that it could barely be the result of chance. These proposed alterations of the original spoIIAC sequence have now been experimentally confirmed (see Note Added in Proof in [2]). The corrected SpoIIAC sequence is shown in fig.1, aligned with the 4 previously studied sigma factors.Addition of a new sequence introduces minor modifications to our previous alignment [l] as it allows a better estimation of the homologous domains: a highly conserved M-amino-acid internal region (called A) flanked by a more variable 33-amino-acid domain (called B) and a 59-aminoacid carboxy-terminal region (called C) containing the characteristic ~-helix-&turn-~-helix structure of DNA-binding proteins. The alignment of the less conserved regions found between domains A-B and C has also been determined. It contains a second, albeit less typical, DNA-binding structure that is also present in the SpoIIAC sequence.The corrected SpoIIAC sequence corroborates perfectly the hypothesis presented in the paper by Errington et al. [2]: the new version is much closer to the SpoIIG sequence and makes it very likely that the genes encoding these two proteins have arisen by duplication of an ancestral gene, itself evolutionarily related to the rpoD gene, encoding the major vegetative sigma factor, a43. On the other hand, the SpoIIAC sequence fits with the general scheme proposed in our original article [ 11, thus strengthening our hypothesis. However, we

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confidence: 54%

Comment on ‘Duplicated sporulation genes in bacteria’ by J. Errington, P. Fort and J. Mandelstam (FEBS Letters 188 (1985) 184‐188)

Stragier

1986

FEBS Letters

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“…The anti-E antiserum also detected a slightly larger protein, called P31, that was synthesized earlier than and thought to be a precursor of E (292). A combination of genetic and protein analysis revealed that E and P31 (now called pro-E ) were the products of the spoIIG locus (279,292). Pulse-chase and microsequencing experiments revealed that pro-E was processed into E by proteolytic removal of 27 residues from its N terminus (159,278).…”

Section: Activation Of Ementioning

confidence: 99%

Compartmentalization of Gene Expression duringBacillus subtilisSpore Formation

Hilbert

Piggot

2004

Microbiol Mol Biol Rev

320

432

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Gene expression in members of the family Bacillaceae becomes compartmentalized after the distinctive, asymmetrically located sporulation division. It involves complete compartmentalization of the activities of sporulation-specific sigma factors, σF in the prespore and then σE in the mother cell, and then later, following engulfment, σG in the prespore and then σK in the mother cell. The coupling of the activation of σF to septation and σG to engulfment is clear; the mechanisms are not. The σ factors provide the bare framework of compartment-specific gene expression. Within each σ regulon are several temporal classes of genes, and for key regulators, timing is critical. There are also complex intercompartmental regulatory signals. The determinants for σF regulation are assembled before septation, but activation follows septation. Reversal of the anti-σF activity of SpoIIAB is critical. Only the origin-proximal 30% of a chromosome is present in the prespore when first formed; it takes ≈15 min for the rest to be transferred. This transient genetic asymmetry is important for prespore-specific σF activation. Activation of σE requires σF activity and occurs by cleavage of a prosequence. It must occur rapidly to prevent the formation of a second septum. σG is formed only in the prespore. SpoIIAB can block σG activity, but SpoIIAB control does not explain why σG is activated only after engulfment. There is mother cell-specific excision of an insertion element in sigK and σE-directed transcription of sigK, which encodes pro-σK. Activation requires removal of the prosequence following a σG-directed signal from the prespore

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“…Nevertheless, there is growing support for the proposal (14-16, 41) that the mother cell-specific counterpart of (rF is cr-, the product of spoIIGB, the second cistron of the spoIIG operon (75,82). The or-protein is synthesized initially as an inactive precursor, pro-a', which is believed to be processed proteolytically by SpoIIGA to yield the active form of the protein (6,30,37,74).…”

mentioning

confidence: 99%

Evidence that the spoIIM gene of Bacillus subtilis is transcribed by RNA polymerase associated with sigma E

Smith

Youngman

1993

J Bacteriol

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We have investigated the temporal and spatial regulation ofspoHIM, a gene ofBacillus subtilis whose product is required for complete septum migration and engulfment of the forespore compartment during sporulation. The spoHIM promoter was found to become active about 2 h after the initiation of sporulation. The effects of mutations on the expression of a spoIIM-lacZ fusion were most consistent with its utilization by &-Fassociated RNA polymerase (Eci). A unique 5' end of the in vivo spoHIM transcript was detected by primer extension analysis and was determined to initiate at the appropriate distance from a sequence conforming very closely to the consensus for genes transcribed by E&F. A partially purified preparation of E&X produced a transcript in vitro that initiated at the same nucleotide as the primer extension product generated from in vivo RNA. Ectopic induction of &E synthesis during growth resulted in the immediate and strong expression of a spoIIM-lacZ fusion, but an identical fusion was completely unresponsive to induced synthesis of either oF or rG under similar conditions. The results of plasmid integration-excision experiments in which the spolIM gene was reversibly disrupted by a temperature-sensitive integrational vector suggested that spolIM expression is required in the forespore compartment, but direct examination of subcellular fractions enriched for mother cell or forespore material indicated that spolIM expression cannot be confined to the forespore. We conclude that spoHIM is a member of the &E regulon and that it may be transcribed exclusively by Ecr-. We discuss the implications of this conclusion for models in which activation of o1r in the mother cell is proposed to be a part of the mechanism responsible for initiating separate programs of gene activity in the two sporangium compartments.Endospore formation in Bacillus subtilis involves a series of temporally and spatially ordered changes in cell morphology and gene expression (42,54). At a critical stage in this process, an asymmetric septation event creates two cell compartments, the mother cell and the forespore, each containing a transcriptionally active chromosome. At some point very soon after asymmetric septation, the mother cell and the forespore compartments begin to execute quite distinct programs of gene expression. The mechanisms responsible for establishing these compartment-specific programs are not fully understood, but they apparently involve, in part, the compartment-specific activation of RNA polymerase sigma factors (16,40,41,76). This is most obvious at the later stages of sporulation, in which a polymerase species associated with g is active exclusively in the mother cell compartment (11,36,43) and a species associated with cyG is active exclusively in the forespore (31, 78). At earlier stages, the situation is less certain and the basis for compartmentspecific gene activity is more speculative. Soon after asymmetric septation, a polymerase species associated with &rF becomes active in the forespore (45, 67). The o-F...

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A developmental gene product of Bacillus subtilis homologous to the sigma factor of Escherichia coli

Cited by 96 publications

References 24 publications

Comment on ‘Duplicated sporulation genes in bacteria’ by J. Errington, P. Fort and J. Mandelstam (FEBS Letters 188 (1985) 184‐188)

Comment on ‘Duplicated sporulation genes in bacteria’ by J. Errington, P. Fort and J. Mandelstam (FEBS Letters 188 (1985) 184‐188)

Compartmentalization of Gene Expression duringBacillus subtilisSpore Formation

Evidence that the spoIIM gene of Bacillus subtilis is transcribed by RNA polymerase associated with sigma E

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