Temporal and spatial control of the mother-cell regulatory gene spoIIID of Bacillus subtilis.

Kunkel, Barbara N.; Kroos, Lee; Poth, Harold; Youngman, Philip; Losick, Richard

doi:10.1101/gad.3.11.1735

Cited by 122 publications

(109 citation statements)

References 48 publications

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“…Thus, SpoIIID divides the regulon into an early phase, when some genes are expressed, and a late phase, when other genes are expressed, VOL. 68, 2004 COMPARTMENTALIZATION OF GENE EXPRESSION 253 on May 10, 2018 by guest http://mmbr.asm.org/ and some genes of the first phase are turned down or off (102,125,152,154). GerE effects a similar division of the K regulon (122,316).…”

Section: Temporal Control and Compartmentalizationmentioning

confidence: 90%

Compartmentalization of Gene Expression duringBacillus subtilisSpore Formation

Hilbert

Piggot

2004

Microbiol Mol Biol Rev

313

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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Section: Temporal Control and Compartmentalizationmentioning

confidence: 90%

Compartmentalization of Gene Expression duringBacillus subtilisSpore Formation

Hilbert

Piggot

2004

Microbiol Mol Biol Rev

313

432

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“…Mapping experiments were carried out with the nine strains of the B. subtilis mapping kit (5,6). Two-and three-factor genetic crosses were performed with strains CU4164 (zii-83::Tn917 trpC2 SP␤c2) (5), BD067 (trpC2 cotB::cat) (7), BK395 (spoIIID83) (15), and QB917 (hisA1 thr-5 trpC2) (6) and the prototrophic strain PY79 (28). Cloning experiments were carried out in Escherichia coli TG1 (23).…”

Section: Methodsmentioning

confidence: 99%

An additional GerE-controlled gene encoding an abundant spore coat protein from Bacillus subtilis

et al. 1995

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We describe the identification and characterization of a gene, herein designated cotG, encoding an abundant coat protein from the spores of Bacillus subtilis. The cotG open reading frame is 195 codons in length and is capable of encoding a polypeptide of 24 kDa that contains nine tandem copies of the 13-amino-acid long, approximately repeated sequence H/Y-K-K-S-Y-R/C-S/T-H/Y-K-K-S-R-S.cotG is located at 300؇ on the genetic map close to another coat protein gene, cotB. The cotG and cotB genes are in divergent orientation and are separated by 1.3 kb. Like the promoter for cotB, the cotG promoter is induced at a late stage of sporulation under the control of the RNA polymerase sigma factor K and the DNA-binding protein GerE. The ؊10 and ؊35 nucleotide sequences of the cotG promoter resemble those of other promoters recognized by K -containing RNA polymerase, and centered 70 bp upstream of the apparent start site is a sequence that matches the consensus binding site for GerE. Spore coat proteins from a newly constructed cotG null mutant lack not only CotG but also CotB, a finding that suggests that CotG may be a morphogenetic protein that is required for the incorporation of CotB into the coat.Spores of the gram-positive bacterium Bacillus subtilis are encased in a complex protein shell known as the coat consisting of 15 or more different proteins. So far, genes for 10 of these coat proteins have been identified. These are located at diverse positions on the chromosome and encode polypeptides of 65 (CotA), 59 (CotB), 10 (CotC), 9 (CotD), 24 (CotE), 19 (CotF), 10 (CotT), 19 (CotX), 26 (CotY), and 18 (CotZ) kDa (2,4,7,29,31). In the cases of CotF and CotT, little of the full-length gene products is found in the coat. Rather, CotF is present as two proteolytic fragments of 8 and 5 kDa, and CotT is present as a proteolytic fragment of 8 kDa (2, 4). Coat proteins are organized in two principal layers, a lamellar inner coat and an electron-dense outer coat (1), with certain proteins, such as CotD, being present in the inner coat, and other proteins, such as CotA, CotB, and CotC, being present in the outer coat (31). The coat is assembled at intermediate to late stages of sporulation when the nascent spore (known as the forespore) is present as a free protoplast, wholly engulfed within the mother cell compartment of the developing sporangium. Coat proteins are recruited to the outer surface of the membrane surrounding the forespore by the sporulation protein SpoIVA (which has not been detected in mature spores and hence is not referred to as a coat protein) (8,19,21). Morphogenetic events under the control of SpoIVA lead to the assembly of a ring of CotE protein around the forespore (8). The CotE ring is separated from the outer surface of the forespore (where SpoIVA is located) by a small gap, which is believed to be the site at which the inner coat will be assembled. Meanwhile, CotE dictates the assembly of the proteins of the outer coat, where it is itself located (8, 31). The production of coat proteins is governed by ...

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“…The distinction between classes 1 and 2 may be attributable mostly to the effects of the regulatory protein SpoIIID upon s E -dependent gene expression (Zheng & Losick, 1990). SpoIIID-independent genes are expressed early, and SpoIIID-dependent genes are expressed later, while the expression of some of the early genes is repressed or switched off Illing & Errington, 1991;Kroos et al, 1989;Kunkel et al, 1989). However, class 3 may represent an overlap between the s E and s K regulons, either because genes in this class have multiple promoters utilized by s E or s K , or because atypical s E -type promoters can also be recognized by s K (Helmann & Moran, 2002 Table S2), encodes a putative transcriptional regulator, highly similar to RsfA.…”

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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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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Temporal and spatial control of the mother-cell regulatory gene spoIIID of Bacillus subtilis.

Cited by 122 publications

References 48 publications

Compartmentalization of Gene Expression duringBacillus subtilisSpore Formation

Compartmentalization of Gene Expression duringBacillus subtilisSpore Formation

An additional GerE-controlled gene encoding an abundant spore coat protein from Bacillus subtilis

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

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