Chromosomal organization governs the timing of cell type-specific gene expression required for spore formation in Bacillus subtilis.
During the early stages of spore formation in Bacillus subtilis, asymmetric division precedes chromosome segregation, such that the forespore transiently contains only about one-third of the genetic material surrounding the origin of replication. Shortly after septum formation, the transcription factor sigmaF initiates forespore-specific gene expression that is essential for the proteolytic activation of pro-sigmaE in the neighbouring mother cell. Moving the sigmaF-dependent spoIIR gene from its original origin-proximal position to an ectopic origin-distal site caused a delay in spoIIR transcription, as well as delays and reductions in the proteolytic activation of pro-sigmaE and sigmaE-directed gene expression. These defects correlated with the accumulation of disporic sporangia, thus reducing sporulation efficiency in a manner that depended upon the distance that spoIIR had been moved from the origin-proximal third of the chromosome. A significant proportion of disporic sporangia exhibited sigmaE activity in their central compartment, indicating that delays and reductions in sigmaE activation can lead to the formation of a second septum at the opposite pole. These observations support a model in which chromosomal spoIIR position temporally regulates sigmaE activation, thereby allowing for the rapid establishment of mother cell-specific gene expression that is essential for efficient spore formation. The implications of these findings for cell type-specific gene expression during the early stages of spore formation in B. subtilis are discussed.
Department of Plant and Microbial Biology, University of California, 111 Koshland Hall, Berkeley, CA 94720-3102, USA.
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Zupancic
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Tran
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Hofmeister
D001412:Bacillus subtilis / Q000502:physiology*; D001426:Bacterial Proteins / Q000235:genetics*; D002876:Chromosomes, Bacterial; D015964:Gene Expression Regulation, Bacterial; D012808:Sigma Factor / Q000235:genetics; D013171:Spores, Bacterial / Q000235:genetics; D014157:Transcription Factors / Q000235:genetics; D014158:Transcription, Genetic
D001426:Bacterial Proteins; C064971:FliA protein, Bacteria; D012808:Sigma Factor; D014157:Transcription Factors; C092468:spoIIR protein, Bacillus subtilis; C030069:spore-specific proteins, Bacillus; C063202:sporulation-specific sigma factors