Transient gene asymmetry during sporulation and establishment of cell specificity in Bacillus subtilis

Abstract

Sporulation in Bacillus subtilis is initiated by an asymmetric division generating two cells of different size and fate. During a short interval, the smaller forespore harbors only 30% of the chromosome until the remaining part is translocated across the septum. We demonstrate that moving the gene for F , the forespore-specific transcription factor, in the trapped region of the chromosome is sufficient to produce spores in the absence of the essential activators SpoIIAA and SpoIIE. We propose that transient genetic asymmetry is the device that releases SpoIIE phosphatase activity in the forespore and establishes cell specificity.

Compartmentalization of Gene Expression duringBacillus subtilisSpore Formation

“…3). This arrangement of genes supported a modest level of sporulation even in the absence of the normally essential factors SpoIIAA and SpoIIE (84). These results clearly suggested that transient genetic asymmetry could play a role in compartmentalization of F activity.…”

“…As a consequence, the two cells are now genetically asymmetric. This asymmetry has important implications for compartmentalization of gene expression (54,84), as discussed below. The developing organism also has a major challenge in that it must ensure that the prespore compartment receives a complete chromosome The transfer of the origin-distal two-thirds of a chromosome from the mother cell into the prespore is concomitant with the activation of different transcription factors in the prespore and mother cell.…”

“…It takes about 15 min before the prespore receives a complete chromosome (148,232). It was proposed that this transient genetic asymmetry could be the key to establishing compartmentalized gene expression (84). This proposal was tested by placing the gene encoding F at the amyE locus very near the origin of replication, so that it was present in the prespore at the time of asymmetric division, and leaving spoIIAB near the terminus, so that it was initially absent from this compartment (Fig.…”

“…(v) The septum is asymmetrically located, with respect to the cell poles, during sporulation but not during vegetative growth (251) (vi) Several proteins become associated with the sporulation septum that are not associated with the vegetative division septum (10,14,72). (vii) Complete partitioning of a chromosome into the prespore occurs after septation (303,310), so that there is genetic asymmetry between the prespore and the mother cell when they are first formed (54,84,305). (viii) After the sporulation division, different programs of gene expression are initiated in the two daughter cells (231).…”

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

“…The discovery that SpoIIE localizes to the polar septum revealed a direct connection between the activation of F and the process of asymmetric division, but left unanswered the questions of how the timing and cell selectivity of F activation are determined (Frandsen et al 1999;Losick and Dworkin 1999). 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.…”