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Chapter 8 : Asymmetric Division and Cell Fate during Sporulation in

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Abstract:

At the onset of sporulation, undergoes a switch from binary fission, the mode of cytokinesis it employs during vegetative growth, to asymmetric division, in which a division septum is laid down close to one of the cell poles. This chapter outlines the genetic pathway governing the switch from binary fission to polar septation in , discusses the connection between polar division and the establishment of cell-type-specific gene expression, and finally describes pathways of intercellular communication between the mother cell and forespore chambers of the sporangium. The current model for gene function in is based on the idea that there are three potential division sites in the cell, the new site at midcell and the old sites at each pole. The polar septum is intimately involved in the activation of both transcription factors and perhaps can be thought of as an organelle for the establishment of cell fate. Finally, the authors return to the issue of how a null mutation of the gene for the DNA translocase is able to break the otherwise-strict compartmentalization of δ activity. The principal goal in the chapter is to consider sporulation in the context of the developmental problem of the establishment of cell fate.

Citation: Levin P, Losick R. 2000. Asymmetric Division and Cell Fate during Sporulation in , p 167-189. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch8
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Figures

Image of FIGURE 1
FIGURE 1

Stages of sporulation. On the left in each panel is shown an electron micrograph of the stage of sporulation, and on the right is depicted in cartoon form the disposition of the chromosomes and the time and site of action of the principal regulatory proteins that govern sporulation gene expression. (A) Vegetative cells; (B through E) sporangia at entry into sporulation (stage 0) (B), at polar division (stage II) (C), at engulfment (stage III) (D), and at cortex and coat formation (stage V to VI) (E); (F) a free spore. Notice that at stage V to VI (E) the forespore chromosome is packaged into a doughnut-like shape (Pogliano et al., 1995). (Electron micrographs reprinted from Driks, 1999, with permission of the publisher.)

Citation: Levin P, Losick R. 2000. Asymmetric Division and Cell Fate during Sporulation in , p 167-189. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch8
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Image of FIGURE 2
FIGURE 2

Asymmetric division. The arrows depict the course of events involved in asymmetric division and the contribution of sporulation transcription factors. The cartoon on the top left and the two cartoons on the right show the terminal phenotype of mutants lacking the indicated transcription factor.

Citation: Levin P, Losick R. 2000. Asymmetric Division and Cell Fate during Sporulation in , p 167-189. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch8
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Image of FIGURE 3
FIGURE 3

Translocation of a chromosome into the forespore. Depicted in the septum is a channel created by the DNA translocase protein SpoIIIE through which the forespore chromosome is translocated.

Citation: Levin P, Losick R. 2000. Asymmetric Division and Cell Fate during Sporulation in , p 167-189. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch8
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Image of FIGURE 4
FIGURE 4

Contrasting roles of MinE and DivIVA in septum site selection. (A) In , MinE (gray ring) localizes to the nascent septal site in an FtsZ-independent manner. By virtue of its localization pattern, it inhibits MinCD division inhibition at mid-cell, allowing for FtsZ ring formation (beaded ring) and binary fission. MinCD activity is thus restricted to the cell poles (black and white bands), where it prevents FtsZ ring formation and cell division. (B) In , DivIVA (gray) localizes to the cell poles, where it recruits MinD and presumably MinC (black and white bands). By recruiting MinCD to the cell poles, DivIVA leaves the medial site free for FtsZ localization (beaded ring) and cell division.

Citation: Levin P, Losick R. 2000. Asymmetric Division and Cell Fate during Sporulation in , p 167-189. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch8
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Image of FIGURE 5
FIGURE 5

Activation of σF. (A) Release of σF from the antisigma factor-kinase SpoIIAB (AB) by the action of SpoIIAA (AA). SpoIIAA is subject to a cycle of phosphorylation and dephosphorylation governed by the SpoIIE phosphatase (E) and the antisigma factor-kinase (AB). SpoIIAB can form alternative complexes with SpoIIAA when it contains ADP and with σF when it contains ATP. (B) Comparison of the state and location of these proteins before and after septation. The SpoIIE phosphatase (stippled circles) is located in rings near each end of the predivisional sporangium and in the septum in the postdivisional sporangium. SpoIIAA (AA) is in the phosphorylated state in the predivisional sporangium and in the mother cell. In the forespore it is unphosphorylated and in a complex with SpoIIAB (AB). Finally, σF is held in a complex with SpoIIAB in the predivisional sporangium and in the mother cell and is free of the antisigma factor in the forespore.

Citation: Levin P, Losick R. 2000. Asymmetric Division and Cell Fate during Sporulation in , p 167-189. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch8
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Image of FIGURE 6
FIGURE 6

An intercellular signal transduction pathway governing the appearance of σ(A) Pro-σE and the SpoIIGA-processing enzyme as associated with the cytoplasmic membrane. (B) Both SpoIIGA and pro-σE have become located at the polar septum. (B and C) The cartoons show that the signaling protein SpoIIR is produced in the forespore under the control of σand that it then triggers the action of SpoIIGA, causing the release of mature σinto the mother cell cytoplasm. The cartoon suggests that proσis sequestered on the mother cell face of the septum, thereby explaining the presence of mature σE exclusively in the mother cell.

Citation: Levin P, Losick R. 2000. Asymmetric Division and Cell Fate during Sporulation in , p 167-189. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch8
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Image of FIGURE 7
FIGURE 7

Intercompartmental pathways governing the activation of σG and σK. (A) Dependence of the appearance of σon a pathway involving σ-dependent gene expression in the mother cell, including expression of spoIIIA. The diagram also indicates that the gene for σG is transcribed under the direction of both σF and its own gene product and that σis subject to inhibition by the antisigma factor SpoIIAB. (B) Pathway governing the processing of pro-σK. σG directs the synthesis of the signal protein SpoIVB in the forespore, which triggers the action of the membrane-bound putative processing enzyme SpoIVFB. Compare this with the pro-σE pathway in Fig. 6 (see the text for further details involving negative regulators of SpoIVFB). The diagram also depicts the creation of the gene for σK by a DNA rearrangement in the mother cell chromosome.

Citation: Levin P, Losick R. 2000. Asymmetric Division and Cell Fate during Sporulation in , p 167-189. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch8
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