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4 Contact-Dependent Signaling in : the Function of the C-Signal in Fruiting Body Morphogenesis

Author: Lotte Søgaard-Andersen1
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Affiliations: 1: Max Planck Institute for Terrestrial Microbiology, Karl-von-Frisch Str., 35043 Marburg, Germany
Content Type: Monograph
Publication Year: 2008
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Abstract:

The intercellular C-signal has a fundamental role in fruiting body morphogenesis in . In this chapter, our current understanding of how the C-signal acts at the molecular level to induce and coordinate events that are separated in time and space is discussed. The first evidence for intercellular signals important for fruiting body formation came from the isolation of a collection of mutants that displayed nonautonomous developmental defects. Importantly, aggregation, sporulation, and C-signal-dependent gene expression were induced earlier than in wild-type cells, whereas the rippling stage was completely skipped. Random transposon mutagenesis followed by screening for mutants with deficiencies in C-signal-dependent responses, isolation of extragenic suppressors of a insertion mutant, proteomics, and biochemical analyses have been instrumental in the identification of proteins in this pathway. Several regulatory mechanisms help to restrict the activity of the pathway to starving cells. First, starvation induces the stringent response, which, in turn, induces transcription and A-signal accumulation, which induces transcription. Secondly, starvation induces mrpAB expression, and MrpAB induces mrpC transcription. Thirdly, by an unknown mechanism secretion of MXAN0206, the protease likely to cleave p25, is induced. Moreover, the establishment of cell-biology-based methods with green fluorescent protein (GFP) fusion proteins and immunofluorescence are likely to result in the detailed understanding of the spatial organization of cells during starvation.

Citation: Søgaard-Andersen L. 2008. 4 Contact-Dependent Signaling in : the Function of the C-Signal in Fruiting Body Morphogenesis, p 77-91. In Whitworth D (ed), Myxobacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815677.ch4
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4 Contact-Dependent Signaling in Myxococcus xanthus : the Function of the C-Signal in Fruiting Body Morphogenesis
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Citation: Søgaard-Andersen L. 2008. 4 Contact-Dependent Signaling in : the Function of the C-Signal in Fruiting Body Morphogenesis, p 77-91. In Whitworth D (ed), Myxobacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815677.ch4
/content/10.1128/9781555815677.ch04.ch04fig01
Figure 1
Schematic outline of fruiting body morphogenesis in . The different morphological stages are indicated. Triangles indicate genes that are induced at different time points during fruiting body formation. Filled and open triangles indicate C-signal-independent and -dependent genes, respectively. The times at which the intercellular A- and C-signals become important for development are indicated. The level of C-signaling that individual cells are exposed to is indicated by the level of gray. The grayscale below the timeline indicates C-signaling levels in individual cells.
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10.1128/9781555815677/f0078-01.gif
Image of Figure 1
Figure 1

Schematic outline of fruiting body morphogenesis in . The different morphological stages are indicated. Triangles indicate genes that are induced at different time points during fruiting body formation. Filled and open triangles indicate C-signal-independent and -dependent genes, respectively. The times at which the intercellular A- and C-signals become important for development are indicated. The level of C-signaling that individual cells are exposed to is indicated by the level of gray. The grayscale below the timeline indicates C-signaling levels in individual cells.

Citation: Søgaard-Andersen L. 2008. 4 Contact-Dependent Signaling in : the Function of the C-Signal in Fruiting Body Morphogenesis, p 77-91. In Whitworth D (ed), Myxobacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815677.ch4
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Figure 2
The C-signal transduction pathway. (A) Model of the C-signal transduction pathway. Three different levels of phosphorylated FruA (FruA-P) are indicated, with the stippled circle indicating a low level and the heavy circle indicating a high level of phosphorylation. The encircled numbers indicate processes initiated at low, intermediate, and high levels of C-signaling and which may correspond to low, intermediate, and high levels of FruA phosphorylation, respectively. The shaded box indicates the site of convergence of the MXAN4899, SdeK, TodK, and RodK pathways with the C-signal transduction pathway. See the text for details. (B) Regulation of MrpC activity. See the text for details.
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10.1128/9781555815677/f0082-01.gif
Image of Figure 2
Figure 2

The C-signal transduction pathway. (A) Model of the C-signal transduction pathway. Three different levels of phosphorylated FruA (FruA-P) are indicated, with the stippled circle indicating a low level and the heavy circle indicating a high level of phosphorylation. The encircled numbers indicate processes initiated at low, intermediate, and high levels of C-signaling and which may correspond to low, intermediate, and high levels of FruA phosphorylation, respectively. The shaded box indicates the site of convergence of the MXAN4899, SdeK, TodK, and RodK pathways with the C-signal transduction pathway. See the text for details. (B) Regulation of MrpC activity. See the text for details.

Citation: Søgaard-Andersen L. 2008. 4 Contact-Dependent Signaling in : the Function of the C-Signal in Fruiting Body Morphogenesis, p 77-91. In Whitworth D (ed), Myxobacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815677.ch4
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Figure 3
A quantitative model for C-signal-induced responses. The three signal amplification loops in the C-signal transduction pathway are indicated. See the text for details.
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10.1128/9781555815677/f0085-01.gif
Image of Figure 3
Figure 3

A quantitative model for C-signal-induced responses. The three signal amplification loops in the C-signal transduction pathway are indicated. See the text for details.

Citation: Søgaard-Andersen L. 2008. 4 Contact-Dependent Signaling in : the Function of the C-Signal in Fruiting Body Morphogenesis, p 77-91. In Whitworth D (ed), Myxobacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815677.ch4
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Figure 4
Model for C-signal-induced aggregation. (A) The basic event with the end-to-end contact between two cells with C-signal transmission followed by a change in cell behavior. (B) Chain formation. This event is a consequence of end-to-end contacts with C-signal transmission between. The formation of a chain depends on the sequential recruitment of cells as shown in the four panels. Cells engaged in C-signal transmission are shown to move towards an aggregation center indicated in gray to the left with a low reversal frequency. Non-C-signaling cells move with a high reversal frequency as indicated by the double-headed arrow. (C) Stream formation. Movement of cells in a chain is predicted to create alignment of neighboring cells with the formation of secondary chains of cells (marked by dark color). Cells in secondary chains are associated with the primary chain by lateral cell-cell contacts and with other cells in the secondary chain by end-to-end contacts. Together, an initiating chain and its associated secondary chains will make up a stream. (D) Stream formation in vivo. Cell arrangements were visualized by fluorescence microscopy of GFP-labeled cells. GFP-labeled wild-type cells were codeveloped with nonfluorescent wild-type cells at a ratio of 1 to 40. Images were acquired after the indicated hours of starvation. Circles in the 6-h image indicate aggregation centers; arrows indicate streams. Scale bar, 50 μm.
10.1128/9781555815677/f0088-01_thmb.gif
10.1128/9781555815677/f0088-01.gif
Image of Figure 4
Figure 4

Model for C-signal-induced aggregation. (A) The basic event with the end-to-end contact between two cells with C-signal transmission followed by a change in cell behavior. (B) Chain formation. This event is a consequence of end-to-end contacts with C-signal transmission between. The formation of a chain depends on the sequential recruitment of cells as shown in the four panels. Cells engaged in C-signal transmission are shown to move towards an aggregation center indicated in gray to the left with a low reversal frequency. Non-C-signaling cells move with a high reversal frequency as indicated by the double-headed arrow. (C) Stream formation. Movement of cells in a chain is predicted to create alignment of neighboring cells with the formation of secondary chains of cells (marked by dark color). Cells in secondary chains are associated with the primary chain by lateral cell-cell contacts and with other cells in the secondary chain by end-to-end contacts. Together, an initiating chain and its associated secondary chains will make up a stream. (D) Stream formation in vivo. Cell arrangements were visualized by fluorescence microscopy of GFP-labeled cells. GFP-labeled wild-type cells were codeveloped with nonfluorescent wild-type cells at a ratio of 1 to 40. Images were acquired after the indicated hours of starvation. Circles in the 6-h image indicate aggregation centers; arrows indicate streams. Scale bar, 50 μm.

Citation: Søgaard-Andersen L. 2008. 4 Contact-Dependent Signaling in : the Function of the C-Signal in Fruiting Body Morphogenesis, p 77-91. In Whitworth D (ed), Myxobacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815677.ch4
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