Identification of an activator protein required for the induction of
            <i>fruA</i>
            , a gene essential for fruiting body development in
            <i>Myxococcus xanthus</i>

Ueki, Toshiyuki; Inouye, Sumiko

doi:10.1073/pnas.1533026100

Cited by 73 publications

(126 citation statements)

References 39 publications

(50 reference statements)

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“…MrpC is similar to CRPfamily transcription factors and was shown previously to be essential for development (20). A form of MrpC lacking the N-terminal 25 residues, called MrpC2, was identified previously in an AS fraction based on binding to the fruA promoter region (24). Our results suggested that MrpC2 in the AS fraction binds to the fmgA promoter region at a site (Ϫ63 to Ϫ46) important for promoter activity.…”

supporting

confidence: 64%

“…Cooperative binding of FruA and MrpC2 to the fmgA promoter region and other promoter regions, together with activation of fruA transcription by MrpC2 (24), represents a coherent feed-forward regulatory loop design found commonly in regulatory networks because of its beneficial characteristics (38). C-signaling could affect production of MrpC2 and/or activity of FruA (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…Expression of fruA depends on MrpC2 (Fig. S1) (24), so neither transcription factor is expected to accumulate in a mrpC mutant. However, MrpC and MrpC2 accumulate normally in a fruA mutant (19) (data not shown), yet fmgA fails to be expressed (17).…”

Section: Frua Is Required For Association Of Mrpc And/or Mrpc2 With Tmentioning

confidence: 99%

“…1 A) (18), suggesting that a transcriptional activator binds to this region and perhaps to similar sequences in other C-signal-dependent promoter regions. To identify the putative activator, DNA-binding proteins were partially purified as described previously (24) from M. xanthus that had undergone 12 h of development, a time when fmgA is expressed (18). Proteins in the AS fraction were incubated with a 32 P-labeled DNA fragment (Ϫ101 to ϩ25) spanning the fmgA promoter region, and electrophoretic mobility shift assays (EMSAs) revealed a single shifted complex (Fig.…”

mentioning

confidence: 99%

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A combination of unusual transcription factors binds cooperatively to control Myxococcus xanthus developmental gene expression

Mittal

Kroos

2009

Proc. Natl. Acad. Sci. U.S.A.

144

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Myxococcus xanthus is a bacterium that undergoes multicellular development requiring coordinate regulation of multiple signaling pathways. One pathway governs aggregation and sporulation of some cells in a starving population and requires C-signaling, whereas another pathway causes programmed cell death and requires the MazF toxin. In response to starvation, the levels of the bifunctional transcription factor/antitoxin MrpC and its related proteolytic fragment MrpC2 are increased, inhibiting the cell death pathway via direct interaction of MrpC with MazF. Herein, we demonstrate that MrpC2 plays a direct role in the transcriptional response to C-signaling. We show that MrpC2 binds to sequences upstream of the C-signal-dependent fmgA promoter. These sequences are present in other C-signal-dependent promoter regions, indicating a general role for MrpC2 in developmental gene regulation. Association of MrpC and/or MrpC2 with the fmgA promoter region in vivo requires FruA, a protein that is similar to response regulators of 2-component signal transduction systems, but may not be phosphorylated. DNA binding studies showed that this association likely involves an unusual mechanism for a response regulator in which FruA and MrpC2 bind cooperatively to adjacent sites upstream of the fmgA promoter. We propose that this unusual mechanism of combinatorial control allows coordination of morphogenetic C-signaling with starvation signaling and cell death, determining spatiotemporal gene expression and cell fate.bacterial development ͉ C-signaling ͉ cell fate ͉ signal transduction ͉ sporulation

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supporting

confidence: 64%

Section: Discussionmentioning

confidence: 99%

Section: Frua Is Required For Association Of Mrpc And/or Mrpc2 With Tmentioning

confidence: 99%

mentioning

confidence: 99%

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A combination of unusual transcription factors binds cooperatively to control Myxococcus xanthus developmental gene expression

Mittal

Kroos

2009

Proc. Natl. Acad. Sci. U.S.A.

144

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“…The expression of fruA is developmentally regulated, dependent on A-and E-signals, and initiates at 6 h after the onset of development. Recently, a fruA promoter-binding protein was isolated from developmental cell extracts by using a DNA binding assay with the DNA fragment containing the upstream region of the fruA promoter (9). Based upon its partial sequence, this fruA promoter-binding protein was found to be identical to MrpC, which belongs to the cyclic AMP receptor protein family of transcriptional regulators (9).…”

Section: Fruiting Body Development In Myxococcus Xanthus Is a Multicementioning

confidence: 99%

Identification of a Gene Involved in Polysaccharide Export as a Transcription Target of FruA, an Essential Factor for Myxococcus xanthus Development

Ueki

Inouye

2005

Journal of Biological Chemistry

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Fruiting body development in Myxococcus xanthus is a multicellular event that is coordinated by exchanging intercellular signals.FruA is a transcription factor essential for fruiting body development and is thought to play a key role in the C-signal pathway. Here we present the first identification of a gene regulated by FruA. The gene was isolated from a genomic library via in vitro selection in a DNA binding assay by using the DNA-binding domain of FruA tagged with His 8 at the C-terminal end (FruA-DBD-H 8 ). The gene, named fdgA (FruA-dependent gene A), encodes a protein homologous to the outer-membrane auxiliary family protein involved in the polysaccharide export system. FruA-DBD-H 8 bound the upstream promoter region of the fdgA gene from nucleotide ؊89 to nucleotide ؊64 with respect to the transcription initiation site, which was required for the induction of fdgA expression during development. fdgA mRNA induced during development was absent in a fruA deletion strain. The deletion of fdgA resulted in defective fruiting body formation and reduced sporulation efficiency (1% that of the parent strain). Moreover, FruA was required for the developmental expression of sasA, which is also involved in the biosynthesis of the lipopolysaccharide O-antigen and is required for fruiting body development. Furthermore, the expression of both fdgA and sasA was partially dependent on the C-signal. These findings expand our understanding of the signal transduction pathway mediated by FruA during development in M. xanthus.

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An Evo‐Devo Perspective on Multicellular Development of Myxobacteria

et al. 2017

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The transition to multicellularity, recognized as one the major transitions in evolution, has occurred independently several times. While multicellular development has been extensively studied in zygotic organisms including plant and animal groups, just a few aggregative multicellular organisms have been employed as model organisms for the study of multicellularity. Studying different evolutionary origins and modes of multicellularity enables comparative analyses that can help identifying lineage-specific aspects of multicellular evolution and generic factors and mechanisms involved in the transition to multicellularity. Among aggregative multicellular organisms, myxobacteria are a valuable system to explore the particularities that aggregation confers to the evolution of multicellularity and mechanisms shared with clonal organisms. Moreover, myxobacteria species develop fruiting bodies displaying a range of morphological diversity. In this review, we aim to synthesize diverse lines of evidence regarding myxobacteria development and discuss them in the context of Evo-Devo concepts and approaches. First, we briefly describe the developmental processes in myxobacteria, present an updated comparative analysis of the genes involved in their developmental processes and discuss these and other lines of evidence in terms of co-option and developmental system drift, two concepts key to Evo-Devo studies. Next, as has been suggested from Evo-Devo approaches, we discuss how broad comparative studies and integration of diverse genetic, physicochemical, and environmental factors into experimental and theoretical models can further our understanding of myxobacterial development, phenotypic variation, and evolution.

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Identification of an activator protein required for the induction of fruA , a gene essential for fruiting body development in Myxococcus xanthus

Cited by 73 publications

References 39 publications

A combination of unusual transcription factors binds cooperatively to control Myxococcus xanthus developmental gene expression

A combination of unusual transcription factors binds cooperatively to control Myxococcus xanthus developmental gene expression

Identification of a Gene Involved in Polysaccharide Export as a Transcription Target of FruA, an Essential Factor for Myxococcus xanthus Development

An Evo‐Devo Perspective on Multicellular Development of Myxobacteria

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