Trends in Microbiology

Trends in Microbiology

Volume 15, Issue 8, August 2007, Pages 363-371
Journal home page for Trends in Microbiology

Review
Global virulence regulation networks in phytopathogenic bacteria

https://doi.org/10.1016/j.tim.2007.06.005Get rights and content

Phytopathogens coordinate multifaceted life histories and deploy stratified virulence determinants via complex, global regulation networks. We dissect the global regulation of four distantly related model phytopathogens to evaluate large-scale events and mechanisms that determine successful pathogenesis. Overarching themes include dependence on centralized cell-to-cell communication systems, pervasive two-component signal-transduction systems, post-transcriptional regulation systems, AraC-like regulators and sigma factors. Although these common regulatory systems control virulence, each functions in different capacities, and to differing ends, in the diverse species. Hence, the virulence regulation network of each species determines its survival and success in various life histories and niches.

Section snippets

Global virulence regulation networks dictate life histories and infection strategies

Phytopathogens survive in diverse environments, not only as pathogens but also as benign epiphytes on plant surfaces or saprophytes in soil and water. Consequently, expression of virulence factors and behaviors associated with virulence must be coordinated for energy conservation, appropriate disease development, evasion of host defense and eventual dispersal. The survival of a phytopathogen, therefore, relies on a controlled global virulence regulation network. Here, we discuss such networks

Cell-density-dependent regulation of virulence factors is crucial for all four phytopathogens

Cell-to-cell communication systems enable temporally coordinated gene expression within bacterial populations. The infection strategies of phytopathogens, which often require swift global changes in gene expression and physiology in response to environmental cues, are particularly reliant on cell-to-cell communication to coordinate crucial steps in pathogenesis. Some of the communication systems of phytopathogens are paradigmatic quorum-sensing systems, analogous in mechanism to the conserved

TCST systems provide environmental signal input to global virulence regulation

TCST systems are commonly used by bacteria to sense and adapt to extracellular environmental signals. The two common, and well studied, components are a membrane-bound sensor kinase and a cognate, cytoplasmic response regulator (for review, see Ref. [27]). Subsequent to signal perception, the cytoplasmic response regulator is either activated or inactivated by phosphorylation. The response regulator can carry out a variety of tasks, including transcriptional regulation and protein–protein

AraC-type regulators regulate T3SS expression in R.s. and X.c.c.

AraC-type regulators commonly have important virulence regulation roles in association with T3SSs in animal and plant bacterial pathogens. Particularly in enterobacterial pathogens such as Salmonella, Shigella, Yersinia and Escherichia coli, AraC-like regulators are key activators of T3SS expression. Pseudomonas aeruginosa also relies on an AraC-like transcription activator, ExsA, to regulate the T3SS [39]. Interestingly, neither P.s. nor P.c.c. use AraC-like proteins to regulate their T3SS,

Concluding remarks

Phytopathogens coordinate transitions in life histories and infection strategies by collecting information from the host plant, the environment and their own population density. These inputs result in a collection of virulence outputs in each species that is determined by integrated, global regulation networks. The current evidence indicates that virulence regulation networks in the phytopathogens we profile here center on global regulators and cell-density-dependent regulation. Complementary

Acknowledgements

We thank Marc Nishimura, Amy Charkowski, Caitilyn Allen and Max Dow for unpublished photographs. Thanks to Caitilyn Allen, Amy Charkowski and the reviewers for their helpful and constructive comments. J.L.D. is supported by NIH grant 5-RO1-GM06625, DOE grant DE-FG02–95ER20187 and NSF grant IOB-0114795, SRG is supported by NSF grants IOB-0416952 and BE-0412599.

References (73)

  • U. Gophna

    Bacterial type III secretion systems are ancient and evolved by multiple horizontal-transfer events

    Gene

    (2003)
  • S.C. De Keersmaecker

    Let LuxS speak up in AI-2 signaling

    Trends Microbiol.

    (2006)
  • D. White

    Phylogenetic distribution of the global regulatory gene csrA among eubacteria

    Gene

    (1996)
  • C. Valverde

    A repeated GGA motif is critical for the activity and stability of the riboregulator RsmY of Pseudomonas fluorescens

    J. Biol. Chem.

    (2004)
  • M.A. Schell

    Control of virulence and pathogenicity genes of Ralstonia solanacearum by an elaborate sensory network

    Annu. Rev. Phytopathol.

    (2000)
  • A.M. Barnard et al.

    Quorum sensing in Erwinia species

    Anal. Bioanal. Chem.

    (2007)
  • S.M. Brumbley

    Phenotype conversion in Pseudomonas solanacearum due to spontaneous inactivation of PhcA, a putative LysR transcriptional regulator

    J. Bacteriol.

    (1993)
  • S.J. Clough

    A two-component system in Ralstonia (Pseudomonas) solanacearum modulates production of PhcA-regulated virulence factors in response to 3-hydroxypalmitic acid methyl ester

    J. Bacteriol.

    (1997)
  • A.B. Flavier

    Identification of 3-hydroxypalmitic acid methyl ester as a novel autoregulator controlling virulence in Ralstonia solanacearum

    Mol. Microbiol.

    (1997)
  • J. Huang

    Joint transcriptional control of xpsR, the unusual signal integrator of the Ralstonia solanacearum virulence gene regulatory network, by a response regulator and a LysR-type transcriptional activator

    J. Bacteriol.

    (1998)
  • G. Bhatt et al.

    Ralstonia solanacearum iron scavenging by the siderophore staphyloferrin B is controlled by PhcA, the global virulence regulator

    J. Bacteriol.

    (2004)
  • A.B. Flavier

    Hierarchical autoinduction in Ralstonia solanacearum: control of acyl-homoserine lactone production by a novel autoregulatory system responsive to 3-hydroxypalmitic acid methyl ester

    J. Bacteriol.

    (1997)
  • M. Pirhonen

    A small diffusible signal molecule is responsible for the global control of virulence and exoenzyme production in the plant pathogen Erwinia carotovora

    EMBO J.

    (1993)
  • M. Welch

    N-acyl homoserine lactone binding to the CarR receptor determines quorum-sensing specificity in Erwinia

    EMBO J.

    (2000)
  • S. Sjoblom

    Cooperation of two distinct ExpR regulators controls quorum sensing specificity and virulence in the plant pathogen Erwinia carotovora

    Mol. Microbiol.

    (2006)
  • Y. Cui

    ExpR, a LuxR homolog of Erwinia carotovora subsp. carotovora, activates transcription of rsmA, which specifies a global regulatory RNA-binding protein

    J. Bacteriol.

    (2005)
  • L.H. Wang

    A bacterial cell–cell communication signal with cross-kingdom structural analogues

    Mol. Microbiol.

    (2004)
  • Y.W. He

    Genome scale analysis of diffusible signal factor regulon in Xanthomonas campestris pv. campestris: identification of novel cell–cell communication-dependent genes and functions

    Mol. Microbiol.

    (2006)
  • J.M. Dow

    Biofilm dispersal in Xanthomonas campestris is controlled by cell–cell signaling and is required for full virulence to plants

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

    (2003)
  • H. Slater

    A two-component system involving an HD-GYP domain protein links cell–cell signalling to pathogenicity gene expression in Xanthomonas campestris

    Mol. Microbiol.

    (2000)
  • P. Ross

    Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylic acid

    Nature

    (1987)
  • Y.W. He

    Xanthomonas campestris cell–cell communication involves a putative nucleotide receptor protein Clp and a hierarchical signalling network

    Mol. Microbiol.

    (2007)
  • B. Quinones

    Regulation of AHL production and its contribution to epiphytic fitness in Pseudomonas syringae

    Mol. Plant Microbe Interact.

    (2004)
  • B. Quinones

    Quorum sensing regulates exopolysaccharide production, motility, and virulence in Pseudomonas syringae

    Mol. Plant Microbe Interact.

    (2005)
  • J.M. Monier et al.

    Differential survival of solitary and aggregated bacterial cells promotes aggregate formation on leaf surfaces

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

    (2003)
  • J. Huang

    A complex network regulates expression of eps and other virulence genes of Pseudomonas solanacearum

    J. Bacteriol.

    (1995)

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