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J. Biol. Chem., Vol. 281, Issue 44, 33414-33421, November 3, 2006

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Dual Signaling Functions of the Hybrid Sensor Kinase RpfC of Xanthomonas campestris Involve Either Phosphorelay or Receiver Domain-Protein Interaction^*

Ya-Wen He, Chao Wang, Lian Zhou, Haiwei Song, J. Maxwell Dow, and Lian-Hui Zhang¹

From the Institute of Molecular and Cell Biology, 61 Biopolis Drive, Singapore 138673 and BIOMERIT Research Centre, Department of Microbiology, BioScience Institute, National University of Ireland, Cork, Ireland

The hybrid sensor kinase RpfC positively regulates the expression of a range of virulent genes and negatively modulates the synthesis of the quorum sensing signal diffusible signal factor (DSF) in Xanthomonas campestris. Three conserved amino acid residues of RpfC implicated in phosphorelay (His¹⁹⁸ in the histidine kinase domain, Asp⁵¹² in the receiver domain, and His⁶⁵⁷ in the histidine phosphotransfer domain) were essential for activation of the production of extracellular enzymes and extracellular polysaccharide (EPS) virulence factors but were not essential for repression of DSF biosynthesis. Domain deletion and subsequent in trans expression analysis revealed that the receiver domain of RpfC alone was sufficient to repress DSF overproduction in an rpfC deletion mutant. Further deletion and alanine scanning mutagenesis analyses identified a peptide of 107 amino acids and three amino acid residues (Gln⁴⁹⁶, Glu⁵⁰⁴, and Ile⁵⁵²) involved in modulating DSF production. Co-immunoprecipitation and far Western blot analyses suggested an interaction between the receiver domain and RpfF, the enzyme involved in DSF biosynthesis. These data support a model in which RpfC modulates two different functions (virulence factor synthesis and DSF synthesis) by utilization of a conserved phosphorelay system and a novel domain-specific protein-protein interaction mechanism, respectively. This latter mechanism represents an added dimension to conventional two-component signaling paradigms.

Received for publication, July 11, 2006 , and in revised form, August 29, 2006.

^* The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Table S1 and Figs. S1 and S2.

¹ To whom correspondence should be addressed: Institute of Molecular and Cell Biology, 61 Biopolis Dr., Singapore 138673. Tel.: 65-6586-9686; Fax: 65-6779-1117; E-mail: lianhui{at}imcb.a-star.edu.sg.

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