Abstract
We previously reported that XccR, a LuxR-type regulator of Xanthomonas campestris pv. campestris (Xcc), activates the downstream proline iminopeptidase virulence gene (pip) in response to certain host plant factor(s). In this report, we further show that the expression of the xccR gene was repressed in the culture medium by an NtrC-type response regulator, which we named XerR (XccR expression-related, repressor), and that this repression was relieved when the bacteria were grown in planta. Such a regulatory mechanism is reinforced by the observations that XerR directly bound to the xccR promoter in vitro, and that mutations at the phosphorylation-related residues of XerR resulted in the loss of its repressor function. Furthermore, the expression level of xccR increased even in XerR-overexpressing Xcc cells when they were vacuum infiltrated into cabbage plants. We also preliminarily characterized the host factor(s) involved in the above mentioned interactions between Xcc and the host plant, showing that a plant material(s) with molecular weight(s) less than 1 kDa abolished the binding of XerR to the xccR promoter, while the same material enhanced the binding of XccR to the luxXc box in the pip promoter. Taken together, our results implicate XerR in a new layer of the regulatory mechanism controlling the expression of the virulence-related xccR/pip locus and provide clues to the identification of plant signal molecules that interact with XerR and XccR to enhance the virulence of Xcc.
Similar content being viewed by others
Log in or create a free account to read this content
Gain free access to this article, as well as selected content from this journal and more on nature.com
or
Accession codes
References
Decho AW, Norman RS, Visscher PT . Quorum sensing in natural environments: emerging views from microbial mats. Trends Microbiol 2010; 18:73–80.
Mullard A . Microbiology: Tinker, bacteria, eukaryote, spy. Nature 2009; 459:159–161.
Antunes LC, Ferreira RB . Intercellular communication in bacteria. Crit Rev Microbiol 2009; 35:69–80.
Engebrecht J, Nealson K, Silverman M . Bacterial bioluminescence: isolation and genetic analysis of functions from Vibrio fischeri. Cell 1983; 32:773–781.
Miller MB, Bassler BL . Quorum sensing in bacteria. Annu Rev Microbiol 2001; 55:165–199.
Waters CM, Bassler BL . Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 2005; 21:319–346.
Bassler BL, Losick R . Bacterially speaking. Cell 2006; 125:237–246.
Ng WL, Bassler BL . Bacterial quorum-sensing network architectures. Annu Rev Genet 2009; 43:197–222.
Cao H, Yang M, Zheng H, et al. Complex quorum-sensing regulatory systems regulate bacterial growth and symbiotic nodulation in Mesorhizobium tianshanense. Arch Microbiol 2009; 191:283–289.
Chevrot R, Rosen R, Haudecoeur E, et al. GABA controls the level of quorum-sensing signal in Agrobacterium tumefaciens. Proc Natl Acad Sci USA 2006; 103:7460–7464.
Haudecoeur E, Planamente S, Cirou A, et al. Proline antagonizes GABA-induced quenching of quorum-sensing in Agrobacterium tumefaciens. Proc Natl Acad Sci USA 2009; 106:14587–14592.
Case RJ, Labbate M, Kjelleberg S . AHL-driven quorum-sensing circuits: their frequency and function among the Proteobacteria. ISME J 2008; 2:345–349.
Subramoni S, Venturi V . LuxR-family 'solos': bachelor sensors/regulators of signalling molecules. Microbiology 2009; 155:1377–1385.
Patankar AV, Gonzalez JE . Orphan LuxR regulators of quorum sensing. FEMS Microbiol Rev 2009; 33:739–756.
Lequette Y, Lee JH, Ledgham F, Lazdunski A, Greenberg EP . A distinct QscR regulon in the Pseudomonas aeruginosa quorum-sensing circuit. J Bacteriol 2006; 188:3365–3370.
Danino VE, Wilkinson A, Edwards A, Downie JA . Recipient-induced transfer of the symbiotic plasmid pRL1JI in Rhizobium leguminosarum bv. viciae is regulated by a quorum-sensing relay. Mol Microbiol 2003; 50:511–525.
McIntosh M, Krol E, Becker A . Competitive and cooperative effects in quorum-sensing-regulated galactoglucan biosynthesis in Sinorhizobium meliloti. J Bacteriol 2008; 190:5308–5317.
Ahmer BM . Cell-to-cell signalling in Escherichia coli and Salmonella enterica. Mol Microbiol 2004; 52:933–945.
Ryan RP, Dow JM . Diffusible signals and interspecies communication in bacteria. Microbiology 2008; 154:1845–1858.
Zhang L, Jia Y, Wang L, Fang R . A proline iminopeptidase gene upregulated in planta by a LuxR homolog is essential for pathogenicity of Xanthomonas campestris pv. campestris. Mol Microbiol 2007; 65:121–136.
Ferluga S, Venturi V . OryR is a LuxR-family protein involved in interkingdom signaling between pathogenic Xanthomonas oryzae pv. oryzae and rice. J Bacteriol 2009; 191:890–897.
Ferluga S, Bigirimana J, Hofte M, Venturi V . A LuxR homologue of Xanthomonas oryzae pv. oryzae is required for optimal rice virulence. Mol Plant Pathol 2007; 8:529–538.
De Carlo S, Chen B, Hoover TR, et al. The structural basis for regulated assembly and function of the transcriptional activator NtrC. Genes Dev 2006; 20:1485–1495.
Kim HS, Lee MA, Chun SJ, Park SJ, Lee KH . Role of NtrC in biofilm formation via controlling expression of the gene encoding an ADP-glycero-manno-heptose-6-epimerase in the pathogenic bacterium, Vibrio vulnificus. Mol Microbiol 2007; 63:559–574.
Freeman JA, Bassler BL . A genetic analysis of the function of LuxO, a two-component response regulator involved in quorum sensing in Vibrio harveyi. Mol Microbiol 1999; 31:665–677.
Andrade MO, Alegria MC, Guzzo CR, et al. The HD-GYP domain of RpfG mediates a direct linkage between the Rpf quorum-sensing pathway and a subset of diguanylate cyclase proteins in the phytopathogen Xanthomonas axonopodis pv citri. Mol Microbiol 2006; 62:537–551.
Stock AM, Robinson VL, Goudreau PN . Two-component signal transduction. Annu Rev Biochem 2000; 69:183–215.
Zhu X, Amsler CD, Volz K, Matsumura P . Tyrosine 106 of CheY plays an important role in chemotaxis signal transduction in Escherichia coli. J Bacteriol 1996; 178:4208–4215.
Flashner Y, Weiss DS, Keener J, Kustu S . Constitutive forms of the enhancer-binding protein NtrC: evidence that essential oligomerization determinants lie in the central activation domain. J Mol Biol 1995; 249:700–713.
Skerker JM, Perchuk BS, Siryaporn A, et al. Rewiring the specificity of two-component signal transduction systems. Cell 2008; 133:1043–1054.
Lee SY, De La Torre A, Yan D, et al. Regulation of the transcriptional activator NtrC1: structural studies of the regulatory and AAA+ ATPase domains. Genes Dev 2003; 17:2552–2563.
Rojo F . Mechanisms of transcriptional repression. Curr Opin Microbiol 2001; 4:145–151.
Rojo F . Repression of transcription initiation in bacteria. J Bacteriol 1999; 181:2987–2991.
Parker CT, Sperandio V . Cell-to-cell signalling during pathogenesis. Cell Microbiol 2009; 11:363–369.
Von Bodman SB, Bauer WD, Coplin DL . Quorum sensing in plant-pathogenic bacteria. Annu Rev Phytopathol 2003; 41:455–482.
Studholme DJ, Dixon R . Domain architectures of σ54-dependent transcriptional activators. J Bacteriol 2003; 185:1757–1767.
Kern D, Volkman BF, Luginbuhl P, et al. Structure of a transiently phosphorylated switch in bacterial signal transduction. Nature 1999; 402:894–898.
Wyman C, Rombel I, North AK, Bustamante C, Kustu S . Unusual oligomerization required for activity of NtrC, a bacterial enhancer-binding protein. Science 1997; 275:1658–1661.
Moore JB, Shiau SP, Reitzer LJ . Alterations of highly conserved residues in the regulatory domain of nitrogen regulator I (NtrC) of Escherichia coli. J Bacteriol 1993; 175:2692–2701.
Rombel I, North A, Hwang I, Wyman C, Kustu S . The bacterial enhancer-binding protein NtrC as a molecular machine. Cold Spring Harb Symp Quant Biol 1998; 63:157–166.
Boehr DD . During transitions proteins make fleeting bonds. Cell 2009; 139:1049–1051.
Gardino AK, Villali J, Kivenson A, et al. Transient non-native hydrogen bonds promote activation of a signaling protein. Cell 2009; 139:1109–1118.
Kenney LJ . How important is the phosphatase activity of sensor kinases? Curr Opin Microbiol 2010; 13:168–176.
Silversmith RE . Auxiliary phosphatases in two-component signal transduction. Curr Opin Microbiol 2010; 13:177–183.
Porter SL, Roberts MA, Manning CS, Armitage JP . A bifunctional kinase-phosphatase in bacterial chemotaxis. Proc Natl Acad Sci USA 2008; 105:18531–18536.
Newton JA, Fray RG . Integration of environmental and host-derived signals with quorum sensing during plant-microbe interactions. Cell Microbiol 2004; 6:213–224.
Piper KR, Beck Von Bodman S, Hwang I, Farrand SK . Hierarchical gene regulatory systems arising from fortuitous gene associations: controlling quorum sensing by the opine regulon in Agrobacterium. Mol Microbiol 1999; 32:1077–1089.
Liu Y, Jiang G, Cui Y, et al. kdgR Ecc negatively regulates genes for pectinases, cellulase, protease, harpinEcc, and a global RNA regulator in Erwinia carotovora subsp. carotovora. J Bacteriol 1999; 181:2411–2421.
Straight PD, Kolter R . Interspecies chemical communication in bacterial development. Annu Rev Microbiol 2009; 63:99–118.
Manefield M, Rasmussen TB, Henzter M, et al. Halogenated furanones inhibit quorum sensing through accelerated LuxR turnover. Microbiology 2002; 148:1119–1127.
Rajamani S, Bauer WD, Robinson JB, et al. The vitamin riboflavin and its derivative lumichrome activate the LasR bacterial quorum-sensing receptor. Mol Plant Microbe Interact 2008; 21:1184–1192.
Soto MJ, Dominguez-Ferreras A, Perez-Mendoza D, Sanjuan J, Olivares J . Mutualism versus pathogenesis: the give-and-take in plant-bacteria interactions. Cell Microbiol 2009; 11:381–388.
Yang Z, Rogers LM, Song Y, Guo W, Kolattukudy PE . Homoserine and asparagine are host signals that trigger in planta expression of a pathogenesis gene in Nectria haematococca. Proc Natl Acad Sci USA 2005; 102:4197–4202.
Turner P, Barber C, Daniels M . Behavior of the transposons Tn5 and Tn7 in Xanthomonas campestris pv. campestris. Mol Gen Genet 1984; 195:101–107.
Schafer A, Tauch A, Jager W, et al. Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene 1994; 145:69–73.
Skerker JM, Prasol MS, Perchuk BS, Biondi EG, Laub MT . Two-component signal transduction pathways regulating growth and cell cycle progression in a bacterium: a system-level analysis. PLoS Biol 2005; 3:e334.
Innes RW, Hirose MA, Kuempel PL . Induction of nitrogen-fixing nodules on clover requires only 32 kilobase pairs of DNA from the Rhizobium trifolii symbiosis plasmid. J Bacteriol 1988; 170:3793–3802.
Pogliano J, Lynch AS, Belin D, Lin EC, Beckwith J . Regulation of Escherichia coli cell envelope proteins involved in protein folding and degradation by the Cpx two-component system. Genes Dev 1997; 11:1169–1182.
Lynch AS, Lin EC . Transcriptional control mediated by the ArcA two-component response regulator protein of Escherichia coli: characterization of DNA binding at target promoters. J Bacteriol 1996; 178:6238–6249.
Acknowledgements
This work was supported by grants from the National Natural Science Foundation of China (No 31030008 and No 30471135), and the National Basic Research Program of China (2011CB100700).
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
About this article
Cite this article
Wang, L., Zhang, L., Geng, Y. et al. XerR, a negative regulator of XccR in Xanthomonas campestris pv. campestris, relieves its repressor function in planta. Cell Res 21, 1131–1142 (2011). https://doi.org/10.1038/cr.2011.64
Received:
Revised:
Accepted:
Published:
Issue date:
DOI: https://doi.org/10.1038/cr.2011.64
Keywords
This article is cited by
-
Interkingdom signaling in plant-microbe interactions
Science China Life Sciences (2017)
-
Secretome analysis of rice suspension-cultured cells infected by Xanthomonas oryzae pv.oryza (Xoo)
Proteome Science (2016)


