Role of the PhoP-PhoQ System in the Virulence of Erwinia chrysanthemi Strain 3937: Involvement in Sensitivity to Plant Antimicrobial Peptides, Survival at Acid pH, and Regulation of Pectolytic Enzymes

Abstract

Erwinia chrysanthemi is a phytopathogenic bacterium that causes soft-rot diseases in a broad number of crops. The PhoP-PhoQ system is a key factor in pathogenicity of several bacteria and is involved in the bacterial resistance to different factors, including acid stress. Since E. chrysanthemi is confronted by acid pH during pathogenesis, we have studied the role of this system in the virulence of this bacterium. In this work, we have isolated and characterized the phoP and phoQ mutants of E. chrysanthemi strain 3937. It was found that: (i) they were not altered in their growth at acid pH; (ii) the phoQ mutant showed diminished ability to survive at acid pH; (iii) susceptibility to the antimicrobial peptide thionin was increased; (iv) the virulence of the phoQ mutant was diminished at low and high magnesium concentrations, whereas the virulence of the phoP was diminished only at low magnesium concentrations; (v) in planta Pel activity of both mutant strains was drastically reduced; and (vi) both mutants lagged behind the wild type in their capacity to change the apoplastic pH. These results suggest that the PhoP-PhoQ system plays a role in the virulence of this bacterium in plant tissues, although it does not contribute to bacterial growth at acid pH.

TheErwinia chrysanthemi3937 PhoQ Sensor Kinase Regulates Several Virulence Determinants

“…At high Mg 2ϩ and acidic pH, resistance to the antibacterial peptide magainin II was severely reduced specifically in the phoQ mutant but not in the phoP mutant compared to that in the wild-type (WT) strain (28). Similarly, differences were observed with respect to virulence for the mutants at high Mg 2ϩ concentrations (the phoQ mutant was more virulent), although at low (10 M) magnesium concentrations, both mutants showed equally diminished virulence (35). Furthermore, in transcriptomic analysis of E. chrysanthemi phoP and phoQ mutants, it was found that the set of genes differentially regulated in the two mutants showed only minimal overlap (Venkatesh et al, unpublished results).…”

“…The phospho-PhoP transcriptionally activates or represses a large number of loci involved in diverse cellular functions (17,24,25,29,42), and, therefore, it has been placed on a par with global regulators such as Crp, Fnr, and ArcA (62). The E. chrysanthemi phoQ and phoP mutants have been previously partially characterized independently by two groups, and these studies have demonstrated the involvement of the E. chrysanthemi PhoPQ system in regulating synthesis of pectinolytic enzymes, its growth at acidic pH, and/or alkalization of external pH in planta, as well as its resistance to antimicrobial peptides (28,35,36). The PhoPQ system can participate in complex regulatory cascades that allow the integration of multiple signals and serve to expand the signal transduction network so as to allow some genes to respond to various signals in the environment (56).…”

The Role of Secretion Systems and Small Molecules in Soft-Rot Enterobacteriaceae Pathogenicity

“…However, despite the importance of ions in virulence, relatively little is known about regulation in response to most of these signals. As with related genera, SRE use the PhoPQ two-component system and SlyA, which responds to magnesium levels, to monitor their environment and control expression of virulence genes (42,52,53,90,92) . In addition to regulation, ions also affect the efficacy of virulence proteins, and this has been most clearly demonstrated with SRE pectate lyases.…”

Characterization of Xylella fastidiosa popP Gene Required for Pathogenicitya

“…PhoPPhoQ of X. oryzae pv. oryzae (Xoo), E. carotovora, and E. chrysanthemi appears to be cell density-dependent in plant host [4][5][6][7][8][9][10]. In this study, while both wild type and popP mutant X. fastidiosa strains showed similar growth curves in vitro, grapevines infected with popP deletion strain have significantly decreased bacterial populations in comparison to the bacterial populations of grapevines inoculated with wild type.…”

“…oryzae, TCS PhoP-PhoQ was recently shown to be a requirement for the induction of density-dependent gene expression, including genes related with biofilm formation [4][5][6][7]. PhoP-PhoQ controls virulence functions in the plant pathogen Erwinia carotovora and E. chrysanthemi [8][9][10][11]. A cell wall degrading enzyme endopolygalacturonase (designated PehA) secreted by Erwinia is transcriptionally regulated by the PhoP-PhoQ homologue PehR-PehS, and the pehR or pehS deficient of Erwinia are attenuated for virulence in tobacco seedlings [8].…”