Degradation of the Plant Defense Signal Salicylic Acid Protects Ralstonia solanacearum from Toxicity and Enhances Virulence on Tobacco

Abstract

Plants use the signaling molecule salicylic acid (SA) to trigger defenses against diverse pathogens, including the bacterial wilt pathogen Ralstonia solanacearum. SA can also inhibit microbial growth. Most sequenced strains of the heterogeneous R. solanacearum species complex can degrade SA via gentisic acid to pyruvate and fumarate. R. solanacearum strain GMI1000 expresses this SA degradation pathway during tomato pathogenesis. Transcriptional analysis revealed that subinhibitory SA levels induced expression of the SA degradation pathway, toxin efflux pumps, and some general stress responses. Interestingly, SA treatment repressed expression of virulence factors, including the type III secretion system, suggesting that this pathogen may suppress virulence functions when stressed. A GMI1000 mutant lacking SA degradation activity was much more susceptible to SA toxicity but retained the wild-type colonization ability and virulence on tomato. This may be because SA is less important than gentisic acid in tomato defense signaling. However, another host, tobacco, responds strongly to SA. To test the hypothesis that SA degradation contributes to virulence on tobacco, we measured the effect of adding this pathway to the tobacco-pathogenic R. solanacearum strain K60, which lacks SA degradation genes. Ectopic addition of the GMI1000 SA degradation locus, including adjacent genes encoding two porins and a LysR-type transcriptional regulator, significantly increased the virulence of strain K60 on tobacco. Together, these results suggest that R. solanacearum degrades plant SA to protect itself from inhibitory levels of this compound and also to enhance its virulence on plant hosts like tobacco that use SA as a defense signal molecule.

Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly

“…Salicylic acid for example, a key regulator of plant metabolism, induces systemic resistance in plants to suppress growth of pathogenic microorganisms 34 . Although some plant pathogens have been reported to degrade it 55 , salicylic acid has been shown to be necessary for the assembly of a 'normal' root microbiome of Arabidopsis thaliana 16 , and together with gamma-aminobutyric acid, salicylic acid concentration has been shown to correlate with specific taxa frequently enriched in the rhizosphere 14 . Taken together with our observations, it appears that the ability to preferentially consume salicylic acid may be a distinguishing feature of rhizosphere bacteria.…”

Pandemonium Breaks Out: Disruption of Salicylic Acid-Mediated Defense by Plant Pathogens

“…highly susceptible to biotrophic and semi-biotrophic pathogens (Gaffney et al, 1993;Delaney et al, 1994). Degradation of SA by Ralstonia solanacearum through the Nag Pathway The bacterial pathogen Ralstonia solanacearum, which causes tomato wilt disease, is able to degrade SA into gentisic acid via the Nag pathway (Lowe-Power et al, 2016) (Figure 1). This process involves the activation of the NagGH and NagAaAb genes by SA.…”

“…Gentisic acid was found to be 10 times less toxic to R. solanacearum compared with SA, thus allowing the pathogen to infect and spread in the host plant. The Nag pathway continues to break down SA further into maleylpyruvate, then fumarylpyruvate, and lastly into pyruvate and fumarate, all of which are inactive for plant defense signal transduction and not toxic or only slightly toxic to R. solanacearum (Lowe-Power et al, 2016). Thus, degradation of SA by the Nag pathway contributes to the fitness and pathogenicity of R. solanacearum in infected tomato plants.…”

Plant–phytopathogen interactions: bacterial responses to environmental and plant stimuli

“…Hence, the ability to degrade HCA contributes to bacterial wilt virulence by facilitating root entry and by protecting the pathogen from HCA toxicity (Lowe et al, 2015). Similarly, the pathogen has a pathway for degrading the plant defense signal salicylic acid (SA) and this degradation ability protects it from SA toxicity and enhances its virulence on tobacco (Lowe-Power et al, 2016). In addition to enzymatic degradation of specific plant defense compounds, R. solanacearum uses multidrug efflux pumps (MDR) to extrude antimicrobial compounds.…”