Flagellin recognition triggers zinc mobilization in Arabidopsis thaliana as a response to Salmonella Typhimurium invasion

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Abstract
Salmonella enterica serovar Typhimurium can enter and colonize the apoplast of plants, including the edible ones, making them a potential reservoir for the pathogen and a route for human contamination. We previously showed that in Arabidopsis thaliana shoot colonization, S. Typhimurium takes advantage of its ability to export zinc primarily through the P1B-type ATPase ZntA induced by zinc excess. Moreover, a plant line with reduced ability to translocate zinc from roots to shoots is more susceptible to S. Typhimurium shoot colonization. We, therefore, hypothesized that plants employ zinc intoxication as a defense strategy against invading bacteria. Here we show that, upon S. Typhimurium colonization, A. thaliana modulates the expression of zinc transporters, favoring the long-distance movement of the metal as well as lowering zinc storage into the plant vacuoles. Notably, we demonstrate that this strategy depends on the recognition of bacterial flagellin by the FLS2 receptor, a signal that triggers the PAMP-Triggered Immunity response in plants. Disrupting this interaction, either using an S. Typhimurium Δfla strain or an A. thaliana fls2 mutant line, reduces the zntA expression in shoot-colonizing bacteria. This observation is confirmed by a luminescent zinc biosensor assay, showing that the A. thaliana fls2 does not increase bioavailable zinc in the S. Typhimurium colonized shoots. Moreover, gene expression analyses in the colonized fls2 line revealed a downregulation of the root-to-shoot zinc translocation compared to Col-0. Overall, our results suggest that flagellin recognition by plants triggers zinc fluxes towards the invading bacteria as a facet of the PAMP-Triggered Immunity response, highlighting the importance of plant zinc homeostasis for the interaction with human pathogens.

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