Salmonella enterica exploits the auxin signaling pathway to overcome stomatal immunity

Abstract

Stomata on the leaf surface can be entry ports for various microbes to gain access to the apoplast. Plants can prevent, or at least diminish, microbial internalization through the activation of pattern-triggered immunity (PTI) in guard cells, a phenomenon known as stomatal immunity. The human pathogen Salmonella enterica serovar Typhimurium strain 14028s (STm 14028s) can overcome PTI and reopen the stomata; however, the underlying mechanism has been elusive. Here, we provide evidence that biosynthesis of auxin from its precursor tryptophan in both the bacterium and the host plant is required for stomatal re-opening in response to STm 14028s, but not Pseudomonas syringae pv. tomato (Pst) strain DC3000. STm 14028s produces auxin on the leaf surface through indole pyruvate decarboxylase (ipdC) and it induces auxin biosynthesis in Arabidopsis likely through YUC5. The heterologous expression of STm 14028s ipdC in Escherichia coli serotype O157:H7 partially restores stomatal reopening, as this bacterium does not induce plant auxin biosynthesis. In addition, auxin signaling is required for STm 14028s-triggered stomatal re-opening evidenced by the lack of response in the tir1-10, axr1-3, and aux1-7 mutants, or in the presence of auxin signaling inhibitors. Overall, our findings underline the unique role of auxin in the interaction between STm 14028s and Arabidopsis as mechanism to overcome stomatal immunity.