The phytohormone indole-3-acetic acid induces quorum sensing signal DSF turnover via a positive feedback biosynthetic loop in the phytopathogen Xanthomonas campestris

Abstract

Indole-3-acetic acid (IAA) accumulates in host plants following infection by Xanthomonas campestris pv. campestris (Xcc), the causal agent of cruciferous black rot. How exposure to IAA affects the invading Xcc remains unclear. Here, we demonstrate that either exogenous addition of IAA or endogenous production of IAA induced turnover of the quorum sensing (QS) signal diffusible signaling factor (DSF) in a RpfB-dependent manner. IAA addition prevented the cytoplasmic and culture pH decline. Transcriptomic analyses revealed four IAA-regulated gene clusters. Specifically, IAA induced the expression of trpB-A, enhancing tryptophan biosynthesis and intracellular IAA accumulation, and thereby establishing a self-reinforcing synthesis loop. IAA upregulated F0F1 ATP synthases and a resistance-nodulation-cell division (RND)-family efflux pump HepABCD to induce a pH-dependent DSF turnover. Moreover, IAA downregulated another RND family efflux pump IaepABCDE to induce a pH-independent DSF turnover. Finally, the IAA-regulated gene clusters were transcribed during the XC1 infection of cabbage. Collectively, these findings reveal a previously unrecognized role of IAA in modulating bacterial QS, underscoring the importance of IAA in the molecular dialogue between the pathogen and its host.