Auxin biosynthesis and signaling drive virulence and plant adaptation in Dickeya dadantii

Plants and their associated bacteria engage in complex bidirectional interactions mediated by a diverse array of signaling molecules of both plant and microbial origin. Indole-3-acetic acid (IAA) is a central phytohormone regulating plant growth and development and is increasingly recognized as an intra- and inter-kingdom signaling molecule that modulates diverse bacterial processes relevant during plant-microbe interactions. While IAA biosynthesis is widespread among plant-associated bacteria, the mechanisms through which this auxin regulates bacterial physiology and virulence, as well as those controlling its production, remain poorly understood. Here, we show that IAA synthesis deficiency in the global phytopathogen Dickeya dadantii triggers transcriptional reprogramming and results in reduced virulence and fitness during plant infection. Endogenous IAA was found to regulate the expression of the AaeXAB efflux pump, which mediates endogenous IAA secretion, confers resistance to plant defense-related phytohormones, and contributes to plant virulence in D. dadantii. Consistent with its role in plant-bacteria interactions, phylogenetic analyses revealed that AaeXAB-encoding genes are commonly present among Pseudomonadota isolated from plant-associated environments. Moreover, IAA deficiency altered the expression of a previously uncharacterized indole-responsive MarR-type regulator, DDA3937_RS07305, suggesting cross-talk between IAA- and indole-mediated signaling networks. Our data also uncover a complex regulatory circuit coordinating IAA production in D. dadantii, involving the ExpIR and Vfm quorum-sensing systems and the transcriptional regulators TyrR, TrpR, and LrhA. Collectively, our findings provide new insights into the role of IAA as a bacterial signal promoting plant adaptation and virulence. Targeting IAA biosynthesis and efflux pump activity may offer promising avenues for the development of anti-virulence strategies in phytopathogenesis.