Plant pathogenic bacteria, such as Pseudomonas syringae strain PtoDC3000, respond to host signals through complex signaling networks that regulate bacterial growth and virulence. The plant hormone indole-3-acetic acid (IAA), also known as auxin, promotes bacterial pathogenesis via multiple mechanisms, including through reprogramming of bacterial transcription. However, the mechanisms that PtoDC3000 uses to sense and respond to auxin are not well understood. Here, we identify a novel bacterial auxin-signaling mechanism mediated by pmeR, which encodes a TetR-like family transcriptional repressor that acts as an important regulator of IAA-responsive gene expression in PtoDC3000. Using qRT-PCR and transcriptional reporter assays, we show that pmeR is induced by IAA and regulates several auxin-responsive genes. pmeR plays two different roles in the regulation of auxin-responsive genes: as a repressor of its own expression and as an activator of other genes. Plant infection assays further show that the disruption of pmeR results in reduced bacterial growth in Arabidopsis thaliana. Notably, although PmeR de-represses the transcription of pmeR upon IAA treatment, it does not appear to directly bind IAA. Rather, our biochemical results indicate that the auxin conjugate IAA-lysine may serve as a ligand for PmeR. Our findings reveal a complex signaling network through which IAA modulates bacterial gene expression and emphasize the role of PmeR in acclimating PtoDC3000 for growth in plant tissue.IMPORTANCEPhytopathogenic bacteria respond to host signals through intricate signaling mechanisms that regulate bacterial growth and virulence. One key host signal involved in these interactions is the phytohormone indole-3-acetic acid (IAA), which has been shown to promote Pseudomonas syringae strain PtoDC3000 pathogenicity in Arabidopsis thaliana and tomato. However, the mechanisms for sensing and responding to IAA remain unclear. Here, we identify pmeR, encoding a TetR-like family transcriptional regulator (TFR), as a key component of the bacterial response to auxin. To our knowledge, pmeR represents the first characterized TFR to participate in bacterial auxin perception. We demonstrate that pmeR is induced by IAA and regulates a set of auxin-responsive genes, several of which are implicated in virulence. We also identify the IAA conjugate IAA-lysine as a potential ligand for PmeR. These findings uncover a novel regulatory mechanism underlying bacterial auxin perception and suggest strategies for controlling bacterial plant diseases through targeted hormone-responsive pathways.