Cadmium (Cd) is a phytotoxic heavy metal that causes rapid growth reduction. To investigate if Cd interferes with the metabolism of auxin, a major growth hormone in plants, poplars (Populus × canescens) expressing a heterologous GH3::GUS reporter gene were exposed to 50 μM Cd in hydroponic solutions. Growth, photosynthetic performance, lignification, peroxidase activity, auxin concentration, and GUS staining were determined in order to record the activities of GH3 enzymes in the stem apex, the elongation zone, wood in the zone of radial growth, and in roots. Cd-induced growth reductions were tissue-specific decreasing in the order: roots>wood>shoot elongation and leaf initiation, whereas Cd concentrations increased in the order: leaves<wood<roots. Cd almost abolished the GH3 signal in the stem apex but caused strong increases in the vascular system of roots as well as in parenchymatic cells in the xylem. These changes were accompanied by increases in lignin and peroxidase activities and decreases in auxin concentrations. Since GH3 enzymes remove auxin from the active pool by conjugation and act as mediators between growth and defence, our data suggest that Cd stress triggered increases in GH3 activities which, in turn, depleted auxin in wood and thereby shunted the metabolism to enhanced formation of lignin.