Thaxtomin A, a key phytotoxin produced by plant pathogenic Streptomyces sp., is implicit in common scab disease expression in potato. Primary targets and modes of action of thaxtomin A toxicity in plant cells are not well understood. In this work, early signalling events associated with thaxtomin A toxicity were studied using the ion-selective microelectrode ion flux estimation (MIFE) technique. Thaxtomin A-induced changes in net ion fluxes were measured across the plasma membrane (PM) of root and pollen tube tissue in Arabidopsis thaliana and tomato. Within a minute after toxin application, a rapid and short-lived Ca2+ influx was observed. Well ahead of the marked inhibition of root growth, a significant shift towards net H+ efflux across the PM occurred in all tissues. Similar to root tissues, thaxtomin A significantly modified ion flux profiles from growing pollen tubes. Thaxtomin A was more effective in young, physiologically active tissues (root elongation zone or pollen tube apex), suggesting a higher density of thaxtomin A-binding sites in these regions. Overall, our data provide the first evidence that thaxtomin A triggers an early signalling cascade, which may be crucial in plant-pathogen interactions. It also suggests a possible interaction between thaxtomin A and PM auxin receptors, as revealed from experiments on the auxin-sensitive ucu2-2/gi2 A. thaliana mutant.