Root system morphology was characterized in the seedlings of heavy-metal sensitive Arabidopsis thaliana, the non-metallicolous (NM) and metallicolous (M) populations of the tolerant A. arenosa and A. halleri, developed on the natural soils: the Zn-Pb-Cd-Cu-contaminated (C soils), the non-contaminated (NC soils), and on an identical nutrient-rich compost. Anatomy of primary roots grown on agar medium with control and elevated zinc concentrations was investigated also in the model A. thaliana ecotype Columbia. The three Arabidopsis species differed in morphological and/or quantitative responses to the varying soil qualities. Comparing to natural NC soil, the morphology of A. thaliana root system differed only on the compost with dominating lateral root lengths while the root lengths were reduced on the C soil. In NM and M populations of A. arenosa the lateral root elongation and density were reduced on the C soil and root growth but not lateral root density were stimulated on the compost. In NM and M populations of A. halleri the root system morphology remained unaltered in all three soils. The root elongation was reduced but lateral root initiation increased on the C soil while the roots were longer and lateral root density lower on the compost. The responses of A. arenosa or A. halleri populations differed only in absolute root lengths. The similarity in morphological responses to varying soil metal contents indicated plastic responses rather than heritable traits of the root systems. The root tissue organization three Arabidopsis species resembled the known A. thaliana ecotype Columbia. Quantitatively, the tolerant species and their M populations had thicker roots due to a greater number and size of cells in epidermis, cortex including a higher number of middle cortex cells, and endodermis. The rates of root growth and quantitative root anatomy may represent morphological traits contributing to heavy metal tolerance of the Arabidopsis species.