The existence of a cell wall–plasma membrane–cytoskeleton (WMC) continuum in plants has long been postulated. However, the individual molecules building such a continuum are still largely unknown. We test here the hypothesis that the integrin-based multiprotein complexes of animal cells have been replaced in plants with more dynamic entities. Using an experimental approach based on protoplast digestion mixtures, and utilising specific antibodies against Arabidopsis ATM1 myosin, we reveal possible roles played by plant-specific unconventional myosin VIII in the functioning of WMC continuum. We demonstrate rapid relocation (less than 5 min) of myosin VIII to statolith surfaces in maize root-cap cells, which is accompanied by the reorganisation of actin cytoskeleton. Upon prolonged stimulation, myosin VIII is also recruited to plasmodesmata and pit-fields of plasmolysing root cap statocytes. The osmotic stimulus is the major factor inducing relocation, but the cell wall–cytoskeleton interactions also play an important role. In addition, we demonstrate the tight association of myosin VIII with the surfaces of chloroplasts, and provide an indication for the differences in the mechanisms of plastid movement in roots and leaves of plants. Overall, our data provide evidence for the active involvement of actomyosin complexes, rooted in the WMC continuum, in the cellular volume control and maintenance of spatial relationships between cellular compartments.