Root architecture can be profoundly affected by the carbon availability in the plant. We hypothesized that this effect could be mediated by the carbon status of root cells involved in elongation and branching processes. Arabidopsis thaliana plants were grown at several photosynthetic photon flux densities (PPFD) and were supplied with various sucrose concentrations in the root medium. Hexose and sucrose concentration was estimated in individual roots in the apical growing region of the primary root and of secondary roots as well as in the zone of primordia development. Local sugar concentration was high in fast-growing and in highly branched roots and robust relationships between root elongation rate or branching and hexose concentration (but not sucrose) were found that were common to all situations experienced. Moreover, these relationships accounted for the plant-to-plant variability within a treatment as well as for the variability among individual secondary roots within a plant. These results support the view that local hexose concentration integrates changes in carbon availability from several sources and acts as a signal to induce at least part of the response of the root architecture to the environment.