Screening pertinent breeding traits for crop adaptation to low N supply remains difficult because plant response is a set of interacting processes, displaying a wide genetic and environmental variability. To integrate processes, a whole-plant structure-function model was developed on A. thaliana. Based on interactions between N/C fluxes, it offers an explicit and dynamic description of root system and leaf area growth. The model was used to estimate in what extend homogeneous limiting N supply affects root architecture via the decrease in carbon availability, due to leaf area reduction. A. thaliana plants were grown in rhizotrons on a combination of C x N levels. Only 12 parameters, kept to the same values for all C x N datasets, were needed to satisfyingly simulate contrasted responses of root system architecture under our steady-state conditions, indicating that the major effect of global N availability on root system architecture was mediated by modifications of C fluxes. Then, the root part of the model was simplified to characterize genetic variability of plant response and to identify the key parameters determining plant efficiency toward low N nutrition. We used this model to interpret the behaviour of five RILs and one mutant impaired on high affinity nitrate uptake. We found that the main source of variation relied on nitrogen uptake and carbon assimilation efficiencies, indicating that these parameters were the major determinants of plant response variability to steady-state N supply. The determining role of the AtNRT2.1 gene was also confirmed. This work highlights how few key-mechanisms and related genes identified through modelling impact whole-plant phenotype.