In temperate area, nitrate (NO3-) is the main source of nitrogen for most higher plants. However, its availability greatly varies both in time and space. Plants use sophisticated adaptive mechanisms to cope with these fluctuating condition. In particular, plants are able to modify their post-embryonic development to promote root system growth in response to high local NO3- availability. Initially characterized as a NO3- carrier and sensor in Arabidopsis thaliana, studies carried out by our team showed that NRT1.1 (NFP6.3/CHL1) is also an auxin transporter in lateral root primordia thereby controlling root system growth in response to NO3-. A first part of our work extends the NRT1.1’s role in the regulation of root development by demonstrating that its action is not limited to the auxin transport in lateral roots primordia, but also orchestrates many key processes of general root auxin trafficking. In particular, our results shed light on the fact that NRT1.1 controls the auxin biosynthesis pathway which drives the hormone acropetal transport toward lateral roots primordia. Moreover, we showed that NRT1.1 also controls the auxin signaling that governs the primary root tissues remodeling to allow primordia emergence. A second part of our work aimed to study the post-transcriptional regulations of NRT1.1 by NO3-. Our results demonstrate that NO3- regulates NRT1.1 protein expression in a radically different way depending on the tissues considered. We also find that this protein is subject to an intracellular recycling and vacuolar degradation, that however does not appear to be affected by NO3-. Our work has therefore enriched our understanding of how NRT1.1 controls lateral root emergence, and highlighted a post-transcriptional regulation of NRT1.1 in aerial parts.