Rapid adjustment of plant physiology and development to external fluctuations is critical for sessile organism, giving a singular interest to network signaling controlling these mechanisms. Among many adaptation processes, root plasticity is primordial to optimize nutrient acquisition but relies on a complex network integrating local and systemic (root <-> shoot) signaling. Indeed, locally, plants invest resource in soil area where nutrients are available and systemically they adjust nutrient acquisition to the whole plant demand. Our main goal is to decipher systemic signaling underlying the perception of nitrate heterogeneous provision, in Arabidopsis. Using the split-root system, in which physically isolated root systems of the same plant were challenged with different environments, we previously demonstrated that cytokinin biosynthesis constitutes one critical component of root-shoot-root communication. By combining the use of cytokinin mutants with hormone measurements, transcriptomic analysis, nitrate uptake assays, and root growth measurements, we show that root to shoot trans-zeatin (tZ) translocation is likely crucial for long distance signaling controlling rapid sentinel gene regulation and long-term functional acclimation to heterogeneous nitrate supply. Interestingly, shoot transcriptome profiling revealed that glutamate/glutamine metabolism is likely a target of tZ root-to-shoot translocation, prompting an interesting hypothesis regarding shoot-to-root communication. Finally, this study also highlights tZ-independent pathways triggered by variation into nitrogen supply.