Nitrogen (N) deficiency critically affects wheat development and productivity. Our study aimed to decipher tolerance mechanisms to N deficiency regulated by a QTL transferred into bread wheat from wild emmer wheat (WEW). Root system architecture (RSA) and transcriptome modifications in response to severe N deficiency were compared between the introgression (IL99) and its cultivated parent. Higher plasticity was demonstrated in IL99 by modifying the growth strategy of RSA coordinated with shoot development. These included a shift in root orientation from shallow to steep, more and longer roots, and higher root networks, enabling nutrient acquisition from a larger volume and deeper soil layers. Transcriptome analyses revealed gene-expression reprogramming, highlighted by unique GO and KEGG-enriched pathways in leaves and toots. Based on transcriptome results and protein-protein interaction, we identified promising candidate genes associated with uptake of NO ₃ ^- (high-affinity transporter NRT2.4), increased root lignification ( trans-cinnamate 4-monooxygenase (CYP73A), and 4-coumarate-CoA ligase (4CL)). Jasmonic acid, known as associated with plasticity of RSA, was predominant among other plant hormones identified in this study, by activating allene oxide synthase ( AOS1), TIFY proteins, transcription factors MTB2 and MYC2. Transcriptomic and developmental changes in IL99 demonstrated fundamental mechanisms underlying its enhanced N-use efficiency and stress tolerance attributed to WEW.