Functional Insights into SlNPF, SlNRT2, and SlAMT Gene Families in Tomato: Leaf Metabolic Performance Controls Root-to-Shoot Nitrogen Partitioning

Low Nitrogen Use Efficiency (NUE) remains a critical agricultural challenge, as an estimated 50–70% of applied nitrogen (N) is lost, resulting in negative environmental impacts and reduced crop production. To elucidate molecular mechanism controlling NUE in tomato (Solanum lycopersicum), we conducted a comprehensive genomic, transcriptomic, and functional analysis of the NPF, NRT2, and AMT transporter families under high-N commercial supply conditions. Our integrated analysis identified a shoot-to-root signaling mechanism where the plant’s metabolic performance systematically regulates N transport capacity. Under N sufficiency, the shoot exhibited reduced N assimilation, evidenced by NO3− accumulation (increased by 55.7%) and reduced Nitrate Reductase (NR) and Glutamine Synthetase (GS) activities (54.0% and 43.2% reduction, respectively), which correlated with a 42.3% reduction in chlorophyll synthesis capacity. This reduction in metabolic demand systematically triggered the downregulation of the key long-distance SlNPF transporters, SlNPF2.13 and SlNPF7.3, restricting N translocation and promoting significant root N accumulation (increased by 41.8%). Our data established that the leaf metabolic state is the systemic regulator of N transport and identified SlNPF2.13 and SlNPF7.3 as pivotal molecular checkpoints. These findings indicate that the manipulation of these transporters could serve as a valuable tool in molecular breeding programs to significantly enhance NUE in commercial tomato varieties.