Glutamate drives root‑localized carbon economy and distinct absorption, transport, assimilation strategies compared with inorganic nitrogen in tobacco

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Whether plants directly absorb intact amino acids and how organic nitrogen functions as a sole nutrient remain unresolved. Using dual 15 N/ 13 C tracing in controlled hydroponics, this study demonstrates that tobacco roots absorb intact glutamate and deploy it as a distinct metabolic effector. Despite 23–49% lower 15 N recovery than nitrate, glutamate sustained comparable biomass through a root‑localized carbon metabolic economy wherein glutamate-derived carbon was oxidized predominantly in the root tricarboxylic acid cycle to fuel local nitrogen assimilation and reduce photosynthate dependency, supported by elevated root nitrate reductase (+107%) and NADH-glutamate synthase (+29%) activities. Metabolomic profiling further revealed that glutamate uniquely minimized transport-associated stress signaling, while the spared photosynthates sustained leaf tricarboxylic acid cycle activity. In contrast, ammonium diverted assimilated nitrogen toward nicotine biosynthesis and stress‑responsive metabolites at the expense of biomass, despite higher aboveground 15 N recovery, whereas nitrate maintained balanced allocation. These findings reveal an energy‑conserving metabolic architecture unique to organic nitrogen, in which low apparent nitrogen recovery coexists with high productivity through stage‑specific carbon–nitrogen reconfiguration across absorption, transport, and assimilation. This framework redefines organic nitrogen as a dual regulator of nutrition and signaling, providing a mechanistic foundation for precision nitrogen management in sustainable agroecosystems.