Zinc acts as an intracellular second messenger, connecting environmental changes to transcriptional regulation in root nodules of legumes, which maintain nitrogen homeostasis through symbiotic bacteria. The study identifies the transcriptional regulator FIXATION UNDER NITRATE (FUN), which controls the transition between an inactive filamentous structure and an active regulator. Lower zinc levels in nodules, induced by higher soil nitrate, dissociate the filament and activate FUN. FUN then targets multiple pathways to initiate nodule breakdown. This zinc-dependent filamentation mechanism adjusts nodule function to environmental nitrogen conditions. The findings have implications for understanding metal ion roles in integrating environmental signals with plant development and optimizing nitrogen delivery in legumes.Zinc acts as an intracellular second messenger, connecting environmental changes to transcriptional regulation in root nodules of legumes, which maintain nitrogen homeostasis through symbiotic bacteria. The study identifies the transcriptional regulator FIXATION UNDER NITRATE (FUN), which controls the transition between an inactive filamentous structure and an active regulator. Lower zinc levels in nodules, induced by higher soil nitrate, dissociate the filament and activate FUN. FUN then targets multiple pathways to initiate nodule breakdown. This zinc-dependent filamentation mechanism adjusts nodule function to environmental nitrogen conditions. The findings have implications for understanding metal ion roles in integrating environmental signals with plant development and optimizing nitrogen delivery in legumes.