The Melatonin-Nitric Oxide Signaling Pathway Alleviates Iron Starvation by Mobilizing Apoplastic Iron Pools and...

Iron (Fe) is indispensable for plant growth and development. Notably, melatonin (MT) serves as a key regulator to improve plant tolerance under nutrient stress conditions. Currently, the exact mechanism regulating MT's involvement in the rice Fe-deficiency response remains to be elucidated. This study reveals that Fe-deficiency stress triggers a rapid increase in endogenous MT levels in rice roots and induces the expression of MT synthesis-related genes, underscoring the involvement of MT in the rice Fe-starvation response. Exogenously applied MT rescues the root growth inhibition triggered by Fe deficiency and efficiently mitigates leaf chlorosis in rice. Mechanistically, MT decreases Fe retention in the root cell wall and its hemicellulose fraction, thereby promoting the remobilization of stored Fe and increasing soluble Fe content. Additionally, MT selectively reshapes the transport networks by robustly upregulating genes associated with Strategy II Fe acquisition and internal Fe transport-including Ferric Reductase Defective 3-like 1 (OsFRDL1), Iron-related transcription factor 3 (OsIRO3), Nicotianamine Aminotransferase 1 (OsNAAT1), OsNAS1, OsNAS2, Yellow Stripe-Like 2 (OsYSL2), and OsYSL15-to accelerate root-to-shoot Fe translocation. Notably, this enhanced internal Fe recycling partially improves the plant's Fe nutritional status, which is consistent with a systemic negative feedback response that partially attenuates the core Strategy I ferrous iron transporters (OsIRT1/2) along with root-surface ferric reductase (FCR) activity and proton secretion. Moreover, nitric oxide (NO) acts as a pivotal downstream mediator in MT-induced mitigation of the rice Fe-starvation response. In conclusion, MT alleviates Fe deficiency in rice by promoting the remobilization of hemicellulose-bound Fe and enhancing root-to-shoot Fe translocation in an NO-dependent manner. These processes are accompanied by partial attenuation of root-surface FCR activity, proton secretion, and OsIRT1/2 expression, revealing a coordinated adjustment between internal Fe reutilization and external Fe-acquisition responses.