SlSTOP1-SlFRDL1-mediated citrate exudation modulates apoplastic iron-redox homeostasis to promote primary root elongation under phosphate deficiency in tomato.

Phosphate (Pi) deficiency dramatically reshapes root system architecture (RSA) in a species-dependent manner. In Arabidopsis thaliana, a well-studied STOP1-ALMT1 malate-exudation module promotes iron (Fe)-dependent reactive oxygen species (ROS) accumulation in root apices, leading to primary root (PR) inhibition. In contrast, agronomically important crops such as tomato (Solanum lycopersicum) exhibit PR promotion under Pi deficiency, but the underlying mechanisms remain unclear. Here, we show that in tomato the C2H2-type transcription factor SlSTOP1 promotes PR elongation under low Pi by activating citrate-dependent control of apoplastic iron (Fe) redox chemistry. Using Slstop1 and Slfrdl1 loss-of-function mutants, genomic complementation lines, and root co-culture assays, we demonstrate that SlSTOP1 induces the citrate transporter SlFRDL1 to drive citrate exudation, limiting Fe overaccumulation and spatially confined reactive oxygen species (ROS) accumulation in the root apex. Under Pi deficiency, disruption of SlSTOP1 or SlFRDL1 suppresses PR growth, enhances Perls/DAB-detected apoplastic Fe accumulation, and increases DAB/NBT-detected H2O2 and O2·- accumulation sites, whereas exogenous citrate or antioxidant treatment partially restores root growth. In vitro ferrozine and electron paramagnetic resonance assays further reveal that Fe-citrate complexes generate moderate Fe2+ and hydroxyl radicals compared with Fe-malate complexes, while low external H2O2 concentrations promote, but high concentrations inhibit, PR elongation. Together, these results identify a rewired SlSTOP1-SlFRDL1-citrate module that replaces the Arabidopsis STOP1-ALMT1-malate pathway, converting an inhibitory Fe-ROS signal into a growth-permissive redox regime and providing a mechanistic basis for species-specific root adaptation to Pi deficiency.