Exogenous citric acid-mediated modification of metabolism, transport and signal transduction of non-structural carbohydrates in rice under hexavalent chromium stress

Hexavalent chromium [Cr(VI)] is a highly toxic heavy metal that adversely affects plant growth and development. Non-structural carbohydrates (NSCs) serve as dynamic metabolic buffers under environmental stress, balancing growth and detoxification demands. This study elucidates how exogenous citric acid (CA) alters subcellar distribution of Cr(VI) and reprograms NSC allocation to alleviate Cr(VI) toxicity in Oryza sativa through integrated biochemical and transcriptomic analyses. CA application significantly enhanced biomass growth in Cr(VI)-stressed seedlings, with Cr(VI) redistribution across subcellular compartments and NSC reconfiguration. Tissue-specific transcriptomic shifts revealed CA-mediated modulation of NSC metabolic genes, transporters, and signaling components. Genome-scale metabolic network modeling identified OsNIN4 and OsTPP3 as predicted regulatory nodes to mediate a dynamic equilibrium between NSC partitioning and Cr(VI) detoxification in roots of Cr(VI)-treated rice seedlings supplied with exogenous CA. OsNIN4 suppressed sucrose synthesis to favor nitrogen-based defenses, while OsTPP3 enhanced fructose retention via trehalose-OsSnRK signaling network from “CA + Cr(VI)” treatments. Divergent expression patterns of other NSC-associated genes revealed the multifaceted regulatory mechanism governing NSC metabolism, translocation, and stress-responsive signaling. Exogenous CA application improved the growth of Cr(VI)-treated rice seedlings. The integrated analysis of genome-scale metabolic network indicated OsNIN4 and OsTPP3 as predicted regulatory nodes for optimizing NSC flux during CA-mediated Cr(VI) detoxification in rice plants.