Iron homeostasis is critical for plant growth; however, the mechanisms underlying responses to iron deficiency and toxicity remain poorly understood. We investigated the adaptive strategies of Ulmus pumila, focusing on leaf physiological, transcriptomic, and metabolomic responses to iron stresses. Both iron deficiency and toxicity impaired chlorophyll biosynthesis, PS II efficiency, and chloroplast ultrastructure, resulting in reduced photosynthetic capacity and etiolation/wilting phenotypes. Iron deficiency reduced antioxidant enzyme activity and ROS levels, while iron toxicity activated the antioxidant enzyme system in response to the ROS burst. Integrated transcriptomic and metabolomic analyses provided insights into the underlying mechanism of these divergent responses: iron deficiency promoted primary metabolic adjustments, particularly the upregulation of genes (e.g., MDH, ACO, and IDH) and metabolites (e.g., malic acid, citric acid, and fumaric acid) associated with the TCA cycle to meet energy demands. Conversely, iron toxicity triggered a metabolic shift from primary to secondary metabolism, upregulating the genes (e.g., CHS, CHI, and F3H) and metabolites (e.g., laricitrin, trifolin, and rutin) involved in flavonoids biosynthesis to mitigate oxidative stress. Overall, U. pumila employs distinct adaptive mechanisms to balance survival and growth under iron stress: prioritizing energy metabolism and iron uptake to meet energy demands and improve iron uptake efficiency under deficiency, and enhancing the secondary metabolism to mitigate oxidative damage under toxicity. These findings enhance understanding of plant nutrient homeostasis and stress adaptation, providing insights into mitigating the impacts of soil degradation on agriculture and forestry.
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