AMF-mediated samarium tolerance in Avena sativa: insights into primary metabolism, amino acid biosynthesis, and flavonoid accumulation

Abstract

BACKGROUND: Samarium (Sm), a rare earth element increasingly released into the environment through industrial activities and electronic waste, can adversely affect plant growth and metabolism. Although arbuscular mycorrhizal fungi (AMF) are known to enhance plant tolerance to various abiotic stresses, their role in mitigating Sm toxicity and regulating metabolic pathways in oat (Avena sativa L.) remains poorly understood. This study investigated the physiological and metabolic mechanisms underlying AMF-mediated Sm tolerance in oat plants. METHODS: A greenhouse pot experiment was conducted using oat plants grown under control conditions or exposed to Sm stress (125 and 250 mg kg⁻¹ soil), with or without Rhizophagus irregularis inoculation. Plant growth, grain yield, photosynthetic performance, nutrient status, Sm accumulation, carbohydrate metabolism, nitrogen-assimilating enzymes, amino acid profiles, organic and fatty acids, and secondary metabolites were analyzed. RESULTS: Sm exposure markedly impaired plant performance, reducing grain yield by up to 60% and decreasing the photosynthetic rate by 43.2-60% compared to the control. Sm stress also disrupted nutrient acquisition and induced substantial metabolic imbalances. AMF inoculation significantly alleviated these adverse effects by reducing Sm accumulation in plant tissues (by 21.7% and 31.5% at the low and high Sm levels, respectively) and increasing grain yield by up to 33.9% compared with non-inoculated stressed plants. AMF enhanced carbohydrate metabolism (increasing glucose content and starch synthase activity) and stimulated nitrogen metabolism by increasing glutamine synthetase and glutamate dehydrogenase activities, leading to greater accumulation of several amino acids. AMF also promoted the accumulation of organic acids, fatty acids, and protective secondary metabolites (phenolics and tocopherols). Effects on phenolics, flavonoids, and antioxidant capacity were treatment-dependent, with AMF generally enhancing these parameters under non-stressed or low-Sm conditions while modulating the stress-induced responses at high Sm concentrations. CONCLUSIONS: AMF effectively mitigated Sm-induced toxicity in oat by limiting Sm accumulation, preserving photosynthetic function, enhancing primary metabolism, stimulating amino acid biosynthesis, and promoting protective secondary metabolites. These findings provide new insights into the metabolic basis of AMF-mediated tolerance to rare earth element stress and highlight the potential application of AMF as a sustainable strategy for crop production in contaminated soils.