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Manganese (Mn) and aluminum (Al) toxicities are serious edaphic limitations to crop production in acidic soils. Excess Mn can be countered using a stress-adapted soil microbiota that establish symbiotic relationships with native plants. The arbuscular mycorrhizal fungi (AMF) associated with Lolium rigidum L. develop extraradical mycelia (ERM) that quickly colonize wheat and lead to greater shoot growth by promoting stress-evading mechanisms that are not yet completely explained. In the present study, wheat growth was assessed after 3 weeks on disturbed and undisturbed (intact ERM) acidic soil where the native non-mycotrophic Silene gallica L. or strongly mycotrophic L. rigidum were previously developed. The physiological and biochemical mechanisms responsible for increased growth were analyzed by assessing wheat leaf chlorophyll content, photosystem II quantum yield and performance index, enzymatic activity of ascorbate peroxidase (APX), catalase (CAT), glutathione reductase (GR), guaiacol peroxidase (GPX), superoxide dismutase (SOD) and contents and subcellular localization of Mn, Mg, Si and K. The soil from native plants had a beneficial effect on shoot weight and chlorophyll levels. The highest benefits were obtained for wheat grown in soil with intact ERM associated with L. rigidum. In this condition, where earlier mycorrhization was favored, the Mn content decreased, alongside the content of Si, while the Mg/Mn ratio increased. Mn was redirected to the apoplast, while Si was redirected to the symplast. The activity of APX, GPX and SOD increased, probably due to increased metabolic growth (higher shoot weight and chlorophyll content). Understanding the mechanisms induced by native AMF responsible for increasing wheat performance can contribute to the establishment of sustainable approaches for crop production in acidic soils with Mn toxicity. The use of native plant AMF developers can improve the sustainable use of natural resources in the scope of greener agricultural practices. [ABSTRACT FROM AUTHOR]