Physiological, transcriptomic and MdABR1-mediated mechanisms underlying manganese resistance in 'Fuji' apple

Manganese (Mn) toxicity is a major factor limiting apple yield and quality. To cope with manganese stress, apple trees regulate the uptake of external Mn while maintaining internal homeostasis of growth and stress responses. However, research on the physiological and transcriptomic responses of the apple trees 'Fuji' to Mn stress remains limited. In this study, we found that Mn stress significantly inhibited the growth of apple seedlings, leading to Mn accumulation, increased hydrogen peroxide (H₂O₂), nutrient imbalances, degradation of photosynthetic pigments and impaired photosynthesis. Simultaneously, the increase in antioxidant enzymes (superoxide dismutase, catalase, and peroxidase) and the accumulation of antioxidants (glutathione, flavonoids, non-protein thiols, and proline) helped alleviate oxidative stress induced by Mn toxicity. Transcriptome analysis identified 458 differentially expressed genes (DEGs), including genes from the AP2/ERF gene family and metal-binding proteins. GO and KEGG analyses highlighted key pathways, such as cell wall biosynthesis, phenylpropanoid biosynthesis, and fatty acid elongation, emphasizing the molecular mechanisms involved in manganese detoxification and stress adaptation. MdABR1 was confirmed to play a crucial role in reducing Mn bioaccumulation and regulating Mn toxicity through yeast genetic transformation and transient expression in tobacco. Based on the physiological and transcriptomic results, a systemic regulatory model for apple's response to Mn toxicity was constructed, providing a valuable foundation for developing apple varieties with enhanced resistance to Mn toxicity and offering insights for future breeding strategies.