Abstract
BACKGROUND: Peanut exhibits sensitivity to manganese (Mn) toxicity in acidic soil, but the molecular mechanisms remain unclear. This study used physiological, transcriptomic, and metabolomic analyses to investigate peanut root and leaf responses to Mn toxicity. RESULTS: Mn toxicity reduced plant biomass, plant height, leaf chlorophyll and caused leaf yellowing. In roots, the contents of Proline (Pro), Ascorbate Peroxidase (APX) and soluble sugar increased by 41.78%, 148.98% and 107.52%, respectively, whereas malondialdehyde (MDA) decreased by 28.92%. In leaves, Pro, APX and soluble sugar increased by 876.49%, 138.98% and 455.20%, respectively, whereas MDA decreased by 39.54%. High Mn stress (300 µM vs. 10 µM) elevated the levels of IAA, T-Zeatin, ABA, SA, JA, and GA3 in leaves (by 33.01%, 49.76%, 58.56%, 435.56%, 2368.97%, and 1218.10%) and SA, JA, and GA3 in roots (by 478.36%, 413.53%, and 730.56%), while decreasing T-Zeatin in roots by 27.37%. Additionally, Mn stress disrupted ion absorption and transport. Transcriptomic analysis identified 4107 differentially expressed genes (DEGs) in roots and 657 in leaves, including those involved in antioxidant enzymes, ion transport and hormone pathways. Metabolomic analysis revealed 399 differentially expressed metabolites (DEMs) in leaves and 362 in roots. Key enriched pathways included phenylpropanoid biosynthesis in roots and tryptophan metabolism and plant hormone signal transduction in leaves. Functional analysis of AhMTP9, a key gene in the plant hormone signal transduction pathway, showed its localization to the cell membrane. Heterologous expression of AhMTP9 in Arabidopsis thaliana increased plant height, rosette leaf diameter, soluble sugar and reduced MDA content under high Mn stress, paralleling trends observed in peanut. CONCLUSIONS: These findings advance understanding of Mn toxicity effects on peanut development and offer a foundation for improving Mn tolerance in peanuts through genetic approaches.