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Aluminum (Al) and manganese (Mn) toxicity are the top two constraints of crop production in acid soil. Crops have evolved common and specific mechanisms to tolerate the two stresses. In the present study, the responses (toxicity and tolerance) of near-isogenic wheat lines (ET8 and ES8) and their parents (Carazinho and Egret) to Al and Mn were compared by determining the physiological parameters and conducting transcriptome profiling of the roots. The results showed the following: (1) Carazinho and ET8 exhibited dual tolerance to Al and Mn compared to Egret and ES8, indicated by higher relative root elongation and SPAD. (2) After entering the roots, Al was mainly distributed in the roots and fixed in the cell wall, while Mn was mainly distributed in the cell sap and then transported to the leaves. Both Al and Mn stresses decreased the contents of Ca, Mg, and Zn; Mn stress also inhibited the accumulation of Fe, while Al showed an opposite effect. (3) A transcriptomic analysis identified 5581 differentially expressed genes (DEGs) under Al stress and 4165 DEGs under Mn stress. Among these, 2774 DEGs were regulated by both Al and Mn stresses, while 2280 and 1957 DEGs were exclusively regulated by Al stress and Mn stress, respectively. GO and KEGG analyses indicated that cell wall metabolism responds exclusively to Al, while nicotianamine synthesis exclusively responds to Mn. Pathways such as signaling, phenylpropanoid metabolism, and metal ion transport showed commonality and specificity to Al and Mn. Transcription factors (TFs), such as MYB, WRKY, and AP2 families, were also regulated by Al and Mn, and a weighted gene co-expression network analysis (WGCNA) identified PODP7, VATB2, and ABCC3 as the hub genes for Al tolerance and NAS for Mn tolerance. The identified genes and pathways can be used as targets for pyramiding genes and breeding multi-tolerant varieties.

Aluminum (Al) toxicity and low phosphorus availability (LP) are the top two co-existing edaphic constraints limiting agriculture productivity in acid soils. Plants have evolved versatile mechanisms to cope with the two stresses alone or simultaneously. However, the specific and common molecular mechanisms, especially those involving flavonoids and carbohydrate metabolism, remain unclear. Laboratory studies were conducted on two wheat genotypes—Fielder (Al-tolerant and P-efficient) and Ardito (Al-sensitive and P-inefficient)—exposed to 50 μM Al and 2 μM Pi (LP) in hydroponic solutions. After 4 days of stress, wheat roots were analyzed using transcriptomics and targeted metabolomics techniques. In Fielder, a total of 2296 differentially expressed genes (DEGs) were identified under Al stress, with 1535 upregulated and 761 downregulated, and 3029 DEGs were identified under LP stress, with 1591 upregulated and 1438 downregulated. Similarly, 4404 DEGs were identified in Ardito under Al stress, with 3191 upregulated and 1213 downregulated, and 1430 DEGs were identified under LP stress, with 1176 upregulated and 254 downregulated. GO annotation analysis results showed that 4079 DEGs were annotated to the metabolic processes term. These DEGs were significantly enriched in the phenylpropanoid, flavonoid, flavone and flavonol biosynthesis, and carbohydrate metabolism pathways by performing the KEGG enrichment analysis. The targeted metabolome analysis detected 19 flavonoids and 15 carbohydrate components in Fielder and Ardito under Al and LP stresses. In Fielder, more responsive genes and metabolites were involved in flavonoid metabolism under LP than Al stress, whereas the opposite trend was observed in Ardito. In the carbohydrate metabolism pathway, the gene and metabolite expression levels were higher in Fielder than in Ardito. The combined transcriptome and metabolome analysis revealed differences in flavonoid- and carbohydrate-related genes and metabolites between Fielder and Ardito under Al and LP stresses, which may contribute to Fielder’s higher resistance to Al and LP. The results of this study lay a foundation for pyramiding genes and breeding multi-resistant varieties.