The underlying mechanisms by which boron mitigates copper toxicity in Citrus sinensis leaves revealed by integrated analysis of transcriptome, metabolome and physiology

• Published in: Tree physiology 2024-09, Vol.44 (9)
• Main Authors: Chen, Xu-Feng, Wu, Bi-Sha, Yang, Hui, Shen, Qian, Lu, Fei, Huang, Wei-Lin, Guo, Jiuxin, Ye, Xin, Yang, Lin-Tong, Chen, Li-Song
• Format: Article
• Language: English
• Subjects: Boron - metabolism; Boron - pharmacology; Boron - toxicity; Citrus sinensis - drug effects; Citrus sinensis - genetics; Citrus sinensis - growth & development; Citrus sinensis - metabolism; Citrus sinensis - physiology; Copper - metabolism; Copper - toxicity; Gene Expression Regulation, Plant - drug effects; Metabolome - drug effects; Plant Leaves - drug effects; Plant Leaves - metabolism; Transcriptome
• ISSN: 1758-4469; 1758-4469
• DOI: 10.1093/treephys/tpae099

Abstract Both copper (Cu) excess and boron (B) deficiency are often observed in some citrus orchard soils. The molecular mechanisms by which B alleviates excessive Cu in citrus are poorly understood. Seedlings of sweet orange (Citrus sinensis (L.) Osbeck cv. Xuegan) were treated with 0.5 (Cu0.5) or 350 (Cu350 or Cu excess) μM CuCl2 and 2.5 (B2.5) or 25 (B25) μM HBO3 for 24 wk. Thereafter, this study examined the effects of Cu and B treatments on gene expression levels revealed by RNA-Seq, metabolite profiles revealed by a widely targeted metabolome, and related physiological parameters in leaves. Cu350 upregulated 564 genes and 170 metabolites, and downregulated 598 genes and 58 metabolites in leaves of 2.5 μM B-treated seedlings (LB2.5), but it only upregulated 281 genes and 100 metabolites, and downregulated 136 genes and 40 metabolites in leaves of 25 μM B-treated seedlings (LB25). Cu350 decreased the concentrations of sucrose and total soluble sugars and increased the concentrations of starch, glucose, fructose and total nonstructural carbohydrates in LB2.5, but it only increased the glucose concentration in LB25. Further analysis demonstrated that B addition reduced the oxidative damage and alterations in primary and secondary metabolisms caused by Cu350, and alleviated the impairment of Cu350 to photosynthesis and cell wall metabolism, thus improving leaf growth. LB2.5 exhibited some adaptive responses to Cu350 to meet the increasing need for the dissipation of excessive excitation energy (EEE) and the detoxification of reactive oxygen species (reactive aldehydes) and Cu. Cu350 increased photorespiration, xanthophyll cycle-dependent thermal dissipation, nonstructural carbohydrate accumulation, and secondary metabolite biosynthesis and abundances; and upregulated tryptophan metabolism and related metabolite abundances, some antioxidant-related gene expression, and some antioxidant abundances. Additionally, this study identified some metabolic pathways, metabolites and genes that might lead to Cu tolerance in leaves.