Integrative physiological, transcriptomic and metabolomic analysis reveals how the roots of two ornamental Hydrangea macrophylla cultivars cope with lead (Pb) toxicity.

Lead (Pb) soil contamination has caused serious ecological and environmental issues. Hydrangea macrophylla is a potential Pb-contaminated soil remediation plant, however, their Pb stress defense mechanism is largely unknown. Here, the physiology, transcriptomic and metabolome of two H. macrophylla cultivars (ML, Pb-sensitive cultivar; JC, Pb-resistant cultivar) under Pb stress were investigated. The results demonstrated that JC performed superiorly, with activities of the antioxidant enzymes superoxide dismutase (SOD), peroxidase (POD), and catalase (CAT) were 1.25, 2.84, and 1.67 times higher than those of ML after Pb treatment, respectively, and the amount of soluble sugar in JC increased by 231.34 % compared with that in ML. The electrical conductivity (EC) value of the root exudates of JC was 43.71 % lower than that of ML under Pb stress. The non-targeted metabolomics analysis revealed 193 metabolites grouped into nine categories. Pb stress-induced differential expression of the 37 metabolites, among which the major metabolites up-regulated in ML were organic acids, while in JC, these were carbohydrates, fatty acids, organic acids and lipids. The transcriptomic analysis revealed that Pb exposure induced 1075 and 1314 differentially expressed genes (DEGs) in JC and ML, respectively. According to the functional annotation results, hub genes were primarily enriched in carbohydrate metabolism, root growth, and plant resistance to external stresses. A conjoint analysis of the two omics indicated that the cutin, suberine and wax biosynthesis pathway in JC played an essential role in Pb detoxification. These findings clarify the resistance mechanism of H. macrophylla to Pb stress and open up a new avenue for breeding H. macrophylla Pb-resistant cultivars.