Integrative physiological, transcriptome, and metabolome analysis uncovers the drought responses of two Zanthoxylum bungeanum cultivars

Zanthoxylum bungeanum (ZB) is a medicinal plant that is widely cultivated in arid and semi-arid areas. The drought tolerance mechanism of ZB has not yet been clearly elucidated. Here, the physiological indicators, transcriptome, and metabolome of two ZB cultivars with contrasting drought tolerance (FJ, Z. bungeanum cv. ‘Fengjiao’; HJ, Z. bungeanum cv. ‘Hanjiao’) were analyzed under drought stress. The results showed that HJ was more tolerant to drought stress, with stronger antioxidant enzyme activities, higher contents of soluble sugar, soluble protein and proline as well as lower content of malondialdehyde and H2O2. Transcriptome analysis revealed that there were more differentially expressed genes in FJ than in HJ throughout the drought treatment. Metabolome analysis identified 911 metabolites, which were divided into 10 classes. The up-regulated metabolites in HJ were mainly amino acids and their derivatives and flavonoids; those in FJ were mainly amino acids and their derivatives and alkaloids. Candidate structural genes related to drought tolerance and key transcription factor genes involved in drought-response pathways were sheltered by weighted gene co-expression network analysis (WGCNA). Conjoint analysis of the transcriptome and metabolome emphasized the importance of respiration metabolism in enhancing drought tolerance. In general, HJ improves drought tolerance by enhancing antioxidant enzyme activities; increasing the intensity of the pentose phosphate pathway; promoting the accumulation of osmotic substances; stimulating the synthesis of abscisic acid, brassinosteroid, and heat shock proteins; and accelerating signal transduction. The results improve our understanding of the molecular mechanism of drought tolerance in ZB and provide new insights for molecular breeding of ZB as well as other crops.