Integrated transcriptomic and metabolomics analysis reveals abscisic acid signal transduction and sugar metabolism pathways as defense responses to cold stress in Argyranthemum frutescens

Argyranthemum frutescens is an important ornamental plant, whose distribution and application is limited owing to its susceptibility to low temperatures. The molecular mechanisms underlying the response of A. frutescens to cold stress is unknown. We used physiology, transcriptome, and metabolome analyses to characterize responses of A. frutescens subjected to 12 h (Mu12) and 24 h (Mu24) of low-temperature treatment. The results showed enhanced superoxide dismutase (SOD) activity during low temperature treatment and an increase in soluble sugar content at 12 h followed by a sharp decrease. A large number of differentially expressed genes (DEGs) were detected in A. frutescens plants exposed to low temperature. The up-regulated DEGs related to flavonoid biosynthesis, circadian rhythm, phenylpropanoid biosynthesis, and phenylalanine metabolism were significantly enriched in 12 h and 24 h compared to control, while those related to photosynthesis-antenna protein and photosynthesis pathway were down-regulated. Increased expression of transcription factors (TFs), including MYB, AP2-EREBP, and NAC indicated their role in triggering cold-responsive genes in A. frutescens. In total, 205 differentially accumulated metabolites were enriched during the low-temperature treatment, including amino acids, carbohydrates, and organic acids. Levels of eleven common metabolites, including abscisic acid, were up -regulated following cold treatment. In addition, sucrose, trehalose, and maltose accumulated at 12 h, but their levels decreased at 24 h. Integrated metabolome and transcriptome analyses revealed that abscisic acid signal transduction showed a positive response under the low-temperature treatment and sugar metabolism as an early response to cold stress in A. frutescens. These results reveal the potential underlying mechanisms of the low -temperature response of A. frutescens, which would help improve the cold tolerance of A. frutescens and enable extended cultivation in temperate regions in the future.

Automated summary

This study investigated the response of Argyranthemum frutescens to cold stress and found that the activity of superoxide dismutase increased during low temperature treatment while the soluble sugar content initially increased and then sharply decreased. A large number of differentially expressed genes related to flavonoid biosynthesis, circadian rhythm, phenylpropanoid biosynthesis, and phenylalanine metabolism were up-regulated under low temperature conditions. The study also revealed a positive response of abscisic acid signal transduction and sugar metabolism as an early response to cold stress in A. frutescens.