Comprehensive analyses of the metabolome and transcriptome reveal the photosynthetic effects in Arabidopsis thaliana of SaPEPC1 gene from desert plant with single-cell C4 photosynthetic pathway

The enzyme phosphoenolpyruvate carboxylase (PEPC) plays an important role in the photosynthetic metabolism of higher plants. Although the photosynthetic pathway involving PEPC has been clarified, further investigation is required to elucidate the effects of different light intensity treatments on plant photosynthetic and metabolism of PEPC. In this study, wild-type (WT) Arabidopsis was used as a control to investigate the effect of SaPEPC1 overexpression on the photosynthesis and metabolism of Arabidopsis. The results showed that intense light promoted and weak light inhibited the growth of Arabidopsis. Under different light intensity treatments, overexpression of SaPEPC1 led to increases in the photosynthetic rate (Pn) and photosynthetic enzyme activity (PEPC, Rubisco, PPDK, NADP-ME), a decrease in the intercellular CO₂ concentration (Ci), and increases in sucrose accumulation, leaf length, leaf width, and shoot fresh weight. Transcriptomic data analysis revealed that the starch, sucrose, and glutathione metabolic pathways were significantly enriched in transgenic Arabidopsis under intense light. This was accompanied by the up-regulation of multiple differentially expressed genes related to starch and sucrose metabolism, including AtBAM5, AtSUS6, and AtTPS5; the expression of most genes related to glutathione metabolism was down-regulated. A targeted metabolomic data analysis of transgenic Arabidopsis yielded 56 metabolites, the majority of which were found to participate in the tricarboxylic acid (TCA) cycle, followed by glycolysis. The content of L-aspartate, fumaric acid, malic acid, oxaloacetate, citric acid, and succinic acid was higher in transgenic lines than in WT under intense light. In conclusion, the overexpression of SaPEPC1 in Arabidopsis resulted in an increase in the photosynthetic rate and promoted the TCA cycle, and these changes were more pronounced under intense light treatment.