Transcriptomic and Non-Targeted Metabolomic Analyses Reveal Changes in Metabolic Networks during Leaf Coloration in Cyclocarya paliurus (Batalin) Iljinsk

Abstract

Secondary metabolites in Cyclocarya paliurus (Batalin) Iljinsk. leaves are beneficial for human health. The synthesis and accumulation of secondary metabolites form a complex process that is influenced by the trade-off between primary and secondary metabolism and by the biosynthetic pathways themselves. In this study, we explored the relationship between secondary metabolite accumulation and the activity of metabolic networks in leaves of C. paliurus. Leaves at three different growth stages were subjected to transcriptomic and non-targeted metabolomic analyses. The results revealed that nitrogen assimilation increased and carbon assimilation decreased as leaves matured, and the patterns of secondary metabolite accumulation and gene expression differed among the leaves at different growth stages. Mature green leaves had higher nitrogen assimilation and lower carbon assimilation, which were correlated with variations in secondary metabolite accumulation. As a major source of carbon and nitrogen, glutamine accumulated in the mature green leaves of C. paliurus. The accumulation of glutamine inhibited phenylalanine biosynthesis by modulating the pentose phosphate pathway but promoted acetyl-CoA biosynthesis through the tricarboxylic acid cycle. These changes led to decreased flavonoid contents and increased triterpenoid contents in mature leaves. These metabolomic and transcriptomic data reveal the differential expression of metabolic regulatory networks during three stages of leaf development and highlight the trade-off between primary and secondary metabolism. Our results provide a comprehensive picture of the metabolic pathways that are active in the leaves of C. paliurus at different growth stages.