Integrated Transcriptomics and Metabolomics to Reveal the Regulatory Mechanisms of Flavonoid Biosynthesis in Persicaria capitata Under Different Nitrogen Fertilization Levels

Abstract

Background: Persicaria capitata is a perennial herb and one of the top ten authentic Miao medicinal plants in Guizhou province, China, with flavonoids serving as its primary bioactive components. Agricultural production practices have shown that nitrogen fertilizer application can reduce flavonoid accumulation in P. capitata, although the underlying molecular regulatory mechanism remains unclear. Methods: In this study, a pot experiment was performed to investigate the effects of different nitrogen treatments on the growth performance and yield of P. capitata. Moreover, the related changes in transcriptomic characteristics and metabolic profiles were also systematically analyzed. Results: Nitrogen fertilization significantly promoted stem elongation, branch number, and yield formation. The maximum stem length, branch number, and single-plant yield were recorded in the 0.3 g N/kg treatment group as reaching 80.74 cm, 37.30, and 123.64 g/plant, respectively. Transcriptomic screening yielded 10,880 differentially expressed genes (DEGs), and the number of downregulated DEGs was consistently higher than upregulated DEGs across all comparison groups. Metabolomic analysis identified a total of 3356 differentially accumulated metabolites, including 168 differential flavonoid metabolites. With the increase in nitrogen application rate, most flavonoid compounds, such as chlorogenic acid, 5-hydroxyferulic acid, and 4-hydroxycinnamic acid, exhibited a significantly downregulated accumulation pattern. An integrated transcriptomic and metabolomic analysis revealed that the differential flavonoid metabolites and functional genes were predominantly enriched in the phenylpropanoid biosynthesis, flavonoid biosynthesis, and flavone and flavonol metabolism pathways. The decreased expression of key structural genes, including PAL, 4CL, CHS, FLS, F3H, and F3′H, inhibited the biosynthesis and accumulation of core flavonoid components (e.g., chlorogenic acid, naringenin, and luteolin), thereby deteriorating the medicinal quality of P. capitata. Conclusions: Nitrogen supplementation increases the yield of P. capitata but inhibits flavonoid biosynthesis. Downregulated expression of key genes in flavonoid metabolism is responsible for the decreased flavonoid content. This study provides theoretical support for optimized nitrogen management to coordinate yield formation and quality improvement in planting practices for P. capitata.