Opposing regulatory functions of SmNAC22 and SmNAC58 underlie high light induced phenolic acid accumulation in Salvia miltiorrhiza

Salvia miltiorrhiza is a vital medicinal and industrial crop whose roots are rich in hydrophilic phenolic acids of rosmarinic acid and salvianolic acid B, key indicators of medicinal quality. NAC transcription factors greatly dominate plant secondary metabolism and stress responses, while their roles in phenolic acid biosynthesis following high light exposure in S. miltiorrhiza remain unclear. In this study, S. miltiorrhiza seedlings were subjected to high light treatment (1100 μmol·m⁻²·s⁻¹), and transcriptome analyses were conducted using leaf samples collected at different time points. RA content was significantly increased after 48 h of treatment, reaching 2.18-fold of that at 0 h. Based on differential expression analysis and homology alignment, two NAC transcription factors, SmNAC22 and SmNAC58, were identified as potential regulators of phenolic acid biosynthesis. Yeast one-hybrid and dual-luciferase reporter assays demonstrated that both SmNAC22 and SmNAC58 specifically bind to the CATGTG cis-element in the promoter of SmTAT2, a key gene involved in phenolic acid biosynthesis. Functional analyses revealed that SmNAC22 acts as a transcriptional activator, promoting SmTAT2 expression and RA and SalB accumulation in transgenic hairy roots, whereas SmNAC58 functions as a transcriptional repressor, inhibiting SmTAT2 expression and phenolic acid biosynthesis. Based on these findings, a “yin–yang” regulatory model is proposed, in which SmNAC22 and SmNAC58 oppositely regulate phenolic acid biosynthesis to fine-tune metabolite accumulation under high light conditions. This study provides potential genetic targets for phenolic acid metabolic engineering and a theoretical basis for improving S. miltiorrhiza quality through light-regulated cultivation strategies.