Transcriptome of HY5 transgenic Salvia miltiorrhiza root

Light is a crucial environmental factor influencing secondary metabolism in aerial plant tissues such as leaves, flowers, and fruits. However, whether and how light regulates the biosynthesis of secondary metabolites in plant roots remains poorly understood. Salvia miltiorrhiza is a widely used medicinal plant in many East Asian countries. The contents of tanshinones (tetracyclic diterpenoid quinones) and phenolic acids in its roots critically determine the pharmacological quality of this herb. In this study, we identified a light-responsive regulatory module comprising transcription factors SmPIF3, SmHY5, and SmBBX22 that coordinately governs the biosynthesis of both tanshinones and phenolic acids in S. miltiorrhiza. Light induces the transcription of these three key regulatory genes in roots of S. miltiorrhiza. The accumulated SmPIF3 activates SmHY5 transcription through specific binding to the E-box element in its promoter. SmHY5 directly binds to the promoter regions of two biosynthetic genes, SmKSL1 (tanshinones) and SmPAL1 (phenolic acids), concurrently enhancing the production of these secondary metabolites. In addition, SmHY5 physically interacts with SmBBX22 to form a functional heterodimer that amplifies the transcriptional activation capacity of SmHY5 on its target biosynthetic genes. This work not only establishes a comprehensive framework for understanding light-regulated secondary metabolism in medicinal plant roots but also elucidates a novel molecular paradigm wherein light coordinates the biosynthesis of structurally distinct secondary metabolites through interconnected transcription factor networks.