Tanshinones (TAs), well-known specialized diterpenoid metabolites in Salvia plants, exhibit distinct tissue-specific production in the root periderm. However, the mechanisms regulating this accumulation pattern remain unknown. Here, we employed a multi-omics analysis strategy to uncover the transcriptional regulatory network responsible for TA biosynthesis in Salvia miltiorrhiza roots. By integrating metabolic profiling, RNA-seq, and ATAC-seq, we profile the temporo-spatial dynamics of metabolic, transcriptional, and chromatin landscapes during early root development. Our results demonstrate that TAs biosynthesis and accumulation in S. miltiorrhiza roots display spatiotemporal patterns, marked by periderm-specific accumulation and initiation exclusively at specific developmental stages, tightly coordinated with dynamic changes in chromatin accessibility and transcriptional regulation. The constructed transcriptional regulatory network driving TA biosynthesis was found to be dominated by 211 key transcription factors (TFs). Experimental validations highlighted SmERF105 as a key positive regulator of TA, activating the transcription of KSL1, CYP76AH3, and the TA transporter ABCG1 to modulate the TA production. Our study uncovers novel, high-confidence regulators and offers an effective strategy for dissecting the genetic basis of plant specialized metabolites, offering value for advancing TA metabolic engineering.

Salvia miltiorrhiza  /  Tanshinones biosynthesis  /  Spatiotemporal metabolic  /  Transcriptional regulation network  /  Chromatin accessibility  /  Transcription factor  /  Transport  /  Gene cluster