SmNAC36 promotes the biosynthesis of bioactive compounds and drought tolerance in Salvia miltiorrhiza.

Abstract

Although drought stress typically suppresses plant growth and reduces crop yields, it paradoxically enhances the accumulation of bioactive compounds in the medicinal plant Salvia miltiorrhiza, such as salvianolic acids and tanshinones. However, the regulatory mechanisms behind this phenomenon remain poorly understood. In this study, an NAC transcription factor (TF), SmNAC36, has been identified as a pivotal regulator of bioactive compound biosynthesis and drought response in S. miltiorrhiza. Overexpression of SmNAC36 enhances the accumulation of tanshinones and salvianolic acids, and drought resistance. Conversely, knockout of SmNAC36 attenuated drought tolerance and markedly decreased bioactive compound content. Further mechanistic studies revealed that SmNAC36 directly binds to the promoters of SmPAL and Sm4CL in the salvianolic acids pathway, and to the promoter of SmDXS in the tanshinones biosynthesis pathway, thereby activating key enzymes that promote the accumulation of lignin as well as bioactive compounds. Moreover, SmNAC36 interacts with SmDREB1C, an AP2/ERF family TF that regulates drought tolerance. This interaction activates the expression of enzymes, such as superoxide dismutase and peroxidase, which are responsible for mitigating oxidative stress, thereby improving drought stress tolerance. Our results elucidate a dual-function mechanism whereby SmNAC36 integrates drought stress adaptation with bioactive compound biosynthesis, providing a potential metabolic engineering target for improving the quality and stress resilience of S. miltiorrhiza.