Integrated evolutionary pattern analyses reveal multiple origins of steroidal saponins in plants

Steroidal saponins are a class of specialized metabolites essential for plant's response to biotic and abiotic stresses. They are also important raw materials for the industrial production of steroid drugs. Steroidal saponins are present in some monocots, such as Dioscorea and Paris, but their distribution, origin, and evolution in plants remain poorly understood. By reconstructing the evolutionary history of the steroidal saponin-associated module (SSAM) in plants, we reveal that the steroidal saponin pathway has its origin in Asparagus and Dioscorea. Through evaluating the distribution and evolutionary pattern of steroidal saponins in angiosperms, we further show that steroidal saponins originated multiple times in angiosperms, and exist in early diverged lineages of certain monocot lineages including Asparagales, Dioscoreales, and Liliales. In these lineages, steroidal saponins are synthesized through the high copy and/or high expression mechanisms of key genes in SSAM. Together with shifts in gene evolutionary rates and amino acid usage, these molecular mechanisms shape the current distribution and diversity of steroidal saponins in plants. Consequently, our results provide new insights into the distribution, diversity and evolutionary history of steroidal saponins in plants, and enhance our understanding of plants' resistance to abiotic and biotic stresses. Additionally, fundamental understanding of the steroidal saponin biosynthesis will facilitate their industrial production and pharmacological applications.

Automated summary

Steroidal saponins are specialized metabolites essential for plants' response to stresses and for industrial production of steroid drugs. The origin and evolution of steroidal saponins in plants remain poorly understood. By studying the evolutionary history of steroidal saponin-associated module in plants, this study reveals their origin in Asparagus and Dioscorea and multiple origins in angiosperms. Understanding the distribution and diversity of steroidal saponins contributes to our knowledge of plant resistance to stresses and helps facilitate their industrial production and pharmacological applications.