Determining the genetic basis of ginsenosides variation during ginseng domestication by evolutionary transcriptomics

Abstract

Ginsenosides, the primary medicinally active substances in ginseng, are consistently used to treat a variety of diseases. Cultivated ginseng was domesticated from wild ginseng, for which the mode of domestication and the changes in the content of ginsenosides and their regulatory mechanisms during the domestication process were unclear. Here, transcriptome sequencing and metabolomic analysis were used to compare wild and cultivated ginsengs to gain insight into the genetic and ginsenosides content changes associated with domestication. Genetic structure analysis revealed that ginseng might have undergone independent domestication in China and Korea, respectively. A slightly reduced genetic diversity occurred in wild and cultivated ginsengs and ginseng was domesticated about 2000 years ago in China. 330 genes were identified as signatures of selective sweeps that occurred during ginseng domestication, including bZIP051, GARP222, HMGCS058, and UGTs225. The content of ginsenosides in leaves of cultivated ginseng was higher than leaves of wild ginseng, while substantial monomers content in wild ginseng was significantly higher than that in cultivated ginseng. The content of ginsenosides was higher in leaves than in roots and stems of both wild and cultivated ginsengs. Module-trait association analysis suggested abundant TFs, including MYB, AP2/ERF, NAC, and bZIP, were highly associated with expression level of ginsenosides synthetic genes and monomer content. The occurrence of alternative splicing events in genes was significantly reduced during ginseng domestication, with ginsenosides synthesis genes being particularly susceptible to alternative splicing. The variation of ginsenosides content was independently regulated by alternative splicing and transcription factors between cultivated and wild ginsengs. This study provided valuable genetic sources of ginsenosides that could contribute to ginseng breeding.