Multiomics analyses of Reynoutria japonica unveil genomic landscape and biosynthesis of emodin anthraquinone in Polygonaceae

Reynoutria japonica Houtt. (Polygonaceae), a medicinal plant valued for its anthraquinones, stilbenes, and flavonoids, is mainly cultivated for the extraction of resveratrol and emodin. However, the genome evolution and molecular mechanisms involved in the biosynthesis of emodin anthraquinone backbone remain elusive. Here, we present a comprehensive diploid genome assembly of 2.23 Gb, mapping 67144 protein-coding genes across 22 chromosomes using PacBio sequencing and Hi-C technology. Comparative genome analysis revealed a close genetic relationship with Rheum palmatum and R. hastatulus, and a shared dicotyledon γ-WGD event and a specific WGD event occurred 19 million years ago. Integrated analysis of transcriptomics, metabolomics and mass spectrometry imaging revealed 49 unique compounds, mainly including stilbenes, flavonoids and anthraquinones, and their significant accumulation trend in the root cortex. Three polyketone synthases (CHS1, CHS2, and PKS1) genes were characterized for the production of phloretin, emodin, and polydatin by heteroexpression and transgenic hairy roots of R. japonica, indicating their multifunctional roles in the biosynthesis of anthraquinone, stilbene and flavonoid. This study not only affords new viewpoints into genome evolution of Polygonaceae and anthraquinone biosynthesis, but also pave the way for functional genomic studies and genetic breeding of high resveratrol producing lines in R. japonica.