Comparative genomics reveals the evolution of anthraquinone biosynthesis in Polygonaceae

Polygonaceae is a globally distributed angiosperm family rich in anthraquinones (AQs), which contribute to diverse medicinal properties and species-specific chemical defenses. Despite their ecological and pharmacological significance, the evolutionary dynamics and transcriptional regulation of AQ biosynthesis genes in Polygonaceae remain largely unexplored.

In this study, we combined comparative genomics and multi-omics analyses to investigate these processes. Phylogenomic reconstruction indicated that Polygonaceae diverged from its sister family approximately 66.26 million years ago. A total of 206 polyketide synthase (PKS) genes were identified, with lineage-specific tandem duplication driving substantial expansion. Polyketide biosynthetic gene clusters with dense PKS aggregation were detected in three species, primarily shaped by tandem duplication. By integrating gene expression and synteny analyses, candidate PKS genes likely involved in AQ biosynthesis were identified. Multi-level gene regulatory networks constructed from root transcriptomes of Fallopia multiflora across different growth years revealed hierarchical regulatory relationships and divergence among candidate PKS genes. Weighted gene co-expression network analysis further identified co-expression modules and transcription factors potentially associated with AQ biosynthesis, while machine learning approaches prioritized transcription factors regulating the glycosyltransferase involved in AQ modification.

These results reveal the evolutionary expansion, diversification, and functional specialization of PKS genes, as well as the hierarchical transcriptional regulation underlying AQ biosynthesis in Polygonaceae. The identified candidate genes and regulatory networks provide a valuable resource for metabolic engineering and molecular breeding strategies aimed at enhancing medicinal AQ production.