Multi-omics analysis provides insights into genetic architecture of flavonoid metabolites in Populus

Flavonoids are widely distributed secondary metabolites as well as a major class of chemical defenses in response to light intensity, temperature, and other external factors. However, systematic investigation on the genetic basis of flavonoids in perennial trees is poorly documented. In this study, we married metabolite-based genome wide association analysis (mGWAS), expression quantitative trait loci (eQTL) mapping and weighted co-expression network analysis (WGCNA) analysis to systematically construct the regulatory network underlying flavonoids decoration in Populus. We firstly characterized 172 flavonoids features in 300 natural accessions of Populus tomentosa collected in three widespread geographical regions. Then, we conducted systematical genetic strategy to identify casual candidate genes, and constructed the regulatory network of flavonoids biosynthesis of Populus. Selection signature revealed 83 metabolites exhibited significant divergence among three geographical regions of Populus, we thus determined candidate genes contributing to flavonoids divergence based on the selection sweep analysis. Furthermore, we focused on PtoLDOX, a key gene responsible for the levels of anthocyanin and dihydrokaempferol, and dissected it through allelic frequency and haplotype analysis. Collectively, our study provides new insights into the genetic basis of flavonoids biosynthesis, and sheds light on the adaptive selection to different geographical regions that potentially dominated by the flavonoids of Populus, facilitating marker-based breeding in poplar varieties.