Domestication Has Reshaped Gene Families, Gene Expressions and Flavonoid Metabolites in Green Jujube (Ziziphus mauritiana Lam.) Fruit

Domestication has been proven to significantly impact the biosynthesis of plant secondary metabolites. Cultivated green jujube (Ziziphus mauritiana Lam.), as an important autotetraploid fruit crop widely planted in tropical regions, exhibits differential physicochemical traits compared with its wild progenitor. To assess the traits lost in cultivated green jujube during domestication, the study performed comprehensive genomic, transcriptomic and metabolomic investigations of flavonoid pathways in wild and cultivated green jujube. Based on the four haplotype genomes of wild and cultivated green jujube, for the first time, the study bulk-identified 16 key gene families associated with flavonoid biosynthesis. Collinearity analysis revealed that tandem duplication was the predominant event in flavonoid-related genes rather than WGD. Through the expression profiles in different tissues, the distinct member of these gene families was classified as “redundant” or “functional”. Transcriptomic analyses illustrated the significant differential expressions (p < 0.05) of 13 flavonoid-related gene families in fruits of six cultivated and three wild green jujube accessions, except for FLS, LAR and PPO. The wild green jujube fruits accumulated more abundance of flavonoid metabolites than in cultivated fruits (p < 0.0001), as evidenced by upregulated chalcones, dihydroflavonol, isoflavones and flavonoid carbonoside. Gene–metabolite co-expression modules further validated the potential transcription regulators, such as BBX21, WRI1 and bZIP44. Together, the study suggested a genomic, transcriptomic and metabolic perspective for domestication regarding fruit flavonoid pathways in green jujube, which provides a valuable genetic resource for fruit quality improvement in cultivated green jujube.