Comparative analysis of 326 chloroplast genomes in Chinese jujube (Ziziphus jujuba): Structural variations, horizontal gene transfer events, and evolutionary patterns impacting its domestication from wild jujube

Abstract

Jujube (Ziziphus jujuba Mill.), renowned for its nutritional value and health benefits, is believed to have originated in the middle and lower reaches of the Yellow River in China, where it underwent domestication from wild jujube. Nonetheless, the evolutionary trajectory and species differentiation between wild jujube and cultivated jujube still require further elucidation. The chloroplast genome (plastome), characterized by its relatively lower mutation rate compared to the nuclear genome, serves as an excellent model for evolutionary and comparative genomic research. In this study, we analyzed 326 nonredundant plastomes, encompassing 133 jujube cultivars and 193 wild jujube genotypes distributed throughout China. Noteworthy variations in the large single copy region primarily account for the size differences among these plastomes, impacting the evolution from wild jujube to cultivated varieties. Horizontal gene transfer (HGT) unveiled a unique chloroplast-to-nucleus transfer event, with transferred fragments predominantly influencing the evolution of the nuclear genome while leaving the plastome relatively unaffected. Population genetics analysis revealed two distinct evolutionary pathways from wild jujube to cultivated jujube: one driven by natural selection with minimal human interference, and the other resulting from human domestication and cultivation. Molecular dating, based on phylogenetic analysis, supported the likelihood that wild jujube and cultivated jujube fall within the same taxonomic category, Z. jujuba. In summary, our study comprehensively examined jujube plastome structures and HGT events, simultaneously contributing novel insights into the intricate processes that govern the evolution and domestication of jujube species.