Phylogenomics provides comprehensive insights into the evolutionary relationships among cultivated buckwheat species

Abstract

Buckwheat belongs to the family Polygonaceae and genus Fagopyrum, which is characterized by high flavonoid content, short growth period, and strong environmental adaptability. Buckwheat has three cultivated species, including the annual food crops common buckwheat (Fagopyrum esculentum) and Tartary buckwheat (Fagopyrum tataricum), and the perennial traditional herbal medicine golden buckwheat (Fagopyrum cymosum). However, the unclear phylogenetic relationships among these three species based on genomic data limit buckwheat interspecific hybridization and genetic improvement. Despite their enormous differences in morphology and genome, we confirm the closet relationship between Fagopyrum cymosum and Fagopyrum tataricum, but not Fagopyrum esculentum. The results are also verified through collecting and sequencing an extensive sampling of cultivated/wild populations across all environmentally distinct regions in which these species are found. The changes in flowering time and style morphology controlled by the AP1 and S-ELF3 loci significantly contribute to the buckwheat speciation. The introgression from Fagopyrum cymosum into wild Fagopyrum tataricum explains why wild Fagopyrum tataricum exhibits seed morphology similar to Fagopyrum cymosum. Furthermore, the convergent traits of leaf morphology and higher flavonoid content between Fagopyrum cymosum and wild Fagopyrum esculentum are linked to high-altitude adaptation. Fagopyrum cymosum is more closely related to wild Fagopyrum tataricum, a fact that is confirmed by interspecific hybridization. Our work provides a valuable example of how phylogenomics can be efficiently utilized for phylogenetic relationship analysis between crops and their wild species relatives, as well as elucidating the plant speciation from the perspectives of genomic evolution and adaptive mechanisms.