Whole-genome resequencing reveals population structure and local adaptation in wild Forsythia suspensa

Forsythia suspensa is a traditional medicinal plant endemic to China that possesses immense economic value. However, the breeding of elite varieties remains severely hindered by a lack of genomic understanding regarding its wild populations. This study aims to elucidate the evolutionary dynamics, genetic differentiation, and local adaptation mechanisms of wild F. suspensa populations. We performed whole-genome resequencing on 149 individuals sampled from 30 wild populations across the core distribution range of the species. Phylogenetic and population-structure analyses identified four major genetic lineages, among which the Shandong (SD) lineage exhibited pronounced genetic differentiation from the other lineages. Demographic modeling revealed a long-term population contraction driven by Pleistocene climatic oscillations, which was followed by a transient rebound in the SD lineage that preserved critical ancestral variation. Furthermore, partial Mantel tests demonstrated that isolation by distance (IBD) primarily drove population differentiation, facilitating the formation of regional ecotypes. Notably, a selective-sweep analysis of the highly differentiated SD lineage identified 315 candidate regions under selection that are significantly enriched in plant-pathogen interactions and the phenylpropanoid biosynthesis pathway. This finding suggests that natural biotic stress acts as a key driver for the differential accumulation of medicinal components. These findings provide genome-wide insights into the evolutionary history of F. suspensa and highlight the highly differentiated SD lineage as a potentially valuable genetic resource. We recommend systematic grid-based germplasm collection and the development of specific molecular markers for marker-assisted selection to accelerate the breeding of high-yielding and disease-resistant elite varieties.