Genomic and population analyses reveal asymmetric subgenome evolution and local adaptation in the polyploid Lycopus lucidus

Polyploidization and subsequent diploidization are fundamental processes in plant evolution, yet how subgenome asymmetry arising from these events shapes ecological adaptation remains poorly understood. We generate a chromosome‑level genome assembly and population genomic data for Lycopus lucidus, a polyploid medicinal plant with broad environmental adaptability across China. The genome reveals a recent whole‑genome triplication event. The three subgenomes show marked asymmetry in transposable element accumulation, gene retention, and evolutionary rates. Subgenome B has been stabilized under strong purifying selection, whereas subgenomes A and C have undergone dynamic reorganization with accelerated gene turnover, pseudogenization, and asymmetric selection pressures. Population genomic analysis of 60 individuals identifies four genetic lineages corresponding to geographic regions, with a demographic bottleneck coinciding with late Holocene cooling. Among genes under selection between lineages, 93.8% originate from subgenome C, suggesting this subgenome serves as a reservoir for adaptive variation. Genotype-environment association analyses identify 9,496 adaptive SNPs enriched in stress response, secondary metabolism, and wax biosynthesis pathways, with precipitation as the primary driver of local adaptation. Our findings demonstrate that subgenome asymmetry established during polyploid diploidization provides the genetic substrate for subsequent environmental adaptation, establishing L. lucidus as a model for understanding polyploid genome evolution and its adaptive consequences.