Haplotype-resolved autotetraploid genome of Dioscorea nipponica provides insights into recent polyploidization, metabolic rewiring, and environmental adaptation.

Whole-genome duplication (WGD, or polyploidization) is a major evolutionary force in plants, yet the genomic, transcriptional, and metabolic consequences of autopolyploidy remain less understood than those of allopolyploidy. Dioscorea nipponica, a medicinal species producing diosgenin-type steroidal saponins, harbors both diploid and autopolyploid populations, providing a unique system to investigate these processes. Here, we present a haplotype-resolved, chromosome-scale genome assembly of autotetraploid D. nipponica (2n = 4x = 40). Comparative and population genomic analyses indicate a single, recent autotetraploid origin (<1.63 Ma), after the divergence of its diploid ancestors (~2.5-2.9 Ma), coinciding with Pliocene-Pleistocene climatic shifts that may have promoted population isolation and genome duplication. The four haplotypes exhibit high average nucleotide identity, extensive synteny and similar global gene expression, with pervasive allele loss (~32% of genes) and widespread allelic transcriptional suppression (~60% of expressed tetrads), together buffering dosage effects. Metabolomic profiling reveals a metabolic trade-off in rhizomes, with autotetraploids accumulating higher flavonoids but lower diosgenin-type steroidal saponins than diploids, potentially enhancing reproductive fitness and adaptation to marginal environments. This shift is supported by expanded flavonoid gene families (e.g., PAL, CHS), some exhibiting positive dosage effects, whereas diosgenin pathway genes (e.g., CYP90, CYP94) remain copy number stable and mostly show negative dosage effects in autotetraploids. Selective sweep analysis further identified genes linked to genome stability (e.g., AtTOP3α, AtDMC1) and abiotic stress response, crucial for polyploid establishment. Overall, these findings offer novel insights into how autopolyploidy shapes gene expression, metabolic evolution, and ecological adaptation, with implications for the conservation and utilization of this medicinally important species.