Multi-omics profiling reveals an auxin–salicylic acid signaling hub driving flavonoid depletion and accelerated vigor loss in tetraploid Chinese cabbage seeds

Background Seed vigor, encompassing rapid uniform germination and robust seedling establishment, is critical for crop yield. While induced tetraploidy confers desirable agronomic traits in Chinese cabbage ( Brassica rapa ssp. pekinensis ), tetraploid seeds exhibit accelerated viability loss during storage compared to diploid counterparts, imposing substantial economic constraints. The metabolic and regulatory mechanisms underlying this ploidy-associated vigor penalty remain elusive. Results TTC assay revealed that seed viability exhibited the most pronounced decline in the 17-year time gradient. Consequently, we prioritized omics analyses on the 19-year and 23-year seeds. Tetraploid seeds demonstrated markedly accelerated viability decline under identical storage conditions, with 2023-harvested tetraploid lots exhibiting the most extensive metabolic rewiring. Comparative transcriptomics revealed ploidy- and year-specific segregation of genes involved in hormone signaling and carbohydrate metabolism. Notably, tetraploid seeds activated a unique auxin--salicylic acid (SA) signaling axis characterized by upregulation of GH3.3 , NPR3 , TGA4 , and IAA family genes, concomitant with elevated indole-3-acetic acid (IAA) and abscisic acid (ABA) accumulation. Genome-wide transcription factor analysis identified ploidy-specific expression patterns in bHLH, WRKY, and bZIP families, with bHLH genes predominantly enriched in tetraploids and bZIP factors associated with diploid seeds. Metabolomic profiling highlighted energy pathway imbalance, specifically starch/sucrose metabolism and glycerophospholipid dysregulation, as the earliest metabolic predictors of vigor loss in tetraploids. Conclusion Our findings redefine ploidy-associated seed vigor deterioration as a predictable, metabolically driven syndrome orchestrated by hormone signaling crosstalk and secondary metabolite depletion. The identified auxin--SA signaling axis and energy-metabolism markers provide molecular targets for marker-assisted breeding of high-vigor tetraploid cultivars.