A Model for Core Responses and Species-Specific Reprogramming to Whole-Genome Duplication in Plants

Whole-genome duplication (WGD) is a fundamental evolutionary force in plants, driving diversification and offering immense potential for crop improvement. While WGD’s molecular effects are well-studied in individual species, the consistency of these responses across diverse lineages remains largely unknown. Here, we integrated multi-omics datasets from established WGD events across 20 plant species, encompassing both experimentally induced and naturally occurring polyploids, to elucidate shared molecular adaptations to genome doubling. Our analysis identified 68 orthologous core WGD-responsive genes, predominantly involved in stress response, hormone signaling, and cellular homeostasis. Interestingly, despite considerable divergence in individual metabolites across species, their enriched pathways consistently converged on osmotic adjustment, redox regulation, and membrane remodeling. This convergent cascade of core transcriptional regulation and metabolic outputs thus defines a foundational adaptive program across diverse species. However, concurrently, extensive transcriptional and metabolic reprogramming exhibited strong species specificity. Based on this duality, we propose a novel model of core responses and species-specific reprogramming to WGD. This model provides crucial insights into polyploid stabilization and trait diversity, by highlighting an endogenously activated stress-buffering state that is pivotal for WGD establishment. Moreover, the identified core genes offer promising molecular markers for targeted polyploid breeding strategies.