Integration of the D-Genome Reshapes Gene Transcription, Chromatin Architecture, and Metabolome of Allohexaploid Wheat, Leading to Enhanced Environmental Adaptability.

The hybridization-led integration of the D-genome into domesticated tetraploid wheat gave rise to allohexaploid wheat, the most cultivated wheat globally grown across diverse environmental conditions. However, the regulatory mechanisms by which this genomic integration confers increased environmental adaptability in allohexaploid remains largely unexplored. Here, we investigated the change of transcriptome, chromatin interactome and metabolome in three independent polyploidization events. Our findings reveal that polyploidization triggers the activation of defense-related genes through a comprehensive reorganization of the epigenome and 3D chromatin architecture. Furthermore, polyploidization significantly enriches secondary metabolites-specifically alkaloids and flavonoids-which are pivotal for environmental adaptation. We further found that B-subgenome genes TaRLK-1B and TaRLK-3B are activated via de novo chromatin interactions to enhance alkali stress tolerance, whereas TaGT-2D boosts UV-B resistance through the accumulation of glycosylated flavonoids. These results shed light on the mechanistic basis of enhanced adaptability in hexaploid wheat, especially to salt, alkali, and UV-B stress, and highlight the indispensable contribution of the D-genome to the evolutionary success of the allohexaploid lineage.