On the evolution and genetic diversity of bread wheat D genome

Bread wheat (Triticum aestivum) became a globally dominant crop after incorporating the D genome from donor species Aegilops tauschii, while the evolutionary history shaping the D genome during this process remains elusive. Here, we proposed a renewed evolutionary model linking Ae. tauschii and hexaploid wheat D genome, by constructing an ancestral haplotype map covering 762 Ae. tauschii and hexaploid wheat accessions. We dissected the evolutionary trajectories of Ae. tauschii lineages and reported a few independent intermediate accessions, demonstrating the low-frequent inter-sublineage geneflow enriched the diversity of Ae. tauschii. We discovered that the D genome of hexaploid wheat inherited from a unified ancestral template, but with a mosaic composition that was highly mixed mainly by three Ae. tauschii L2 sublineages located in the Caspian coastal region, suggesting the early agricultural activities facilitated the innovation of D genome compositions and finalized the success of hexaploidization. We further found that the majority (51.4%) of genetic diversity was attributed to novel mutations absent in Ae. tauschii, and also identified large Ae. tauschii introgressions from various lineages, expanding the diversity of wheat D genome and introducing beneficial alleles. This work sheds light on the wheat hexaploidization process and highlights the evolutionary significance of the multi-layered genetic diversity of the bread wheat D genome.