On the evolution and genetic diversity of the bread wheat D genome

Abstract

Bread wheat (Triticum aestivum) became a globally dominant crop after incorporating the D genome from the donor species Aegilops tauschii, but the evolutionary history that shaped the D genome during this process remains to be clarified. Here, we propose a renewed evolutionary model linking Ae. tauschii and the 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 that low-frequency inter-sublineage gene flow had enriched the diversity of Ae. tauschii. We discovered that the D genome of hexaploid wheat was inherited from a unified ancestral template, but with a mosaic composition that was highly mixed and derived mainly from three Ae. tauschii L2 sublineages located in the Caspian coastal region. This result suggests that early agricultural activities facilitated innovations in D-genome composition and finalized the success of hexaploidization. We found that the majority (51.4%) of genetic diversity was attributed to novel mutations absent in Ae. tauschii, and we identified large Ae. tauschii introgressions from various lineages, which expanded the diversity of the wheat D genome and introduced beneficial alleles. This work sheds light on the process of wheat hexaploidization and highlights the evolutionary significance of the multi-layered genetic diversity of the bread wheat D genome.