The Evolution and Origin of Allotetraploid Aegilops geniculata Revealed by the Homoeolog-Resolved Genome Assembly

Aegilops geniculata Roth is a tetraploid (M^gM^gU^gU^g; 2n = 4x = 28) wild relative of wheat and a valuable source of genetic diversity for improving agronomic traits. We present a high-quality homoeolog-resolved assembly and annotation of the Ae. geniculata genome and use it to study the function, origin and evolution of the M^g and U^g genomes. Comparative genomics revealed that the U^g genome has undergone extensive structural rearrangements (SRAs), which were inherited from its diploid ancestor. Chromosomes 4U^g experienced the most extensive SRAs, including translocations from chromosomes 1, 2, 6 and 7, as well as a pericentric inversion that repositioned the centromere closer to the chromosome terminus. The M^g genome had two large-scale translocations, which likely occurred after polyploidization or in its immediate diploid ancestor. These SRAs resulted in the redistribution of genes among the homoeologous chromosomes, especially affecting the disease resistance genes. Although SRAs altered the expression and H3K4me3 marks of homoeologous genes relative to non-rearranged regions, the overall balance of homoeolog expression and active chromatin remained stable, suggesting selective pressure to maintain gene dosage balance. Population genomic analyses of Ae. geniculata and its diploid ancestors, Ae. comosa (MM) and Ae. umbellulata (UU), suggest that Ae. geniculata originated in Western Anatolia. The genomic resources developed in this study will accelerate trait discovery, gene mapping and the transfer of beneficial alleles from this wild relative into wheat.