The evolution, origin and function of the U and M genomes revealed by the genome assembly of allotetraploid Aegilops geniculata

Aegilops geniculata Roth is (MgMgUgUg; 2n = 4x = 28) is a tetraploid wild relative of wheat that has been used as a source of beneficial diversity for improving agronomic traits. Here, we developed a high-quality long-read genome assembly and annotation to characterize actively transcribed genes and investigate origin and evolution of Ae. geniculata. The comparative genome analysis showed that U and M genomes of Ae. geniculata underwent extensive structural rearrangements (SRA) mostly attributed to events occurred in the diploid ancestor of the U genome. Chromosomes 4U experienced most extensive re-rearrangements including translocations from chromosomes 1, 2, 6 and 7, and pericentric inversion on 4U that resulted in re-positioning of centromere closer to the chromosome terminus. The M genome experienced translocations from chromosome 6 to chromosome 4, and from chromosome 5 to chromosome 4, which likely occurred after polyploidization or in the direct ancestor of the M genome. SRAs led to re-distribution of genes among the homoeologous chromosomes, especially affecting the disease resistance genes. While SRAs changed the expression and chromatin states of homoeologous genes compared to non-rearranged regions, the relative ratios of homeolog expression and active chromatin remained similar between the homoeologs suggesting that selection acts to maintain dosage balance of duplicated gene products. The population genomic analyses of Ae. geniculata and the diploid ancestors of M (Ae. comosa) and U (Ae. umbellulata) genomes placed Ae. geniculata origin to the western regions of Anatolia. The developed genomic resources will inform further trait discovery, mapping and translation efforts using this wild relative to improve wheat.