Dissecting the population structure, diversity and genetic architecture of rust resistance in wild emmer wheat (Triticum turgidum subsp. dicoccoides)

Wild emmer wheat (Triticum turgidum subsp. dicoccoides, WEW) was one of the first crops domesticated in the Neolithic revolution that shifted humanity to agrarian societies. Understanding its population genomics has both evolutionary significance and direct relevance to wheat improvement. Leveraging whole-genome sequencing (WGS) data from 291 accessions (~ 9.5x coverage), we identified 3.4 million high-quality SNPs for population genomics, evolutionary analysis, and genome-wide association studies (GWAS) of seedling-stage resistance to five races each of the stem, leaf, and stripe rust pathogens. Phylogenetic, principal component, and population structure analyses revealed three distinct WEW subgroups: the Northern Population (NP), Southern Levant (SL), and a highly differentiated judaicum subgroup consisting of accessions near the Sea of Galilee. Diversity and pairwise FST analyses highlighted varying divergence among these subpopulations. The SL accessions exhibited higher resistance to all races of the three rust pathogens compared to the judaicum and NP. The SL accessions also exhibited the highest frequency of resistance to all rust pathogens, whereas NP lacked stem rust resistance but retained resistance to some leaf and stripe rust races. GWAS identified 27, 26, and 41 significant loci associated with stem, leaf, and stripe rust resistance, respectively, most of which were novel. A major resistance hotspot was identified on chromosome 1BS (~ 50–100 Mb), associated with multiple races of different rust pathogens, suggesting the presence of shared or tightly linked resistance factors in the region. The most significant loci explained up to 73% of the phenotypic variation, with some conferring race-specific and others multi-race resistance. Notably, several accessions exhibited broad-spectrum resistance, including lines resistant to all stripe rust races, others resistant to multiple leaf and stem rust races, and a subset combining resistance to multiple rust species, representing valuable germplasm for breeding durable resistance. This study provides a comprehensive genomic and phenotypic characterization of WEW, uncovering its population structure and identifying valuable genetic resources for rust resistance. The identified loci and resistant accessions offer key opportunities for the targeted introgression of novel resistance genes into cultivated wheat, contributing to durable and sustainable global wheat production.