Population genomics of Puccinia graminis f.sp. tritici highlights the role of admixture in the origin of virulent wheat rust races

Authors: GUO, YUANWEN - Kansas State University; BETZEN, BLISS - Kansas State University; SALCEDO, ANDRES - Kansas State University; HE, FEI - Kansas State University; Bowden, Robert; Fellers, John; Jordan, Katherine; AKHUNOVA, ALINA - Kansas State University; Rouse, Matthew; SZABO, LES - Retired ARS Employee; AKHUNOV, EDUARD - Kansas State University

Submitted to: Nature Communications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/12/2022
Publication Date: 10/21/2022
Citation: Guo, Y., Betzen, B., Salcedo, A., He, F., Bowden, R.L., Fellers, J.P., Jordan, K., Akhunova, A., Rouse, M.N., Szabo, L., Akhunov, E. 2022. Population genomics of Puccinia graminis f.sp. tritici highlights the role of admixture in the origin of virulent wheat rust races. Nature Communications. https://doi.org/10.1038/s41467-022-34050-w.
DOI: https://doi.org/10.1038/s41467-022-34050-w

Interpretive Summary: One of the most significant diseases that threatens global wheat production is stem rust, caused by the fungus Puccinia graminis f. sp. tritici. For decades, plant breeders have used disease resistance genes to combat the fungus and have been largely successful. However, new virulent races have recently emerged in eastern Africa and southern Europe that overcome most of the resistance genes used in international wheat varieties. The origin of the new virulent strains has been unclear. Previous genetic diversity studies identified several groups or clades of the stem rust fungus. In this study, we identified 12 major clades or subclades. We showed that members of 7 out of the 12 groups appear to have arisen by sexual or asexual recombination between distinct ancestral populations. These population admixture events appear to play a role in the origin of new highly virulent races. Understanding how new virulent races evolve may lead to better strategies for breeding for more durable resistance.

Technical Abstract: Puccinia graminis f.sp. tritici (Pgt) causes stem rust disease in wheat that can result in severe yield losses. The factors driving the evolution of its virulence and adaptation remain poorly characterized. We utilize a long-read sequencing to develop a haplotype-resolved genome assembly of a US isolate of Pgt. Using haplotype-resolved Pgt assemblies as a reference, we characterize the structural variants (SVs) and single nucleotide polymorphisms in a diverse panel of Pgt isolates. SVs impact the repertoire of predicted effectors, secreted proteins involved in host-pathogen interaction, and show evidence of selection suggestive of their involvement in adaptation. By analyzing global and local genomic ancestry we demonstrate that the origin of 7 out of 12 Pgt clades is linked with either somatic hybridization or sexual recombination between the diverged donor populations. Our study shows that SVs and past admixture events appear to play an important role in broadening Pgt virulence and the origin of highly virulent races and creates a resource for detecting avirulence factors that might be exploited to prevent future epidemic outbreaks.