Haplotype-resolved genomes of diverse oat crown rust isolates reveal global dispersion of long-lived clonal haplotypes with limited recombination

Authors: HENNINGSEN, EVA - Commonwealth Scientific And Industrial Research Organisation (CSIRO); NAZARENO, ERIC - University Of Minnesota; SPANNER, REBECCA - University Of Minnesota; LEWIS, DAVID - Commonwealth Scientific And Industrial Research Organisation (CSIRO); LUBEGA, JIBRIL - National Institute Of Agricultural Botany (NIAB); Moreau, Erin; Moscou, Matthew; BOESEN, BRENDAN - Commonwealth Scientific And Industrial Research Organisation (CSIRO); STONE, ERIC - Australian National University; KANYUKA, KOSTYA - National Institute Of Agricultural Botany (NIAB); Kianian, Shahryar; STEFFENSON, BRIAN - University Of Minnesota; DODDS, PETER - Commonwealth Scientific And Industrial Research Organisation (CSIRO); SPERSCHNEIDER, JANA - Commonwealth Scientific And Industrial Research Organisation (CSIRO); FIGUEROA, MELANIA - Commonwealth Scientific And Industrial Research Organisation (CSIRO)

Submitted to: Molecular Plant-Microbe Interactions
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/8/2026
Publication Date: N/A
Citation: N/A
DOI: https://doi.org/10.1094/MPMI-08-25-0111-R

Interpretive Summary: One of the most important diseases affecting oat production worldwide is oat crown rust caused by the fungus Puccinia coronata f. sp. avenae (Pca). The pathogen has high evolutionary potential and can generate new virulences through mutations, meiotic recombination, and reassortment of virulence factors with the aid of its alternate host, common buckthorn (Rhamnus cathartica). Losses due to the disease could reach up to 50% in certain parts of the U.S. To broaden the geographic and temporal distribution of available Pca genomes, we generated nuclear haplotype-resolved genome references for ten isolates from Europe, Africa and the Middle East and compared these with existing references for USA and Australian isolates. Of the full collection of 52 haplotypes, 40 were unique. Importantly, the presence of a nearly identical haplotype in a UK isolate collected in 1984 and in USA isolates from 1990 and 2017 supports the existence of long-lived clonal haplotypes in the global population that have been exchanged between lineages. Taken together with the identification of infrequent recombination between haplotypes from geographically dispersed isolates, this evidence reflects a globally mobile population of Pca that is mostly comprised of persistent clonal lineages with some influence from rare recombination events. We anticipate that this expanded collection of haplotypes will facilitate the development of new surveillance technologies and identification of virulence loci.

Technical Abstract: Genetic diversity of pathogen populations plays an important role in host adaptation. While single high quality genome references are a valuable resource, a compilation of genome references from individuals increases the breadth of genetic variation within a species that is captured. Puccinia coronata f. sp. avenae (Pca), a fungal pathogen causing crown rust of oat, demonstrates rapid virulence evolution and adaptation to newly released cultivars. To broaden the geographic and temporal distribution of available Pca genomes, we generated nuclear haplotype-resolved genome references for ten isolates from Europe, Africa and the Middle East and compared these with existing references for USA and Australian isolates. Of the full collection of 52 haplotypes, 40 were unique. Importantly, the presence of a nearly identical haplotype in a UK isolate collected in 1984 and in USA isolates from 1990 and 2017 supports the existence of long-lived clonal haplotypes in the global population that have been exchanged between lineages. Taken together with the identification of infrequent recombination between haplotypes from geographically dispersed isolates, this evidence reflects a globally mobile population of Pca that is mostly comprised of persistent clonal lineages with some influence from rare recombination events. Analysis of the core and non-core proteome suggests that while the core proteome is enriched for predicted secreted and effector proteins, sequence and expression variation are most prevalent in non-core orthogroups. We anticipate that this expanded collection of haplotypes will facilitate the development of new surveillance technologies and identification of virulence loci.