Haplotype-Resolved Genomes of Diverse Oat Crown Rust Isolates Reveal Global Dispersion of Long-Lived Clonal Haplotypes with Limited Recombination

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 further capture the genetic variation of Pca, we generated nuclear haplotype-resolved genomes 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. We identified infrequent recombination between haplotypes from geographically dispersed isolates, hinting towards a globally mobile population of Pca that is mostly comprised of persistent clonal lineages with some influence from rare recombination events. One isolate contained an additional scaffold with telomeric and centromeric features, suggesting the presence of a supernumerary chromosome. While the core pan-proteome is enriched for predicted secreted and effector proteins, sequence and expression variation are most prevalent in non-core orthogroups, which also displayed allele specific expression. We anticipate that this expanded collection of haplotypes will facilitate the development of new surveillance technologies and identification of virulence loci.