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Whole-genome sequencing of multiple isolates of Puccinia triticina reveals asexual lineages evolving by recurrent mutations

Background The wheat leaf rust fungus, Puccinia triticina Erikss. is a worldwide pathogen of tetraploid durum and hexaploid wheat. Many races of P. triticina differ for virulence to specific leaf rust resistance genes and are found in most wheat-growing regions of the world. Wheat cultivars with effective leaf rust resistance exert selection pressure on P. triticina populations for virulent race types. The objectives of this study were to examine whole-genome sequence data of 121 P. triticina isolates and to gain insight into race evolution. The collection included isolates comprising many different race phenotypes collected worldwide from common wheat in the U.S. and the European Union together with isolates from durum wheat. One isolate from the wild wheat relative Aegilops speltoides, and two from Ae. cylindrica were also included for comparison. Results Based on 121,907 variants identified relative to the reference race 1-1 genome, the isolates were clustered into 11 major lineages with 100% bootstrap support. The isolates were also grouped based on variation in approximately 1400 secreted resistance interactor candidate proteins. In gene-coding regions, all groups had high ratios of non-synonymous to synonymous mutations and nonsense to readthrough mutations. Conclusions Based on total variation or variation in the secreted protein genes, isolates grouped the same indicating that variants were distributed across the entire genome. Our results suggest that recurrent mutation and selection play a major role in differentiation within the clonal lineages.