Nuclear exchange generates population diversity in the wheat leaf rust pathogen Puccinia triticina

Abstract

In clonally reproducing dikaryotic rust fungi, non-sexual processes such as somatic nuclear exchange are postulated to play a role in diversity but have been difficult to detect due to the lack of genome resolution between the two haploid nuclei. We examined three nuclear-phased genome assemblies of Puccinia triticina, which causes wheat leaf rust disease. We found that the most recently emerged Australian lineage was derived by nuclear exchange between two pre-existing lineages, which originated in Europe and North America. Haplotype-specific phylogenetic analysis reveals that repeated somatic exchange events have shuffled haploid nuclei between long-term clonal lineages, leading to a global P. triticina population representing different combinations of a limited number of haploid genomes. Thus, nuclear exchange seems to be the predominant mechanism generating diversity and the emergence of new strains in this otherwise clonal pathogen. Such genomics-accelerated surveillance of pathogen evolution paves the way for more accurate global disease monitoring.