Long-term surveillance reveals hybridization by nuclear reassortment and intercontinental spread as major evolutionary drivers in wheat yellow rust

Evolutionary forces affecting crop pathogens, including hybridization and long-distance dispersal (LDD), may have strong implications for food security and sustainable plant disease control at global scales. However, consolidated evidence is often lacking due to the absence of consistent pathogen surveys beyond national capacities. Our study documents world-wide connectivity between populations of Puccinia striiformis, causing yellow rust on cereals and grasses, when analyzing 3240 pathogen samples collected in 41 countries on six continents from 2009 to 2023. Our analyses revealed 10 cases of intercontinental spread of Puccinia striiformis, including seven cases with major impact on disease epidemics in recipient areas. Somatic hybridization by nuclear reassortment between co-existing multilocus genotypes (MLGs) on a common host was the most plausible mechanism for the emergence of three novel clonal groups that were first detected in Europe. Subsequently, onward spread to South America and Australia was observed. Several high-impact incursions from South Asia into East Africa were also detected, including a genotype with a dramatic impact on wheat breeding programs of global relevance. Our study stresses an urgent need for coordinated crop pathogen monitoring across borders. Only global efforts will enable prevention and control of airborne pathogens that represent major challenges for food security at regional and global scales.