Corn rust population genomics reveals a cryptic virulent group and adaptive effectorome

Understanding the population structure of pathogens and the genetic determinants driving virulence gains is crucial for managing epidemic plant diseases. Puccinia polysora, a giga-scale fungal pathogen causing southern corn rust, has posed significant threat to global food security recently. Traditionally, P. polysora was considered clonal with minimal genetic variation. However, our population genomic and transcriptomic studies conducted in China, the emerging epicentre of the disease, have challenged this view. By adopting variant analyses appropriate to the dikaryotic nature of the pathogen, we discovered an unexpectedly clear population structure with six distinct groups. A cryptic group exhibits high virulence, facilitated by group-specific variation, and diversification of effectors. Although the Chinese population of P. polysora is predominantly asexual, internuclear exchange on some chromosomes have introduced recombination signals. The comprehensive pan-effectorome analyses revealed substantial presence/absence variation and alternative splicing events on effectors, shaping a highly adaptive effector repertoire in P. polysora. In conclusion, our findings highlight the tandem mapping on exploring clear genetic structure of dikaryotic species and reported the emergence of a virulent group and an adaptive effectorome of P. polysora. Effective containment strategies must be flexible to counter the threats posed by the unexpectedly dynamic evolution of this pathogen.