Polyphyletic origin and horizontal exchange drive the emergence of a novel resistance-breaking Fusarium oxysporum f. sp. lactucae race

Fusarium oxysporum f. sp. lactucae (Fola), the pathogen responsible for lettuce fusarium wilt, now presents a growing danger to worldwide lettuce production as resistance-breaking strains emerge swiftly. The origins and methods driving this diversification are not yet fully comprehended. Researchers examined 103 Fola strains using molecular profiling, focusing on ten crucial isolates for in-depth study.

This investigation included sequencing the genomes of the newly discovered Fola2 and Fola3, as well as a highly divergent isolate from France, designated as a potential new race called FolaX. Phylogenomic analysis showed that Fola is polyphyletic, with lettuce pathogenicity evolving independently in different F. oxysporum groups. Despite this, all lineages share a common set of conserved effector genes called PanFola, which are nearly identical, suggesting widespread horizontal gene transfer.

Resistance-breaking Fola strains within existing races were connected to copy number variations and targeted gene deletions. For instance, the SIX8/PSE1 gene was lost in Fola4+. In contrast, FolaX had a distinct core genome and a chimeric accessory genome assembled from multiple Fola lineages through segmental chromosome transfer and transposon-mediated reshuffling.

These discoveries underline the remarkable adaptability of Fola and the requirement for breeding methods that consider the continually changing nature of its effector repertoires.