Pathotypes of Fusarium oxysporum f. sp. fragariae express discrete repertoires of accessory genes and induce distinct host transcriptional responses during root infection

Convergent evolution of phytopathogenicity is poorly described, especially among multiple strains of a single microbial species. We investigated this phenomenon with genetically diverse isolates of Fusarium oxysporum f. sp. fragariae (Fof) that cause one of two syndromes: chlorosis and wilting (the ‘yellows‐fragariae’ pathotype), or only wilting (the ‘wilt‐fragariae’ pathotype). We challenged strawberry (Fragaria × ananassa) plants to root infection by five fungal isolates: three yellows‐fragariae, one wilt‐fragariae and one that is not pathogenic to strawberry. All Fof isolates had chromosome‐level assemblies; three were newly generated. The two pathotypes triggered distinct host responses, especially among phytohormone‐associated genes; yellows‐fragariae isolates strongly induced jasmonic acid‐associated genes, whereas the wilt‐fragariae isolate primarily induced ethylene biosynthesis and signalling. The differentially expressed genes on fungal accessory chromosomes were almost entirely distinct between pathotypes. We identified an ~150 kbp ‘pathogenicity island’ that was horizontally transferred between wilt‐fragariae strains. This predicted pathogenicity island was enriched with differentially expressed genes whose predicted functions were related to plant infection, and only one of these genes was also upregulated in planta by yellows‐fragariae isolates. These results support the conclusion that wilt‐ and yellows‐fragariae cause physiologically distinct syndromes by the expression of discrete repertoires of genes on accessory chromosomes.