Related mobile pathogenicity chromosomes in Fusarium oxysporum determine host range on cucurbits

Fusarium oxysporum f. sp. radicis‐cucumerinum (Forc) causes severe root rot and wilt in several cucurbit species, including cucumber, melon, and watermelon. Previously, a pathogenicity chromosome, chr(RC), was identified in Forc. Strains that were previously nonpathogenic could infect multiple cucurbit species after obtaining this chromosome via horizontal chromosome transfer (HCT). In contrast, F. oxysporum f. sp. melonis (Fom) can only cause disease on melon plants, even though Fom contains contigs that are largely syntenic with chr(RC). The aim of this study was to identify the genetic basis underlying the difference in host range between Fom and Forc. First, colonization of different cucurbit species between Forc and Fom strains showed that although Fom did not reach the upper part of cucumber or watermelon plants, it did enter the root xylem. Second, to select candidate genomic regions associated with differences in host range, high‐quality genome assemblies of Fom001, Fom005, and Forc016 were compared. One of the Fom contigs that is largely syntenic and highly similar in sequence to chr(RC) contains the effector gene SIX6. After HCT of the SIX6‐containing chromosome from Fom strains to a nonpathogenic strain, the recipient (HCT) strains caused disease on melon plants, but not on cucumber or watermelon plants. These results provide strong evidence that the differences in host range between Fom and Forc are caused by differences between transferred chromosomes of Fom and chr(RC), thus narrowing down the search for genes allowing or preventing infection of cucumber and watermelon to genes located on these chromosomes.