Evidence for horizontal gene transfer and separation of effector recognition from effector function revealed by analysis of effector genes shared between cape gooseberry- and tomato-infecting formae speciales of Fusarium oxysporum

Abstract

RNA sequencing (RNAseq) reads from cape gooseberry plants (Physalis peruviana) infected with Fusarium oxysporumf. sp. physali (Foph) were mapped against the lineage‐specific transcriptome of Fusarium oxysporumf. sp. lycopersici (Fol) to look for putative effector genes. Homologues of Fol SIX1(designated SIX1a and SIX1b), SIX7, SIX10, SIX12, SIX15 and Ave1were identified. The near identity of the Foph and Fol SIX7, SIX10 and SIX12genes and their intergenic regions suggest that this gene cluster may have undergone recent lateral transfer. Foph SIX1a and SIX1bwere tested for their ability to complement a SIX1 knockout mutant of Fol. This mutant shows reduced pathogenicity on susceptible tomato plants, but is able to infect otherwise resistant tomato plants carrying the I‐3 gene for Fusarium wilt resistance (SIX1 corresponds to Avr3). Neither SIX1a nor SIX1b could restore full pathogenicity on susceptible tomato plants, suggesting that any role they may play in pathogenicity is likely to be specific to cape gooseberry. SIX1b, but not SIX1a, was able to restore avirulence on tomato plants carrying I‐3.These findings separate the recognition of SIX1 from its role as an effector and suggest direct recognition by I‐3. A hypervariable region of SIX1undergoing diversifying selection within the F. oxysporum species complex is likely to play an important role in SIX1 recognition. These findings also indicate that I‐3could potentially be deployed as a transgene in cape gooseberry to protect this emerging crop from Foph.Alternatively, cape gooseberry germplasm could be explored for I‐3homologues capable of providing resistance to Foph.