Tomato immune receptor Ve1 recognizes surface-exposed co-localized N- and C-termini ofVerticillium dahliaeeffector Ave1

Abstract

Effectors are secreted by plant pathogens to facilitate infection, often through deregulation of host immune responses. During host colonization, race 1 strains of the soil-borne vascular wilt fungus Verticillium dahliae secrete the effector protein Ave1 that triggers immunity in tomato genotypes that encode the Ve1 immune receptor. Homologs of V. dahliae Ave1 (VdAve1) are found in plants and in few plant pathogenic microbes, and are differentially recognized by Ve1.However, how VdAve1 is recognized by Ve1 remained unknown. Interestingly, C-terminally affinity-tagged versions of VdAve1 failed to activate Ve1-mediated immunity, suggesting that exposure of the C-terminus of VdAve1 is required for Ve1-mediated recognition. This was confirmed by subsequent analysis of C-terminal deletion mutants, and by domain swap experiments. Although required, only the C-terminus of VdAve1 is not sufficient to activate Ve1-mediated immunity. Intriguingly, a three-dimensional structural model of VdAve1 revealed that the N-and C-termini co-localize on a surface-exposed patch of the VdAve1 protein. Indeed, subsequent analyses of N-terminal deletion mutants confirmed that also the N-terminus of VdAve1 is required to activate Ve1-mediated immunity. Thus, we conclude that a surfaceexposed patch of the VdAve1 protein that is composed by co-localized N-and C-termini is recognized by the tomato immune receptor Ve1.

Transfer of tomato immune receptor Ve1 confers Ave1‐dependent Verticillium resistance in tobacco and cotton

“…In summary, our data demonstrate that transfer of tomato Ve1 into the closely related crop species tobacco and the distantly related crop species leads to enhanced resistance against Verticillium wilt in an Ave1‐dependent manner. Given that Ave1 homologues were found in a number of pathogenic microbes (Gan et al ., ; de Jonge et al ., ; Nembaware et al ., ), and these homologs were differentially recognized by tomato Ve1 (de Jonge et al ., ; Song et al ., ), our findings may further broaden biotechnological avenues to exploit tomato Ve1 for engineering disease resistance in an Ave1(homolog)‐dependent manner, for instance through transfer or artificial evolution of tomato Ve1 .…”

Recognition of Verticillium effector Ave1 by tomato immune receptor Ve1 mediates Verticillium resistance in diverse plant species

“…Ave1 complementation construct pFBT 005_pAve1::Ave1 that was described earlier (Song et al, 2017b) was used to generate Ave1 expression strains in V. alfalfae strain Va2 (Table S1). …”

“…alfalfae and V. nonalfalfae Song et al, 2017b). Interestingly, homologues of Ave1 were found in the bacterial plant pathogen Xanthomonas axonopodis pv.…”

“…Given that Ave1 homologues were found in a number of pathogenic microbes Gan et al, 2013), and these homologs were differentially recognized by tomato Ve1 Song et al, 2017b), our findings may further broaden biotechnological avenues to exploit tomato Ve1 for engineering disease resistance in an Ave1(homolog)-dependent manner, for instance through transfer or artificial evolution of tomato Ve1. …”

“…A few of these homologues are differentially recognized by tomato Ve1 in Nicotiana tabacum Song et al, 2017b). …”