Knock-out mutation of eukaryotic initiation factor 4E2 (eIF4E2) confers resistance to pepper veinal mottle virus in tomato.

Translation initiation factors 4E (eIF4E) are the main source of resistance to potyvirus. We systematically assessed tomato single and double knock-out (KO) mutants of members of the eIF4E-coding gene family for resistance to Pepper veinal mottle virus (PVMV), a major constraint to tomato production. We show that the KO mutant of eIF4E2 has partial resistance to PVMV isolate IC, with plants harboring weak symptoms and low virus loads at the systemic level. The causal effect of eIF4E2 loss-of-function on resistance was confirmed on a progeny segregating for the KO mutation. The eIF4E2 KO mutant was resistant to six of the eight PVMV isolates tested and no resistance to other potyviruses was observed. This is the first evidence that mutation of eIF4E2 is in itself conferring resistance to a potyvirus and 3D protein modelling suggests that the eIF4E2 gene could be converted into a functional resistance allele.

Interaction patterns between potato virus Y and eIF4E-mediated recessive resistance in the Solanaceae.

UNLABELLED: The structural pattern of infectivity matrices, which contains infection data resulting from inoculations of a set of hosts by a set of parasites, is a key parameter for our understanding of biological interactions and their evolution. This pattern determines the evolution of parasite pathogenicity and host resistance, the spatiotemporal distribution of host and parasite genotypes, and the efficiency of disease control strategies. Two major patterns have been proposed for plant-virus genotype infectivity matrices. In the gene-for-gene model, infectivity matrices show a nested pattern, where the host ranges of specialist virus genotypes are subsets of the host ranges of less specialized viruses. In contrast, in the matching-allele (MA) model, each virus genotype is specialized to infect one (or a small set of) host genotype(s). The corresponding infectivity matrix shows a modular pattern where infection is frequent for plants and viruses belonging to the same module but rare for those belonging to different modules. We analyzed the structure of infectivity matrices between Potato virus Y (PVY) and plant genotypes in the family Solanaceae carrying different eukaryotic initiation factor 4E (eIF4E)-coding alleles conferring recessive resistance. Whereas this system corresponds mechanistically to an MA model, the expected modular pattern was rejected based on our experimental data. This was mostly because PVY mutations involved in adaptation to a particular plant genotype displayed frequent pleiotropic effects, conferring simultaneously an adaptation to additional plant genotypes with different eIF4E alleles. Such effects should be taken into account for the design of strategies of sustainable control of PVY through plant varietal mixtures or rotations. IMPORTANCE: The interaction pattern between host and virus genotypes has important consequences on their respective evolution and on issues regarding the application of disease control strategies. We found that the structure of the interaction between Potato virus Y (PVY) variants and host plants in the family Solanaceae departs significantly from the current model of interaction considered for these organisms because of frequent pleiotropic effects of virus mutations. These mutational effects allow the virus to expand rapidly its range of host plant genotypes, make it very difficult to predict the effects of mutations in PVY infectivity factors, and raise concerns about strategies of sustainable management of plant genetic resistance to viruses.