Defects in plant immunity modulate the rates and patterns of RNA virus evolution

Abstract

It is assumed that host genetic variability for susceptibility to infection necessarily conditions virus evolution. Differences in host susceptibility can either drive the virus to diversify into strains that track different defense alleles (e.g., antigenic diversity) or to infect only the most susceptible genotypes. To clarify these processes and their effect on virulence, we have studied how variability in host defense responses determine the evolutionary fate of viruses. To accomplish this, we performed evolution experiments with Turnip mosaic potyvirus in Arabidopsis thaliana mutants. Mutant plants had disruptions in infection-response signaling pathways or in genes whose products are essential for potyvirus infection. Genotypes were classified into five phenogroups according to their response to infection. In order to disentangle how host susceptibility affects virus adaptation, independent viral lineages were evolved in selected plant genotypes. Evaluating disease-related traits of the evolved lineages, we found that evolution proceeded faster in the most resistant hosts than in the most permissive ones, as expected for adaptation to a harsh environment. By sequencing the genomes of the evolved viral lineages, we found that the multifunctional protein VPg turned out to be the target of selection in most host genotypes. When all evolved viral lineages were tested for fitness in all plant genotypes used in the experiments, we found compelling evidences that generalist viruses were selected by the most restrictive plant genotypes, while permissive genotypes selected for specialist viruses. Overall, this work illustrates how different host defense signaling pathways constrain not only disease-related traits but virus evolution.