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 conditions virus evolution. Differences in host susceptibility can drive a virus to diversify into strains that track different defense alleles (e.g., antigenic diversity) or to infect only the most susceptible genotypes. Here, we have studied how variability in host defenses determine the evolutionary fate of a plant RNA virus. We performed evolution experiments with Turnip mosaic potyvirus in Arabidopsis thaliana mutants that had disruptions in infection-response signaling pathways or in genes whose products are essential for potyvirus infection. Plant genotypes were classified into five phenogroups according to their response to infection. We found that evolution proceeded faster in more restrictive hosts than in more permissive ones. Most of the phenotypic differences shown by the ancestral virus across host genotypes were removed after evolution, suggesting the combined action of selection and chance. When all evolved viral lineages were tested in all plant genotypes used in the experiments, we found compelling evidences that the most restrictive plant genotypes selected for more generalist viruses, while more permissive genotypes selected for more specialist viruses. Sequencing the genomes of the evolved viral lineages, we found that selection targeted the multifunctional protein VPg in most host genotypes. Overall, this work illustrates how different host defenses modulate the rates and extent of virus evolution.

Host developmental stages shape the evolution of a plant RNA virus

“…The selection on VPg mutants at position N2039 seems related with the functions of this protein: virus movement, genome replication and suppression of host antiviral RNA silencing [ 53 ]. Previous evolutionary experiments from our group have also described mutations in the same region of VPg on evolved viruses with increased virulence, independently of the Arabidopsis genotype, its susceptibility to infection or the environmental conditions [ 70 , 73 ]. Similarly, mutations in this protein increased the fitness of TuMV in Arabidopsis plants with knock-outs in the eIF(iso)4E and eIF(iso)4G genes [ 74 ] as well as the virulence of potato virus Y in resistant pepper plants [ 75 ].…”

Genetic basis ofArabidopsis thalianaresponses to infection by naïve and adapted isolates of turnip mosaic virus

“…The increase in virulence of the evolved isolate used in this study is associated with two non-synonymous mutations acquired during adaptation to A. thaliana (Navarro et al, 2022). First, mutation T1293I was found in the cylindrical inclusion protein (CI) that is involved in viral genome replication and cell-to-cell movement (Deng et al, 2015), and has been shown to interact with the photosystem I PSI-K protein in A. thaliana (Jiménez et al, 2006).…”

“…Second, mutation N2039H was found in the viral genome-linked protein (VPg) that is involved in replication and intracellular movement (Wu et al, 2018), and is a hub for interactions with other viral proteins (Bosque et al, 2014). Mutations in VPg have been pervasively observed in evolution experiments of potyviruses in A. thaliana , in all cases resulting in increased infectivity, virulence and viral load (Agudelo-Romero et al, 2018; Hillung et al, 2014; González et al, 2021; Navarro et al, 2022; Melero et al, 2023). Together, these observations indicate that genome replication and viral movement underlie the increased virulence of the evolved virus.…”

Effect of disease prevalence and growth stage on symptoms severity in theTurnip mosaic virus - Arabidopsis thalianapathosystem

“…Furthermore, these authors concluded that JIN1 affected basal resistance rather than resistance based on gene-for-gene interactions. In general, enhanced JA accumulation favors plant defense against viral infections (Islam et al 2019); and for example, jin1 plants show increased susceptibility to TuMV infection (Navarro et al 2022).…”