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 will necessarily condition the evolution of viruses, either by driving them to diversification into strains that track the different host defense alleles (e.g., antigenic diversity), or by canalization to infect only the most susceptible genotypes. Associated to these processes, virulence may or may not increase. To tackle these questions, we performed evolution experiments with turnip mosaic virus (TuMV) in Arabidopsis thaliana genotypes that differ in mutations in genes involved in resistance pathways and in genes whose products are essential for potyviruses infection. Plant genotypes classified into five groups according to their degree of resistance and intensity of symptoms. 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. The multifunctional viral protein VPg turned out to be the target of selection in most host genotypes. When all evolved TuMV lineages were tested for fitness in all plant genotypes used in the experiments, we found that the infection matrix was significantly nested, suggesting the evolution of generalist viruses selected by the most restrictive mutant genotypes. At the other side, a modular pattern, driven by convergent evolution of lineages evolved in the same host genotype, was also observed.

Arabidopsis thalianagenes contributing to differences in the outcome of infection with generalist and specialist strains ofTurnip mosaic virusidentified by genome-wide association studies

“…The two strains of TuMV used in this study, TuMV-G and TuMV-S were obtained by evolving, during 12 experimental passages, an ancestral TuMV strain in mutant plants of the A. thaliana Col-0 accession, as detailed in [27] and summarized in the Introduction.…”

“…TuMV infects mostly Brassicaceae and is widespread worldwide causing huge economical loses by damaging important crops and other plant species [25,26]. The viral strains used in this study were obtained by Navarro et al [27] by experimentally evolving a naïve ancestral TuMV isolate in A. thaliana mutants deficient in different disease signaling pathways or in presence of recessive susceptibility genes. Among all the resulting viral lineages, one evolved in the enhanced disease susceptibility 8 ( eds8-1 ) mutant, hereafter referred as TuMV-G, and another one evolved in the jasmonate insensitive 1 ( jin1 ) mutant, referred as TuMV-S, showed strikingly different host ranges.…”

“…This difference in susceptibility gave rise to the two TuMV strains, the generalist TuMV-G and the specialist TuMV-S. TuMV-G was able of infecting with equal fitness all tested plant genotypes, while TuMV-S did so only for its local host genotype. Indeed, Navarro et al [27] calculated Blüthgen’s d ’ specialization indexes [28], finding that TuMV-G had d ’ = 0 (no specialization) while TuMV-S had d ’ = 1 (complete specialization). In agreement with previous potyvirus- A. thaliana studies [29,30], more permissive hosts (here jin1 ) select for more specialized viruses while more restrictive hosts (in this case, eds8-1 ) select for more generalist viruses.…”

A genome-wide association study identifies Arabidopsis thaliana genes that contribute to differences in the outcome of infection with two Turnip mosaic potyvirus strains that differ in their evolutionary history and degree of host specialization

“…They face species with different response to infection or in many instances differences in immune status among individuals within the same host species. Some viruses adapt to a particular host species, genotype, or even cell type in which they efficiently complete their reproductive cycle ( Turner and Elena 2000 ; Cooper and Scott 2001 ; Cuevas, Moya, and Elena 2003 ; Bedhomme, Lafforgue, and Elena 2012 ; Hillung et al 2014 ; Navarro et al 2020 ). These viruses are called specialists.…”

“…This binary definition, however, does not fully reflect the complexity of interactions between parasites and their potential hosts. Specialism and generalism are broad terms that can be applied to different levels; viruses that are able to infect only one or more different hosts species, cell types, or genotypes ( Turner and Elena 2000 ; Cooper and Scott 2001 ; Cuevas, Moya, and Elena 2003 ; Bedhomme, Lafforgue, and Elena 2012 ; Navarro et al 2020 ). Let us take a very simple numerical example that easily illustrates this inconsistency.…”