Phenotypic and genomic changes during Turnip mosaic virus adaptation to Arabidopsis thaliana mutants lacking epigenetic regulatory factors

Abstract

In this study we investigated how RNA viral populations evolve, interact and adapt to epigenetically-controlled plant defense mechanisms. We have evolved five independent lineages of turnip mosaic virus (TuMV) in a set of Arabidopsis thaliana genotypes carrying mutations that influence important elements of two main epigenetic pathways. All evolved lineages showed adaptation to the lack of epigenetically-regulated responses through significant increases in infectivity, virulence and viral load although the magnitude of the improvements strongly depended on the plant genotype. In early passages, these traits evolved more rapidly, but the rate of evolution flattened out in later ones. Viral load was positively correlated with different measures of virulence, though the strength of the associations changed from the ancestral to the evolved viruses. High-throughput sequencing was used to evaluate the viral diversity of each lineage, as well as characterizing the nature of fixed mutations, evolutionary convergences and potential targets of TuMV adaptation. Within each lineage, we observed a net increase in genome-wide genetic diversity, with some instances where nonsynonymous alleles experienced a transient rise in abundance before being displaced by the ancestral allele. Viral VPg protein has been shown as a key player in the adaptation process, even though no obvious association between fixed alleles and host genotype was found. Layman SummaryEpigenetic factors influence the expression of defense genes in plants, allowing for phenotypic rapid responses to infections by pathogens. The role of epigenetics in shaping the coevolution between host and pathogens has received very little attention. Here, we explored how RNA viruses interact and adapt to plant defense mechanisms that are controlled by epigenetic factors. We conducted evolution experiments on turnip mosaic virus using Arabidopsis thaliana genotypes with mutations that affect epigenetic pathways. We found that all evolved viral lineages adapted to the alteration of epigenetically-regulated responses by becoming more infectious, virulent, and having a higher viral load. The improvements varied depending on the plant genotype. The study also found that viral load was positively correlated with virulence, but the associations changed from the original to the evolved viruses. We used high-throughput sequencing to evaluate viral diversity and found an increase in each evolving lineage. We found that virus adaptation primarily targeted viral VPg, despite no obvious association between fixed alleles and host genotype being found. Teaser TextDiscover how RNA viruses adapt and evolve to plant defense mechanisms controlled by epigenetic factors. This research found that epigenetic regulation of defense genes modulates viral evolution. Viral lineages became more infectious, virulent, and had a higher viral load. Find out more about the correlation between viral load and virulence, viral diversity, and the primary virus genomic target of adaptation.