Transcriptional and hormonal profiling uncovers the interactions between plant developmental stages and RNA virus infection.

Arabidopsis thaliana is more susceptible to certain viruses during its later developmental stages. The differential responses and the mechanisms behind this development-dependent susceptibility to infection are still not fully understood. Here we explored the outcome of a viral infection at different host developmental stages by studying the response of A. thaliana to infection with turnip mosaic virus at three developmental stages: juvenile vegetative, bolting, and mature flowering plants. We found that infected plants at later stages downregulate cell wall biosynthetic genes and that this downregulation may be one factor facilitating viral spread and systemic infection. We also found that, despite being more susceptible to infection, infected mature flowering plants were more fertile (i.e. produce more viable seeds) than juvenile vegetative and bolting infected plants; that is, plants infected at the reproductive stage have greater fitness than plants infected at earlier developmental stages. Moreover, treatment of mature plants with salicylic acid increased resistance to infection at the cost of significantly reducing fertility. Together, these observations support a negative trade-off between viral susceptibility and plant fertility. Our findings point towards a development-dependent tolerance to infection.

Viral strain-dependent impact of plant developmental stages on the nestedness and modularity of plant-virus interaction matrices.

This study examines the specificity of adaptation of lineages of turnip mosaic virus that were experimentally evolved from naïve and preadapted strains to Arabidopsis thaliana plants at various plant developmental stages. We conducted a cross-infection experiment involving three plant developmental stages and assessed the progression of disease and symptoms. We found a significative interaction between the host developmental stage where the virus evolved and the host developmental stage in which the virus was tested. The analysis of the resulting interaction matrices revealed significant nestedness for viruses evolved from the naïve strain, but not for those originating from the preadapted one. Furthermore, there was an absence of modularity across all matrices. Our findings suggest that the past adaptation history of the ancestral strain influences its future evolution, and each plant developmental stage imposes unique selective constraints. The study highlights the complexity of host-parasite interactions and the potential influence of the host's developmental stage on viral adaptation.

Host developmental stages shape the evolution of a plant RNA virus.

Viruses are obligate pathogens that entirely rely on their hosts to complete their infectious cycle. The outcome of viral infections depends on the status of the host. Host developmental stage is an important but sometimes overlooked factor impacting host-virus interactions. This impact is especially relevant in a context where climate change and human activities are altering plant development. To better understand how different host developmental stages shape virus evolution, we experimentally evolved turnip mosaic virus (TuMV) on Arabidopsis thaliana at three different developmental stages: vegetative (juvenile), bolting (transition) and reproductive (mature). After infecting plants with an Arabidopsis-naive or an Arabidopsis-well-adapted TuMV isolate, we observed that hosts in later developmental stages were prone to faster and more severe infections. This observation was extended to viruses belonging to different genera. Thereafter, we experimentally evolved lineages of the naive and the well-adapted TuMV isolates in plants from each of the three developmental stages. All evolved viruses enhanced their infection traits, but this increase was more intense in viruses evolved in younger hosts. The genomic changes of the evolved viral lineages revealed mutation patterns that strongly depended on the founder viral isolate as well as on the developmental stage of the host wherein the lineages were evolved. This article is part of the theme issue 'Infectious disease ecology and evolution in a changing world'.

Plant virus evolution under strong drought conditions results in a transition from parasitism to mutualism.

Environmental conditions are an important factor driving pathogens' evolution. Here, we explore the effects of drought stress in plant virus evolution. We evolved turnip mosaic potyvirus in well-watered and drought conditions in Arabidopsis thaliana accessions that differ in their response to virus infection. Virus adaptation occurred in all accessions independently of watering status. Drought-evolved viruses conferred a significantly higher drought tolerance to infected plants. By contrast, nonsignificant increases in tolerance were observed in plants infected with viruses evolved under standard watering. The magnitude of this effect was dependent on the plant accessions. Differences in tolerance were correlated to alterations in the expression of host genes, some involved in regulation of the circadian clock, as well as in deep changes in the balance of phytohormones regulating defense and growth signaling pathways. Our results show that viruses can promote host survival in situations of abiotic stress, with the magnitude of such benefit being a selectable trait.