Viral fitness determines the magnitude of transcriptomic and epigenomic reprogramming of defense responses in plants

Abstract

<jats:title>SUMMARY</jats:title><jats:p>Although epigenetic factors may influence the expression of defense genes in plants, their role in antiviral responses and the impact of viral adaptation and evolution in shaping these interactions are still poorly explored. We used two isolates of turnip mosaic potyvirus (TuMV) with varying degrees of adaptation to <jats:italic>Arabidopsis thaliana</jats:italic> to address these issues. One of the isolates was experimentally evolved in the plant and presented increased load and virulence relative to the ancestral isolate. The magnitude of the transcriptomic responses were larger for the evolved isolate and indicated a role of innate immunity systems triggered by molecular patterns and effectors in the infection process. Several transposable elements (TEs) located in different chromatin contexts and epigenetic-related genes were also affected. Correspondingly, mutant plants having loss or gain of repressive marks were, respectively, more tolerant and susceptible to TuMV, with a more efficient response against the ancestral isolate. In wild-type plants both isolates induced similar levels of cytosine methylation changes, including in and around TEs and stress-related genes. Results collectively suggested that apart from RNA silencing and basal immunity systems, DNA methylation and histone modification pathways may also be required for mounting proper antiviral defenses in plants and that the effectiveness of this type of regulation strongly depends on the degree of viral adaptation to the host.</jats:p>

Role of the methionine cycle in the temperature‐sensitive responses of potato plants to potato virus Y

“…Another possibility would be a change in plant DNA methylation (Figure 7b), which is one of the epigenetic factors that regulates gene expression. DNA methylation is controlled by several plant SAM‐dependent DNA methyltransferases and therefore may be affected by perturbations in the MTC (Correa et al, 2020; Kuznicki et al, 2019). To fulfil its functions in plant development and responses to biotic and abiotic stress conditions, DNA methylation in plants normally achieves a balance between stable and flexible methylation status tuned with the transcriptional repressive or active state of the corresponding genes.…”

“…With regard to virus–plant interactions, the MTC is closely linked to RNAi pathways, in which siRNAs are stabilized by the MTC‐based methylation process (Li et al, 2005). Plant host DNA methylation, as an epigenetic mechanism driven by the MTC, has also been suggested as playing an important role in modulating host responses to viruses by modifying functions of host genes and affecting gene expression (Corrêa et al, 2020; Wang et al, 2019). Another factor released as a product of the MTC‐related pathway is ethylene, a plant hormone that, like other hormones, plays important roles in plant responses to biotic and abiotic stress responses (reviewed in Müller and Munné‐Bosch, 2015).…”

Adaptation of turnip mosaic potyvirus to a specific niche reduces its genetic and environmental robustness

“…In the TuMV/Arabidopsis pathosystem, there is a one-to-one match between infection status and the development of symptoms ( González, Butković, and Elena 2019 ; Corrêa et al. 2020 ); all infected plants develop obvious symptoms at the temperature conditions used in this experiment.…”

“…2020 ); all infected plants develop obvious symptoms at the temperature conditions used in this experiment. Likewise, in this pathosystem the intensity of symptoms is significantly correlated with viral load ( Corrêa et al. 2020 ).…”

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

“…A collection of 21 different A. thaliana mutants of the Col-0 accession were used for this study (Table 1). In all experiments described below, plants were all maintained in a BSL- promoter and the nos terminator (Chen et al 2003) as described elsewhere (González et al 2019;Corrêa et al 2020). This TuMV sequence variant corresponds to the YC5 isolate from calla lily (Zantesdeschia sp) (Chen et al 2003).…”