Inter‐virus relationships in mixed infections and virus‐drought relationships in plants: a quantitative review

Abstract

SUMMARYInter‐virus relationships in mixed infections and virus‐drought relationships are important in agriculture and natural vegetation. In this quantitative review, we sampled published factorial experiments to probe for relationships against the null hypothesis of additivity. Our sample captured antagonistic, additive and synergistic inter‐virus relationships in double infections. Virus‐drought relationships in our sample were additive or antagonistic, reinforcing the notion that viruses have neutral or positive effects on droughted plants, or that drought enhances plant tolerance to viruses. Both inter‐virus and virus‐drought relationships vary with virus species, host plant to the level of cultivar or accession, timing of infection, plant age and trait and growing conditions. The trait‐dependence of these relationships has implications for resource allocation in plants. Owing to lagging theories, more experimental research in these fields is bound to return phenomenological outcomes. Theoretical work can advance in two complementary directions. First, the effective theory models the behaviour of the system without specifying all the underlying causes that lead to system state change. Second, mechanistic theory based on a nuanced view of the plant phenotype that explicitly considers downward causation; the influence of the plant phenotype on inter‐virus relations and vice versa; the impact of timing, intensity and duration of drought interacting with viruses to modulate the plant phenotype; both the soil (moisture) and atmospheric (vapour pressure deficit) aspects of drought. Theories should scale in time, from short term to full growing season, and in levels of organisation up to the relevant traits: crop yield in agriculture and fitness in nature.

Interplay between drought and plant viruses co-infecting melon plants

“…2 ); the expected reduction from an additive effect (0.19 + 0.22 = 0.41) compared with an actual reduction of 0.17 MPa, returning an actual-to-additive ratio of 0.42 (0.17/0.41), i.e. the reduction in leaf water potential was 42% of that expected from additivity in correspondence with an antagonistic relationship 22 . At 78 DAT, the actual-to-additive ratio was 2.1, highlighting the synergy between CMV and CABYV (Fig.…”

“…In common with 30 – 32 we established water stress before virus inoculation as opposed to studies of virus-drought relations where plants were subjected to water stress weeks after virus inoculation 20 , 28 , 29 . Our experimental sequence of treatments corresponds to a scenario where virus infection follows the development of drought stress in association with, for example, (i) dry spells early in the season and (ii) gradual development of viral diseases 22 . Plant virus spread is a gradual process and may take several infection cycles that last many days for non-persistently transmitted viruses, including CMV in our study 33 .…”

“…Both inter-virus relationships in mixed infections and virus-drought relations have attracted substantial research effort, and a quantitative review captured antagonistic, additive, and synergistic inter-virus relationships in double infections whereas virus-drought relationships are dominantly additive or antagonistic, reinforcing the notion that viruses have neutral or positive effects on droughted plants, or that drought enhances plant tolerance to viruses 22 . However, this interpretation partially stems from experiments where virus-infected plants are subjected to water stress after virus infection; the sequence of treatments, namely virus infection followed by drought or drought followed by virus infection influences the outcome of the relationships.…”

“…However, this interpretation partially stems from experiments where virus-infected plants are subjected to water stress after virus infection; the sequence of treatments, namely virus infection followed by drought or drought followed by virus infection influences the outcome of the relationships. The interplay between inter-virus relationships in mixed infections and drought, the focus of this study, remains largely unexplored 22 .…”

Stress combination: from genes to ecosystems

“…The conceptual framework described by these authors will help inform the next generation of plant-focused global change experiments, specifically aimed at the non-additivity of effects at the confluence of many factors. Sadras et al (2024) review some of the very interesting aspects of virus-virus (intervirus) and virus-drought combinations, discussing antagonistic, additive, and synergistic inter-virus relationships in double infections, as well as additive or antagonistic virusdrought interactions. They then relate these to crop yield in agriculture and crop fitness in the field.…”