Plant viruses have traditionally been studied as causes of crop diseases or, more recently, of wild plants. This has introduced a significant bias in our perception of their diversity and in the interpretation of the nature of plant-virus interactions and their evolution. Studies of the set of viruses (the virome) infecting a host plant population or a plant community have revealed a remarkable diversity of viruses that, in general, are not associated with disease symptoms in infected plants. Moreover, experiments conducted under controlled conditions have shown that viruses can confer benefits to plants by enhancing their tolerance to other stresses. These findings have led to the proposal that viruses are not necessarily plant pathogens; under certain conditions, infection may have no effects (commensalism) or even be beneficial (mutualism).

Extrapolate results obtained under controlled conditions to natural environments can be risky. Therefore, the possibility that viruses provide benefits to plants under certain circumstances (that is, that they act as conditional mutualists) must be demonstrated under field conditions. A new study conducted by the ‘Plant-virus interaction and co-evolution’ research group at the CBGP and published in New Phytologist reveals that, in nature, the type of interaction between plants and viruses varies along a continuum ranging from beneficial to detrimental for the plant.

The type of plant-virus interaction in nature depends on various factors

The researchers analyzed the effect of infection by Cucumber mosaic virus (CMV), which frequently infects Arabidopsis thaliana in nature, in two wild populations of this plant that occur under very different ecological conditions. In each population, they examined plant demography and the dynamics of CMV infection, and for each individual plant, they quantified traits related to survival and reproduction.

They also experimentally tested whether infection increases tolerance to cold and drought. The data obtained show that the plant-virus interaction can be neutral, beneficial, or detrimental to the plant depending on several factors, including the population, the plant’s life cycle (whether it germinated in autumn and thus overwintered, or in spring), and the timing of infection relative to plant development. In addition, the researchers found that infection enhances drought tolerance.

A field study of exceptional detail

The results, obtained from field work with a level of detail not previously achieved in other systems, demonstrate that in nature, the type of interaction between plants and viruses varies along a continuum, ranging from beneficial to detrimental interactions. The type of interaction depends on environmental conditions and the plant itself (e.g., its life cycle), and in this study, we identified several of these conditions.

Furthermore, these findings challenge preconceived ideas about the interactions between viruses and plants. For example, if viruses are not always pathogenic, do plants develop defenses against their infection? And if they do, what is the cost of these defenses?