Viruses are far more than pathogenic agents in plants

Invited comment of CBGP researchers on the discovery of a persistent plant virus infecting Arabidopsis thaliana ecotypes from wild populations and laboratory collections: “This might be a breakthrough on our understanding of plant-virus interactions and a potential game changer for the management of A. thaliana in the laboratory”.

Plant viruses are generally regarded as pathogenic agents causing diseases in plants. CBGP researchers of Dr. Pagán´s group have been invited to comment on the recent discovery of a new plant virus (Arabidopsis latent virus 1, ArLV1) infecting Arabidopsis thaliana asymptomatically (Verhoeven et al. 2022; New Phytologist, doi: 10.1111/nph.18466). ArLV1 has been detected not only in wild plant populations but also in individuals grown from laboratory seed stocks. Dr. Pagán group highlights the relevance of this discovery for plant biology at large, and in particular for plant pathology. First, the study shows an example of a non-pathogenic plant-virus interaction, supporting the increasingly accepted idea that viruses may establish neutral or even beneficial interactions with their hosts. Second, the discovery of the virus, which was found at high prevalence, opens the possibility to explore the evolutionary processes that led to establish this apparently successful plant-virus interaction: Do viruses alter the plant biology to confer the host the capacity to better adapt to the environment? Are viruses “biological weapons” that plants can use to compete with other plants? Or a non-pathogenic interaction is just due to virus evolution towards optimal adaptation to the host and does not benefit the plant? Third, because ArLV1 is present in germplasm collections maintained in the laboratory (in theory under virus-free conditions), the only mode for virus persistence is transmission through the seeds. Thus, the results of the study highlight the importance of this mode of transmission for plant virus epidemiology and evolution. Finally, the outcome of most plant-virus interactions is genotype-per-genotype dependent. Thus, the effect of ArLV1 presence in laboratory wild-type and mutant A. thaliana genotypes can be unpredictable, and a safer use of such plants would require testing for the presence of this virus in the stocks maintained in the laboratory. This observation also has implications beyond A. thaliana as to what extent other plants commonly used in laboratory work may also contain asymptomatic viruses. Overall, the comment highlights how Verhoeven et al. work allows opening new avenues of future research to understand long-standing questions on plant biology and phytopathology, and that it might be a game changer for the management of A. thaliana, and other plants, in the laboratory.

Image: Schematic representation of the contribution of the recent article published in New Phytologist by Verhoeven et al. (2022; 10.1111/nph.18466) to the understanding of asymptomatic plant virus infections. Possible scenarios that conduced to Arabidopsis latent virus 1 (ArLV1) asymptomatic infection in Arabidopsis include mutualistic interactions between ArLV1 and Arabidopsis (note the image of the bee represents beneficial insects in general) (top left), differential effects of ArLV1 infection according to the host plant (middle left), and evolution toward ArLV1 lower virulence through adaptation to seed transmission (bottom left). Potential consequences arising from ArLV1 presence in Arabidopsis span from unexpected infection outcomes when ArLV1 is in mixed infection with other viruses (top right), to implications for Arabidopsis germplasm exchange (middle right) and routinary detection (for instance, by sequencing) in laboratory plant materials (bottom right).

Original Paper:

Sáez, C., Pagán, I. 2022. When plants are Trojan horses for viruses. New Phytologist. DOI: 10.1111/nph.18571