Hidden Players: Latent Viruses Can Modulate Plant Disease Outcomes in Coinfection Contexts

Abstract

Latent viruses are ubiquitous components of plant viromes and are likely the rule rather than the exception in natural host populations. Yet, despite their prevalence, little is known about how they influence the outcome of infections by acute viruses. Here, we used a factorial design to test the effects of two latent secoviruses, apple latent spherical virus (ALSV) and Arabidopsis latent virus 1 (ArLV1), on infections by the acute viruses tobacco rattle virus (TRV) and turnip mosaic virus (TuMV). Coinfections were evaluated across eight Arabidopsis thaliana genotypes, including wild-type and mutants impaired in RNA silencing, DNA methylation and hormone-signaling pathways. Latent-virus effects on both viral accumulation and disease severity were highly dependent on the combination of host and viral genotypes. Hormonal pathways played a prominent role in mediating these interactions, with recurrent responses involving jasmonic acid, salicylic acid and ethylene signaling. ALSV generally attenuated disease severity and acute-virus accumulation, whereas ArLV1 produced both antagonistic and synergistic outcomes depending on host background. Notably, ArLV1 coinfection increased TuMV-induced disease severity in some genotype, an effect never observed with ALSV. These results demonstrate that latent viruses can substantially modify disease expression and viral fitness and highlight the need to account for the pre-existing virome when predicting plant disease outcomes, viral emergence, and epidemiological dynamics.