Arabidopsis RNA processing body components LSM1 and DCP5 aid in the evasion of translational repression during Cauliflower mosaic virus infection

Viral infections impose extraordinary RNA stress, triggering cellular RNA surveillance pathways such as RNA decapping, nonsense-mediated decay, and RNA silencing. Viruses need to maneuver among these pathways to establish infection and succeed in producing high amounts of viral proteins. Processing bodies (PBs) are integral to RNA triage in eukaryotic cells, with several distinct RNA quality control pathways converging for selective RNA regulation. In this study, we investigated the role of Arabidopsis thaliana PBs during Cauliflower mosaic virus (CaMV) infection. We found that several PB components are co-opted into viral factories that support virus multiplication. This pro-viral role was not associated with RNA decay pathways but instead, we established that PB components are helpers in viral RNA translation. While CaMV is normally resilient to RNA silencing, dysfunctions in PB components expose the virus to this pathway, which is similar to previous observations for transgenes. Transgenes, however, undergo RNA quality control-dependent RNA degradation and transcriptional silencing, whereas CaMV RNA remains stable but becomes translationally repressed through decreased ribosome association, revealing a unique dependence among PBs, RNA silencing, and translational repression. Together, our study shows that PB components are co-opted by the virus to maintain efficient translation, a mechanism not associated with canonical PB functions. Arabidopsis RNA processing body components LSM1 and DCP5 are co-opted by Cauliflower mosaic virus to maintain efficient virus translation in the presence of RNA DEPENDENT POLYMERASE6-governed silencing.

Automated summary

Viral infections cause significant stress on cellular RNA and trigger RNA surveillance pathways. In this study, PB components in Arabidopsis were found to be co-opted by the Cauliflower mosaic virus (CaMV) to facilitate viral replication and translation. This pro-viral role was not associated with RNA decay but instead helped in viral RNA translation. Dysfunctions in PB components exposed the virus to RNA silencing, similar to what has been observed in transgenes. Our study highlights the importance of PB components in maintaining efficient virus translation and their unique dependence on RNA silencing.