Cauliflower Mosaic Virus Utilizes Processing Bodies to Escape Translational Repression in Arabidopsis

Abstract

Viral infections impose extraordinary RNA stress on a cell, triggering cellular RNA surveillance pathways like RNA decapping, nonsense-mediated decay and RNA silencing. Viruses need to maneuver between 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 investigate the role of Arabidopsis thaliana PBs during Cauliflower Mosaic Virus (CaMV) infection. We find that several PB components are co-opted into viral replication factories and support virus multiplication. This pro-viral role was not associated with RNA decay pathways but instead, we could establish PB components as essential helpers in viral RNA translation. While CaMV is normally resilient to RNA silencing, PB dysfunctions expose the virus to this pathway, similar to previous observations on transgenes. Transgenes, however, undergo RNA Quality Control dependent RNA degradation, whereas CaMV RNA remains stable but becomes translationally repressed through decreased ribosome association, revealing a unique dependence between 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.

Cauliflower mosaic virusdisease spectrum uncovers novel susceptibility factor NCED9 inArabidopsis thaliana

“…Importantly, no resistance gene is known for Caulimoviruses, except the CAR1 locus in the Arabidopsis En-2 accession which has not been further mapped (Adhab et al, 2018). Nonetheless, several genes involved in various cellular homeostatic processes have been identified through genetic studies that influence CaMV accumulation (Hoffmann et al, 2022;Shukla et al, 2021;Hafren et al, 2017;Schepetilnikov et al, 2011;Love et al, 2005). Eight out of the 15 T-DNA insertion lines we tested displayed reduced CaMV accumulation in the Col-0 background compared to Col-0 wild type, which appears high as SNPs identified via GWA are frequently effective only in their natural genetic background (Gallois et al, 2018;Corwin et al, 2016).…”

“…Thus, NCED9 appears to be a CaMV specific susceptibility factor. CaMV RNAs are very stable and can accumulate to high levels despite reduction in viral DNA (Hoffmann et al, 2022). In nced9, all three major viral RNA species were reduced, but not as drastic as the viral DNA (Figure 3B and Figure 5E), but still a remarkable inhibition of infection.…”

“…CaMV challenges its host with the establishment of large cytoplasmic viral replication centers, as well as an uncommon increase of global translation, due to the viral translational transactivator protein P6 (Hoffmann et al, 2022;Schoelz & Leisner, 2017). The unique properties of CaMV implicate the existence of a network of host factors possibly influencing CaMV disease.…”