NB-LRR signaling induces translational repression of viral transcripts and the formation of RNA processing bodies through mechanisms differing from those activated by UV stress and RNAi

Abstract

Plant NB-LRR proteins confer resistance to multiple pathogens, including viruses. Although the recognition of viruses by NB-LRR proteins is highly specific, previous studies have suggested that NB-LRR activation results in a response that targets all viruses in the infected cell. Using an inducible system to activate NB-LRR defenses, we find that NB-LRR signaling does not result in the degradation of viral transcripts, but rather prevents them from associating with ribosomes and translating their genetic material. This indicates that defense against viruses involves the repression of viral RNA translation. This repression is specific to viral transcripts and does not involve a global shutdown of host cell translation. As a consequence of the repression of viral RNA translation, NB-LRR responses induce a dramatic increase in the biogenesis of RNA processing bodies (PBs). We demonstrate that other pathways that induce translational repression, such as UV irradiation and RNAi, also induce PBs. However, by investigating the phosphorylation status of eIF2α and by using suppressors of RNAi we show that the mechanisms leading to PB induction by NB-LRR signaling are different from these stimuli, thus defining a distinct type of translational control and anti-viral mechanism in plants.

Alterations in cellular RNA decapping dynamics affect tomato spotted wilt virus cap snatching and infection in Arabidopsis

“…Increased processing body (PB) production by TRV recovery enhances TSWV accumulation in N. benthamiana Studies in multiple systems (Teixeira et al, 2005;Parker & Sheth, 2007), including plants (Meteignier et al, 2016), suggest that the formation of PBs depends on mRNA that is translationally repressed and that PB numbers increase in response to increased amounts of translationally repressed mRNAs. It was hypothesized that TSWV may replicate more efficiently when PB numbers are increased as this would indicate an increase in nonactive mRNAs whose caps would be more available for snatching.…”

“…RNA-protein complexes formed by cytoplasmic RNA decay pathways including mRNA decapping, NMD and small RNAmediated decay (RNA silencing) localize in cytoplasmic foci known as processing bodies (PBs) (Xu & Chua, 2011;Meteignier et al, 2016). Many mRNAs that are translationally repressed and/or marked for degradation accumulate in PBs, where they are either degraded or later returned to the cytoplasm (Hubstenberger et al, 2017).…”

Perception of double‐stranded RNA in plant antiviral immunity

“…a). Infection with Turnip crinkle virus, Turnip yellow mosaic virus or Potato virus X , however, does not appear to induce eIF2 alpha phosphorylation in plants (Meteignier et al ., ; Zhang et al ., ). It remains to be seen whether other viruses induce eIF2 alpha phosphorylation in plants or whether virus‐encoded inhibitors interfere with this plant response.…”

Meeting report: processing, translation, decay – three ways to keep RNA sizzling

“…Peter Moffett (Université de Sherbrooke, Canada) shared new data on the fate of translation during an active viral infection (Meteignier et al . ), as well as global changes in mRNA translatability during an artificially induced, effector‐triggered immunity response in Arabidopsis . In the latter, groups of mRNAs coding for primary metabolism and for defence responses tend to be affected in opposite ways.…”

“…These data emerged from an elegant suppressor screen for novel mutant alleles of AGO1 that escape from the pathway whereby RNA poleroviruses target AGO1 for protein degradation through the autophagy pathway. Peter Moffett (Université de Sherbrooke, Canada) shared new data on the fate of translation during an active viral infection (Meteignier et al 2016), as well as global changes in mRNA translatability during an artificially induced, effector-triggered immunity response in Arabidopsis. In the latter, groups of mRNAs coding for primary metabolism and for defence responses tend to be affected in opposite ways.…”