Global translational reprogramming is a fundamental layer of immune regulation in plants

Abstract

In the absence of specialized immune cells, the need for plants to reprogram transcription to transition from growth-related activities to defence is well understood1, 2. However, little is known about translational changes that occur during immune induction. Using ribosome footprinting (RF), we performed global translatome profiling on Arabidopsis exposed to the microbe-associated molecular pattern (MAMP) elf18. We found that during this pattern-triggered immunity (PTI), translation was tightly regulated and poorly correlated with transcription. Identification of genes with altered translational efficiency (TE) led to the discovery of novel regulators of this immune response. Further investigation of these genes showed that mRNA sequence features are major determinants of the observed TE changes. In the 5′ leader sequences of transcripts with increased TE, we found a highly enriched mRNA consensus sequence, R-motif, consisting of mostly purines. We showed that R-motif regulates translation in response to PTI induction through interaction with poly(A)-binding proteins. Therefore, this study provides not only strong evidence, but also a molecular mechanism for global translational reprogramming during PTI in plants.

Arabidopsis nonresponding to oxylipins locus NOXY7 encodes a yeast GCN1 homolog that mediates noncanonical translation regulation and stress adaptation

“…As for plants on the Col‐0 background, we found no marked differences between wild type and gcn2 L er plant responses to bacterial inoculation or in 35 S‐Met/Cys incorporation after CHL treatment (Figure S7), which confirms lack of GCN2 and P‐eIF2α participation in activating immunity to Pseudomonas infection (Figure ). In line with our results are the findings by Xu et al () showing that the microbe‐associated molecular pattern elf18 activates GCN2‐mediated P‐eIF2α but this reaction is not required for elf18‐induced resistance.…”

“…As translational reprogramming regulates plant immunity (Xu et al, ), we examined whether Arabidopsis GCN1 has a regulatory function in translation after pathogen attack. We used distinct gcn1 alleles and tested their response to bacterial infection.…”

“…The enhanced susceptibility of gcn1 and gcn20 mutants to Pst DC3000 infection supports a role for GCN1 and GCN20 in the plant response to bacterial infection, in which these proteins could regulate translation. Specific mRNA translation is an important response in plant immunity (Moeller et al, ; Robaglia & Caranta, ), and a recent contribution by Xu et al () showed that global translational reprogramming is a fundamental layer in immune regulation. Our results are consistent with this, as we found that bacterial infection caused a notable change in the pattern of newly synthesized proteins at 24 hr, followed by an overall reduction in protein synthesis (Figure and Figure S5).…”

“…Protein synthesis is one of the most expensive cellular processes, as it requires more than half of all energy in rapidly dividing cells (Browning & Bailey‐Serres, ). Translation is tightly regulated in early pathogen recognition responses and other energy‐disturbing conditions such as hypoxia/reoxygenation (Branco‐Price, Kaiser, Jang, Larive, & Bailey‐Serres, ) and light/dark transition (Branco‐Price et al, ; Pal et al, ; Xu et al, ). This implies a little understood functional connection between protein synthesis and energy‐supplying organelles such as mitochondria and chloroplasts.…”

Recent Discoveries on the Role of TOR (Target of Rapamycin) Signaling in Translation in Plants

“…In plants, TOP-like motifs are abundant within mRNA 59-UTRs of ribosomal proteins (Dobrenel et al, 2016b), but whether these cis-elements are involved in translation regulation in plants requires further research. Interestingly, several recent publications revealed the existence of so-called R-motifs containing GA, G(A) 3 , G(A) 6 , etc., repeats (Dobrenel et al, 2016;Xu et al, 2017), and provided evidence that the R-motif regulates translation of its mRNA via interaction with poly(A)-binding proteins during immune regulation in plants . Whether R-motifs are targets of TOR signaling in plants remains a very interesting subject of study (Fig.…”