Translation-dependent retrograde signaling coordinates high-light acclimation in plants

Abstract

Canonical chloroplast retrograde signaling is typically defined as chloroplast-initiated signaling circuits that regulate nuclear transcription for acclimation. This study reveals that high light (HL) also initiates translation-dependent retrograde signaling pathways (TraDeRS), which bifurcate to increase translation of chloroplast-targeted proteins and nuclear transcription factors thereby enhancing photosynthesis and reducing photoinhibition. Reprogramming of translation within 10 min of HL predominates over transcriptional regulation, evidenced by global downregulation of translation based both on ribosomal footprints (RPF) and polysome profiles in Arabidopsis. RPF-seq reveal four distinct subsets of transcripts for ribosome-mediated regulation: two subsets showing changes in ribosomal association only, and two showing combined changes of ribosomal association and transcript abundance. The ‘increased translation’ subset is enriched for chloroplast-targeted photosynthetic proteins containing evolutionarily-conserved 5’-UTR mRNA motifs. The motifs bind and release an RNA-binding protein, Glyceraldehyde 3-phosphate dehydrogenase (GAPDH), in a HL and co-factor dependent manner. The motifs were sufficient to increase reporter gene translation and Rieske protein expression in vitro and in Setaria viridis. This light intensity-dependant, redox-regulated switch responds to pharmacological treatments that perturb photosynthesis and retrograde signaling, but not a generic abiotic stress, namely heat. It promotes the translation of photosynthesis proteins and HL-responsive transcription factors, such as Stress-associated proteins (SAPs), creating a rapidly responsive feed-forward loop to amplify known retrograde transcriptional responses, thereby reducing photoinhibition. The functional conservation of the GAPDH-motif interaction in Setaria viridis foreshadows new strategies for improving photosynthesis and expands our understanding of translational control mechanisms in response to chloroplast communication.