Retrograde Control of Cytosolic Translation Targets Synthesis of Plastid Localized Proteins and Nuclear Responses for Efficient Light Acclimation.

Canonical retrograde signaling is the transmission of information from organelles to the nucleus. Discrepancies between protein accumulation and transcript abundance in response to oxidative stress were suggestive of protein translation responding to retrograde signaling. Here we uncover multiple components of a translation-dependent retrograde signaling pathway that impact translation efficiency and gene expression, including the kinases, MPK6 and the SnRK1 subunit, AKIN10. Global ribosome foot-printing demonstrated rapid differential loading of 939 of transcripts from polyribosomes within 10 min after transfer from Low to High-light. Translationally regulated transcripts shared motifs in their 5-UTR that act as binding sites for RBPs such as GAPC. The Stress Associated Proteins 2 and 3 carry such motifs in their UTRs and interact with the calcium sensor Calmodulin-like 49, relocating to the nucleus to co-regulate a translation-dependent transcriptional response. Translation dependent retrograde signaling bifurcates into a direct translational circuit and a translation-reliant nuclear circuit synchronizing translation, nuclear and anterograde response pathways, which may serve as a just in time-provision of needed proteins to the plastids.