Retrograde Control of Cytosolic Translation Targets Synthesis of Plastid Proteins and Nuclear Responses for High-Light Acclimation

Abstract

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.

Oxylipins and Reactive Carbonyls as Regulators of the Plant Redox and Reactive Oxygen Species Network under Stress

“…On the other hand, GAPDH also exerts RNA binding functions, hence modulating protein synthesis [ 120 ]. RNA binding motifs of GAPDH are primarily found in high light-induced transcripts [ 131 ]. Therefore, modulation of GAPDH levels and oxidation state might help in steering protein synthesis in the direction of stress signaling and defense, similar to the induction of ORGs by interaction with Cyp20-3.…”

The mutual interaction of glycolytic enzymes and RNA in post-transcriptional regulation

“…In contrast to mammalian GAPDH, RNA-binding activity of plant or yeast glyceraldehyde 3-phosphate dehydrogenases is less understood. In 2021 only, GAPC1 and GAPC2 (plant glyceraldehyde 3-phosphate dehydrogenase) were shown to interact in vitro with a sequence motif that was overrepresented in translationally regulated transcripts in response to high light treatment ( Moore et al 2021 ). The authors hypothesize a translation-repressing function of GAPC1/C2 induced by low energy conditions.…”

Synergism and antagonism in plant acclimation to abiotic stress combinations

“…The cellular mRNA pool associated with actively translating ribosomes is termed translatome and undergoes rapid and profound reorganization upon environmental changes, e.g., upon wounding (Chen et al 2021) or following the shift of low light-acclimated plants to high light (Moore et al 2021). Only this pool is used to synthesize de novo proteins.…”