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Abstract Various messenger RNA (mRNA) decay mechanisms play major roles in controlling mRNA quality and quantity in eukaryotic organisms under different conditions. While it is known that the recently discovered co‐translational mRNA decay (CTRD), the mechanism that allows mRNAs to be degraded while still being actively translated, is prevalent in yeast, humans, and various angiosperms, the regulation of this decay mechanism is less well studied. Moreover, it is still unclear whether this decay mechanism plays any role in the regulation of specific physiological processes in eukaryotes. Here, by re‐analyzing the publicly available polysome profiling or ribosome footprinting and degradome sequencing datasets, we discovered that highly translated mRNAs tend to have lower co‐translational decay levels. Based on this finding, we then identified Pelota and Hbs1, the translation‐related ribosome rescue factors, as suppressors of co‐translational mRNA decay in Arabidopsis. Furthermore, we found that Pelota and Hbs1 null mutants have lower germination rates compared to the wild‐type plants, implying that proper regulation of co‐translational mRNA decay is essential for normal developmental processes. In total, our study provides further insights into the regulation of CTRD in Arabidopsis and demonstrates that this decay mechanism does play important roles in Arabidopsis physiological processes.
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What, where, and how: Regulation of translation and the translational landscape in plants
Abstract Translation is a crucial step in gene expression and plays a vital role in regulating various aspects of plant development and environmental responses. It is a dynamic and complex program that involves interactions between mRNAs, tRNAs, and the ribosome machinery, through both cis- and trans-regulation, while integrating internal and external signals. Translational control can act in a global (transcriptome-wide) or mRNA-specific manner. Recent advances in genome-wide techniques, particularly ribosome profiling and proteomics, have led to numerous exciting discoveries in both global and mRNA-specific translation. In this review, we aim to provide a ‘primer’ that introduces readers to this fascinating yet complex cellular process and provide a big picture of how essential components connect within the network. We begin with an overview of mRNA translation, followed by a discussion of the experimental approaches and recent findings in the field, focusing on unannotated translation events and translational control through cis-regulatory elements on mRNAs and trans-acting factors, as well as signaling networks through three conserved translational regulators TOR, SnRK1, and GCN2. Finally, we briefly touch on the spatial regulation of mRNAs in translational control. Here, we focus on cytosolic mRNAs, and translation in organelles and viruses is not covered in this review.
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- Award ID(s):
- 2051885
- PAR ID:
- 10492891
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- The Plant Cell
- ISSN:
- 1040-4651
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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SUMMARY Translation of the chloroplastpsbAmRNA in angiosperms is activated by photodamage of its gene product, the D1 subunit of photosystem II (PSII), providing nascent D1 for PSII repair. The involvement of chlorophyll in the regulatory mechanism has been suggested due to the regulatory roles of proteins proposed to mediate chlorophyll/D1 transactions and the fact that chlorophyll is synthesized only in the light in angiosperms. We used ribosome profiling and RNA‐seq to address whether the effects of light on chloroplast translation are conserved in the liverwort Marchantia (Marchantia polymorpha), which synthesizes chlorophyll in both the dark and the light. As in angiosperms, ribosome occupancy onpsbAmRNA decreased rapidly upon shifting plants to the dark and was rapidly restored upon a transfer back to the light, whereas ribosome occupancy on other chloroplast mRNAs changed very little. The results were similar in aMarchantiamutant unable to synthesize chlorophyll in the dark. Those results, in conjunction with pulse‐labeling data, suggest that light elicits a plastome‐wide activation of translation elongation and a specific increase inpsbAtranslation initiation inMarchantia, as in angiosperms. These findings show that light regulates chloroplast translation similarly in vascular and non‐vascular plants, and that constitutive chlorophyll synthesis does not affect light‐regulatedpsbAtranslation initiation. Additionally, the translational outputs of chloroplast genes are similar inMarchantiaand angiosperms but result from differing contributions of mRNA abundance and translational efficiencies. This adds to the evidence that chloroplast mRNA abundance and translational efficiencies co‐evolve under selection to maintain protein outputs.more » « less
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Abstract Decay of mRNAs can be triggered by ribosome slowdown at stretches of rare codons or positively charged amino acids. However, the full diversity of sequences that trigger co-translational mRNA decay is poorly understood. To comprehensively identify sequence motifs that trigger mRNA decay, we use a massively parallel reporter assay to measure the effect of all possible combinations of codon pairs on mRNA levels in S. cerevisiae. In addition to known mRNA-destabilizing sequences, we identify several dipeptide repeats whose translation reduces mRNA levels. These include combinations of positively charged and bulky residues, as well as proline-glycine and proline-aspartate dipeptide repeats. Genetic deletion of the ribosome collision sensor Hel2 rescues the mRNA effects of these motifs, suggesting that they trigger ribosome slowdown and activate the ribosome-associated quality control (RQC) pathway. Deep mutational scanning of an mRNA-destabilizing dipeptide repeat reveals a complex interplay between the charge, bulkiness, and location of amino acid residues in conferring mRNA instability. Finally, we show that the mRNA effects of codon pairs are predictive of the effects of endogenous sequences. Our work highlights the complexity of sequence motifs driving co-translational mRNA decay in eukaryotes, and presents a high throughput approach to dissect their requirements at the codon level.more » « less
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/plcell/koad197
