Abstract
RNA turnover is a general process that maintains appropriate mRNA abundance at the posttranscriptional level. Although long thought to be antagonistic to translation, discovery of the 5' to 3' cotranslational mRNA decay pathway demonstrated that both processes are intertwined. Cotranslational mRNA decay globally shapes the transcriptome in different organisms and in response to stress; however, the dynamics of this process during plant development is poorly understood. In this study, we used a multiomics approach to reveal the global landscape of cotranslational mRNA decay during Arabidopsis (Arabidopsis thaliana) seedling development. We demonstrated that cotranslational mRNA decay is regulated by developmental cues. Using the EXORIBONUCLEASE4 (XRN4) loss-of-function mutant, we showed that XRN4 poly(A+) mRNA targets are largely subject to cotranslational decay during plant development. As cotranslational mRNA decay is interconnected with translation, we also assessed its role in translation efficiency. We discovered that clusters of transcripts were specifically subjected to cotranslational decay in a developmental-dependent manner to modulate their translation efficiency. Our approach allowed the determination of a cotranslational decay efficiency that could be an alternative to other methods to assess transcript translation efficiency. Thus, our results demonstrate the prevalence of cotranslational mRNA decay in plant development and its role in translational control.
Highlights
Over its entire lifetime, any mature cytoplasmic mRNA is in balance between translation, storage and decay
Pathway, Sorenson et al used Col0 Arabidopsis complemented with a functional allele of SOV. mRNAs we find up-regulated in the absence of XRN4 here again show increased halflives in the absence of VCS despite the presence of an active SOV (Figure 4F compared Col0 to vcs-7 SOVLER)
We looked for putative cis elements shared by mRNAs we found as XRN4 cotranslational decay targets
Summary
Any mature cytoplasmic mRNA is in balance between translation, storage and decay. This equilibrium maintains the proper dynamic of gene expression and is crucial to control mRNA homeostasis. Long thought to be mutually exclusive, there is a large body of evidence supporting that, in eukaryotes, mRNA translation and decay are interconnected (Heck and Wilusz, 2018). The impact of codon optimality on mRNA halflife is a clear example of this relationship. Codon optimality is defined as the ribosome decoding efficiency according to tRNAs availability. The finding that codon optimality is a key cis determinant of transcript stability places the ribosome as a core component linking translation elongation to mRNA degradation
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