RNA Helicases from the DEA(D/H)-Box Family Contribute to Plant NMD Efficiency

Sulkowska, Aleksandra; Auber, Andor; Sikorski, Pawel J.; Silhavy, Dï Niel; Auth, Mariann; Sitkiewicz, Ewa; Jean, Viviane; Merret, Rémy; Bousquet-Antonelli, Cï Cile; Kufel, Joanna

doi:10.1093/pcp/pcz186

“…Thus, UPF1 may directly affect homeostasis of splicing factors on transcribed RNA and influence splicing efficiency. Proteomic data suggesting an association between splicing factors and UPF1 also hint at a more intimate connection between splicing and NMD in Arabidopsis (Sulkowska et al 2019).…”

Section: Discussionmentioning

confidence: 97%

Nonsense-Mediated RNA Decay Factor UPF1 Is Critical for Posttranscriptional and Translational Gene Regulation in Arabidopsis

Raxwal

¹

,

Simpson

²

,

Gloggnitzer

³

et al. 2020

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Nonsense mediated RNA decay (NMD) is an evolutionary conserved RNA control mechanism that has also been implicated in the broader regulation of gene expression. Nevertheless, a role for NMD in genome regulation has not been fully assessed, partially because NMD inactivation is lethal in many organisms. Here, we performed in depth comparative analysis of Arabidopsis mutants lacking key proteins involved in different steps of NMD. We observed that UPF3, UPF1, and SMG7 have different impacts on NMD and the Arabidopsis transcriptome, with UPF1 having the biggest effect. Transcriptome assembly using stringent pipeline in UPF1-null plants revealed genome wide changes in alternative splicing, including switches in mRNA variants, suggesting a role for UPF1 in splicing. We further found that UPF1 inactivation leads to translational repression, manifested by a global shift in mRNAs from polysomes to monosomes and a downregulation of genes involved in translation and ribosome biogenesis. Despite this global change, NMD targets and low-expressed mRNAs with short half-lives were enriched in polysomes, indicating that UPF1 specifically suppresses the translation of aberrant RNAs. Particularly striking was an increase in the translation of TIR domain-containing, nucleotide-binding, leucine-rich repeat (TNL) immune receptors. The regulation of TNLs via UPF1/NMD-mediated mRNA stability and translational derepression offers a dynamic mechanism for the rapid activation of TNLs in response to pathogen attack..

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“…Thus, UPF1 may directly affect homeostasis of splicing factors on transcribed RNA and influence splicing efficiency. Proteomic data suggesting an association between splicing factors and UPF1 also hint at a more intimate connection between splicing and NMD in Arabidopsis (Sulkowska et al 2019). mRNAs processed by NMD become translationally repressed through UPF1-mediated inhibition of translation initiation (Isken et al 2008).…”

Section: Discussionmentioning

confidence: 99%

Nonsense mediated RNA decay factor UPF1 is critical for post-transcriptional and translational gene regulation in Arabidopsis

Raxwal

¹

,

Simpson

²

,

Gloggnitzer

³

et al. 2020

Preprint

View full text Add to dashboard Cite

Nonsense mediated RNA decay (NMD) is an evolutionary conserved RNA control mechanism that has also been implicated in the broader regulation of gene expression. Nevertheless, a role for NMD in genome regulation has not been fully assessed, partially because NMD inactivation is lethal in many organisms. Here, we performed in depth comparative analysis of Arabidopsis mutants lacking key proteins involved in different steps of NMD. We observed that UPF3, UPF1, and SMG7 have different impacts on NMD and the Arabidopsis transcriptome, with UPF1 having the biggest effect. Transcriptome assembly using stringent pipeline in UPF1-null plants revealed genome wide changes in alternative splicing, including switches in mRNA variants, suggesting a role for UPF1 in splicing. We further found that UPF1 inactivation leads to translational repression, manifested by a global shift in mRNAs from polysomes to monosomes and a downregulation of genes involved in translation and ribosome biogenesis. Despite this global change, NMD targets and low-expressed mRNAs with short half-lives were enriched in polysomes, indicating that UPF1 specifically suppresses the translation of aberrant RNAs. Particularly striking was an increase in the translation of TIR domain-containing, nucleotide-binding, leucine-rich repeat (TNL) immune receptors. The regulation of TNLs via UPF1/NMD-mediated mRNA stability and translational derepression offers a dynamic mechanism for the rapid activation of TNLs in response to pathogen attack.

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“…The NMD mechanism requires three Upf proteins (UPF1 to UPF3), SMG1 and SMG7, and a helicase distantly related to eIF4A, eIF4A III (Ohtani & Wachter, 2019; Poidevin, Unal, Belda‐Palazon, & Ferrando, 2019). NMD is further stimulated by other accessory proteins such as the helicase DDX6 (RH12) (Sulkowska et al, 2019).…”

Section: The Plant Translation Apparatusmentioning

confidence: 99%

Translational gene regulation in plants: A green new deal

Camacho

¹

,

Lokdarshi

²

,

Arnim

³

2020

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The molecular machinery for protein synthesis is profoundly similar between plants and other eukaryotes. Mechanisms of translational gene regulation are embedded into the broader network of RNA-level processes including RNA quality control and RNA turnover. However, over eons of their separate history, plants acquired new components, dropped others, and generally evolved an alternate way of making the parts list of protein synthesis work. Research over the past 5 years has unveiled how plants utilize translational control to defend themselves against viruses, regulate translation in response to metabolites, and reversibly adjust translation to a wide variety of environmental parameters. Moreover, during seed and pollen development plants make use of RNA granules and other translational controls to underpin developmental transitions between quiescent and metabolically active stages. The economics of resource allocation over the daily light-dark cycle also include controls over cellular protein synthesis. Important new insights into translational control on cytosolic ribosomes continue to emerge from studies of translational control mechanisms in viruses. Finally, sketches of coherent signaling pathways that connect external stimuli with a translational response are emerging, anchored in part around TOR and GCN2 kinase signaling networks. These again reveal some mechanisms that are familiar and others that are different from other eukaryotes, motivating deeper studies on translational control in plants.

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RNA Helicases from the DEA(D/H)-Box Family Contribute to Plant NMD Efficiency

Cited by 15 publications

References 87 publications

Nonsense-Mediated RNA Decay Factor UPF1 Is Critical for Posttranscriptional and Translational Gene Regulation in Arabidopsis

Nonsense-Mediated RNA Decay Factor UPF1 Is Critical for Posttranscriptional and Translational Gene Regulation in Arabidopsis

Nonsense mediated RNA decay factor UPF1 is critical for post-transcriptional and translational gene regulation in Arabidopsis

Translational gene regulation in plants: A green new deal

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