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Arabidopsis DXO1 is an evolutionarily diverged homolog that impacts translation and translation-dependent mRNA decay

ABSTRACT: The Rai1/Dxo1/DXO protein family function in eukaryotic 5′-end RNA quality control by hydrolyzing non-canonical mRNA cap structures, such as the NAD+ 5′-cap. The plant ortholog, DXO1, shows distinct biochemical properties compared to its fungal and mammalian counterparts, but only minor phenotypic differences are attributed to its NAD+-decapping (deNADding) activity. On the other hand, abnormalities in chloroplast development and growth in dxo1 mutant plants appear linked to the serine-rich N-terminal extension (NTE) of DXO1. Here, we report that plant DXO1 is a distinct ortholog that likely diverged earlier than its fungal and mammalian counterparts. We attribute this to the presence of a serine-rich N-terminal extension, which is found almost exclusively in plants and likely arose during the emergence of angiosperms. Degradome analysis revealed that Arabidopsis DXO1 contributes to translation-dependent mRNA decay, including mRNA surveillance and co-translation RNA decay, in a manner that is reliant on its serine-rich NTE. Furthermore, polysome profiling revealed that plants lacking DXO1 exhibit globally reduced translation, which may explain the loss of translation-dependent mRNA decay and changes in pre-rRNA processing. From our data, we propose that 5′-end RNA quality control by Arabidopsis DXO1 is important for translation and translation-dependent mRNA decay.

ORGANISM(S): Arabidopsis thaliana

PROVIDER: GSE285834 | GEO | 2025/10/28

REPOSITORIES: GEO

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Project description:The spliceosome is a dynamic macromolecular machine that catalyzes the removal of introns from pre-mRNA to make mature message. Schizosaccharomyces pombe Cwf10 (homolog Saccharomyces cerevisiae Snu114 and of Human U5-116K), an integral member of the U5 snRNP, is a GTPase that shares sequence homology with the eukaryotic translation elongation factor EF2. Cwf10 is required for pre-mRNA splicing; however, its mechanism(s) of action is still not understood. Cwf10/Snu114 family members contain a conserved N-terminal extension (NTE) that lacks homology with EF2 and has been predicted to be an intrinsically unfolded domain. Using S. pombe as a model system, we show that the NTE is not essential, but cells lacking this domain are defective in pre-mRNA splicing at all temperatures. Genetic interactions between cwf10-M-NM-^TNTE and other pre-mRNA splicing mutants are consistent with a role for the NTE in spliceosome activation. Characterization of Cwf10-NTE by various biophysical techniques shows the NTE contains both regions of structure and disorder in solution. The first twenty-three highly-conserved amino acids of the NTE are essential for its role in splicing, but are not sufficient to restore pre-mRNA splicing to wild-type levels in cwf10-M-bM-^HM-^FNTE cells. When the NTE is overexpressed in the cwf10-M-NM-^TNTE background, it can complement the truncated Cwf10 protein in trans, and it also immunoprecipitates a complex similar in composition to the late-stage U5.U2/U6 spliceosome. These data show that the structurally flexible NTE is capable of making specific contacts within the spliceosome that may facilitate Cwf10M-bM-^@M-^Ys overall role facilitating spliceosome rearrangements. Interrogation of the S. pombe transcriptome using poly-A enriched RNA sequencing (Illumina HiSeq 2500) in wild type and cwf10-M-NM-^TNTE cultures. A total of 4 samples were analysed: two biological repeats of wild-type strain and two biological repeats of cwf10-M-NM-^TNTE

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Arabidopsis DXO1 is an evolutionarily diverged homolog that impacts translation and translation-dependent mRNA decay

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