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EDC-3 and EDC-4 Regulate Embryonic mRNA Clearance and Biomolecular Condensate Specialization

ABSTRACT: Animal development is dictated by the selective and timely decay of mRNAs in developmental transitions, but the impact of mRNA decapping scaffold proteins in development is unknown. This study unveils the roles and interactions of the DCAP-2 decapping scaffolds EDC-3 and EDC-4 in the embryonic development of C. elegans. EDC-3 facilitates the timely removal of specific embryonic mRNAs, including cgh-1, car-1, and ifet-1 by reducing their expression, and preventing excessive accumulation of DCAP-2 condensates in somatic cells. We further uncover a novel role for EDC-3 in defining the boundaries between P-bodies, germ granules, and stress granules. Lastly, we show that EDC-4 counteracts EDC-3 and engenders the assembly of DCAP-2 with the GID (CTLH) complex, a ubiquitin ligase involved in maternal-to-zygotic transition (MZT). Our findings support a model wherein multiple RNA decay mechanisms temporally partake in the clearance of maternal and zygotic mRNAs throughout embryonic development.

ORGANISM(S): Caenorhabditis elegans

PROVIDER: GSE273136 | GEO | 2024/09/23

REPOSITORIES: GEO

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EDC-3 and EDC-4 Regulate Embryonic mRNA Clearance and Biomolecular Condensate Specialization

Project description:Animal development is dictated by the selective and timely decay of mRNAs in developmental transitions. The implication of mRNA decapping scaffold proteins in these processes was unknown. This study delineates the roles and interactions of the DCAP-2 decapping scaffolds EDC-3 and EDC-4 in the embryonic development of C. elegans. EDC-3 facilitates the timely removal of specific embryonic mRNAs, including ifet-1, car-1, and cgh-1, reducing their expression, and preventing excessive accumulation of DCAP-2 condensates in somatic cells. We further uncover a novel role for EDC-3 in defining the biochemical boundaries between P-bodies, P-granules, and stress granules. Lastly, we show that EDC-4 counteracts EDC-3 and mediates the assembly of DCAP-2 with the GID (CTLH) complex, a ubiquitin ligase involved in maternal-to-zygotic transition (MZT). Our findings refine a model wherein multiple RNA decay mechanisms temporally partake in the clearance of maternal and zygotic mRNAs throughout embryonic development.

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Expression data from mid-aged decapping mutant C. elegans nematodes

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The Cytoplasmic mRNA Decay Landscape of Arabidopsis Seedlings [RNA-seq]

Project description:Cytoplasmic mRNA decay occurs through several pathways, but the contributions of these decay pathways to the degradation of specific mRNAs, and interactions between the pathways, are not well understood. We carried out a genome-wide analysis of mRNA decay rates using wild-type Arabidopsis and mutants with defects in mRNA decapping and SOV/DIS3L2. Decay rates and contributions of decapping and SOV to decay were estimated for 18,674 mRNAs using maximum likelihood modeling. Most mRNAs decayed by multiple pathways, few mRNAs degraded exclusively by mRNA decapping or SOV, and specific codon usage was linked to decay rates. Unexpected faster decay of transcripts in some genotypes was found to be independent of siRNAs; instead the data suggested an RNA buffering-like phenomenon in Arabidopsis, and that VCS (decapping) is essential for both this process and the decay of very unstable mRNAs.

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Project description:mRNA decay factors regulate mRNA turnover by recruiting non-translating mRNAs and targeting them for degradation, yet it remains poorly understood how mRNA decay factors function in vivo to regulate specific cellular processes. Here we show that mRNA decay factors form cytoplasmic puncta in C. elegans neurons and have opposing roles in axon maintenance and regrowth. While the decapping enzymes DCAP-1/DCP1 and DCAP-2/DCP2 regulate developmental axon guidance and promote axon regrowth upon injury, the translational repressors CAR-1/LSM14 and CGH-1/DDX6 regulate axon maintenance and inhibit axon regrowth in adult animals. We identified mRNA targets of CAR-1 in neurons and found that the mitochondrial calcium uptake regulator micu-1 is repressed by CAR-1. We show that axon injury triggers a transient mitochondrial calcium influx via the MCU-1 uniporter that is more sustained in car-1 loss of function mutants. The enhanced axon regrowth and defective axon maintenance of car-1 mutants are dependent on MICU-1 function. Our results uncover specific roles for mRNA decay regulators in neurons and reveal a novel pathway that controls axon regrowth through mitochondrial calcium uptake.

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Project description:Uridylation is a widespread modification destabilizing eukaryotic mRNAs. Yet, molecular mechanisms underlying TUTase-mediated mRNA degradation remain mostly unresolved. Here, we report that the Arabidopsis TUTase URT1 participates in a molecular network connecting several translational repressors/decapping activators including DECAPPING 5 (DCP5), the Arabidopsis ortholog of human LSM14 and yeast Scd6. A conserved Helical Leucine-rich Motif (HLM) within an intrinsically disordered region of URT1 binds to the LSm domain of DCP5. This interaction connects URT1 to additional decay factors like DDX6/Dhh1-like RNA helicases. The combination of in planta and in vitro analyses supports a model that explains how URT1 reduces the accumulation of oligo(A)-tailed mRNAs: first, by connecting decapping factors and second, because 3’ terminal uridines can intrinsically hinder deadenylation. Importantly, preventing the accumulation of excessively deadenylated mRNAs in Arabidopsis avoids the biogenesis of illegitimate siRNAs that silence endogenous mRNAs and perturb plant growth and development.

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EDC-3 and EDC-4 Regulate Embryonic mRNA Clearance and Biomolecular Condensate Specialization

Project description:EDC-3 and EDC-4 Regulate Embryonic mRNA Clearance and Biomolecular Condensate Specialization

| PRJNA1140226 | ENA

Global analysis of mRNA decay intermediates in Saccharomyces cerevisiae

Project description:The general pathways of eukaryotic mRNA decay occur via deadenylation followed by 3’ to 5’ degradation or decapping, although some endonuclease sites have been identified in metazoan mRNAs. To determine the role of endonucleases in mRNA degradation in Saccharomyces cerevisiae, we mapped 5’ monophosphate ends on mRNAs in wild-type and dcp2∆ xrn1∆ yeast cells, wherein mRNA endonuclease cleavage products are stabilized. This led to three important observations. First, only few mRNAs that undergo low level endonucleotyic cleavage were observed suggesting that endonucleases are not a major contributor to yeast mRNA decay. Second, independent of known decapping enzymes, we observed low levels of 5’ monophosphates on some mRNAs suggesting that an unknown mechanism can generate 5' exposed ends, although for all substrates tested Dcp2 was the primary decapping enzyme. Finally, we identified debranched lariat intermediates from intron-containing genes, demonstrating a significant discard pathway for mRNAs during the second step of pre-mRNA splicing, which is a potential new step to regulate gene expression. 5' monophosphorylated ends of poly(A) RNA from wild-type and dcp2D xrn1D strains were identified in duplicates and triplicates, respectively.

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The TUTase URT1 connects decapping activators and prevents the accumulation of excessively deadenylated mRNAs to avoid siRNA biogenesis

Project description:Uridylation is a widespread modification destabilizing eukaryotic mRNAs. Yet, molecular mechanisms underlying TUTase-mediated mRNA degradation remain mostly unresolved. Here, we report that the Arabidopsis TUTase URT1 participates in a molecular network connecting several translational repressors/decapping activators. URT1 directly interacts with DECAPPING 5 (DCP5), the Arabidopsis ortholog of human LSM14 and yeast Scd6, and this interaction connects URT1 to additional decay factors like DDX6/Dhh1-like RNA helicases. Nanopore direct RNA sequencing reveals a global role of URT1 in shaping poly(A) tail length, notably by preventing the accumulation of excessively deadenylated mRNAs. Based on in vitro and in planta data, we propose a model that explains how URT1 could reduce the accumulation of oligo(A)-tailed mRNAs both by favoring their degradation and because 3’ terminal uridines intrinsically hinder deadenylation. Importantly, preventing the accumulation of excessively deadenylated mRNAs avoids the biogenesis of illegitimate siRNAs that silence endogenous mRNAs and perturb Arabidopsis growth and development.

2020-12-01 | PXD022676 | Pride

Decapped mRNAs during Arabidopsis Early Flower Development

Project description:The composition of the transcriptome is regulated by both mRNA synthesis and degradation. One route for mRNA decay is through 5’ decapping, which can be initiated by decapping enzymes and small RNAs. Although decapped RNAs are an important intermediate for mRNA decay, their identity and abundance have never been studied on a large scale. Here we present an experimental method for transcriptome-wide profiling of decapped mRNAs. We applied the method to study the prevalence of decapped transcripts during the early stages of Arabidopsis thaliana flower development. Decapped transcripts were identified for the majority of expressed genes, although at different levels. By comparing decapped RNA levels with steady-state overall transcript levels, our study provides evidence for widespread decapping-mediated mRNA degradation control in numerous biological processes and for genes of varied molecular functions, implying that mRNA decapping is a dynamically regulated process. Sequence analyses identified structural features of transcripts and cis-elements that were associated with levels of decapping. Four sets of biologically independent tissue samples were collect 0,1,2,3,4, and 5 days after activation of the AP1-GR fusion protein. Decapped mRNA and total mRNA of each time point from each set were co-hybridized to micoarrays. Dyes used for labeling the RNA populations derived from the individual samples were switched in the replicate experiments to reduce dye-related artefacts.

2008-10-10 | E-GEOD-12043 | biostudies-arrayexpress

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