Decapping activators Edc3 and Scd6 act redundantly with Dhh1 in post-transcriptional repression of starvation-induced pathways

Degradation of mRNA is a key aspect of gene expression that can be regulated in response to nutrient availability, cell stress, and developmental pathways in eukaryotic cells and further serves to eliminate defective mRNAs. A major pathway of cytoplasmic mRNA turnover involves truncating the poly(A) tail by the Ccr4/Not and Pan2/Pan3 complexes, followed by removal of the m⁷G cap by the Dcp1/Dcp2 decapping complex and 5’ to 3’ exonucleolytic degradation by Xrn1. The decapping complex is activated by factors that interact with low-complexity sequence motifs in the C-terminal tail (CTT) of the catalytic subunit Dcp2, including Edc3, Scd6, DEAD-box helicase Dhh1, and Pat1, which also interact with one another extensively. There is evidence that Pat1 is recruited to oligoadenylate tails remaining on mRNAs following partial deadenylation, in association with the Lsm1-Lsm7 complex, and activates decapping via interactions with other decapping activators and with the Dcp2 CTT itself (Parker, 2012; He and Jacobson, 2023).

Genome-wide analysis of mRNA abundance (RNA-seq) in yeast mutants lacking Dhh1, Pat1, or both factors revealed functional cooperation by Pat1 and Dhh1 (He et al., 2018), with a large fraction being up-regulated only in the pat1∆dhh1∆ double mutant (Vijjamarri et al., 2023a). The majority of mRNAs up-regulated by dhh1∆ or pat1∆ mutations are likewise up-regulated in dcp2∆ cells (He et al., 2018) and exhibit greater than average proportions of decapped mRNAs in WT cells but not in dhh1∆ or pat1∆ cells (Vijjamarri et al., 2023a), consistent with Dhh1/Pat1 targeting mRNAs for degradation via decapping. While more than half of the mRNAs up-regulated by dcp2∆ are up-regulated by dhh1∆ and/or pat1∆, a large fraction are targeted primarily by the Upf factors instead, responsible for nonsense-mediated mRNA decay (NMD) (Vijjamarri et al., 2023b; Celik et al., 2017).

The cumulative contributions of Dhh1 and Pat1 to mRNA decay is consistent with their independent interactions with distinct segments of the Dcp2 CTT (He et al., 2018), which appears to be direct for Pat1 but bridged by Edc3 or Scd6 for Dhh1. There is also evidence for distinct decapping complexes containing either Dhh1 or Pat1 in addition to Xrn1, Edc3, or Scd6 (He et al., 2022). However, Dhh1 occupancy (Miller et al., 2018), tends to be elevated for mRNAs up-regulated by either dhh1∆ (23) or pat1∆ (Vijjamarri et al., 2023a), consistent with Dhh1 contributing to degradation of mRNAs targeted by Pat1. Moreover, Pat1 binding to the Dcp2 CTT was required for degradation of certain Dhh1-targeted mRNAs when Dhh1 recruitment to the CTT was compromised (He et al., 2022).

There is evidence that Edc3 is a common constituent of decapping complexes containing Xrn1 and one or more of the decapping activators Dhh1, Pat1, Scd6, and Upf1 (He et al., 2022). It is surprising, therefore, that Edc3 has been implicated in targeting only two transcripts for degradation, YRA1 and RPS28B (Badis et al., 2004; Dong et al., 2007). Edc3 shares sequence similarity with decapping activator Scd6 and both proteins contain an FDF motif shown to interact competitively with the Dhh1 homolog in animal systems (Tritschler et al., 2008; Tritschler et al., 2009). Edc3 and Scd6 also share N-terminal LSm domains that compete for binding to helical-leucine-rich (HLM) motifs in the CTT of fission yeast Dcp2 (Fromm et al., 2012). Analyzing effects of deleting the Edc3 interaction site in the S. cerevisiae Dcp2-CTT on levels of several Dhh1-repressed mRNAs suggested that recruitment of Dhh1 to Dcp2 can be mediated interchangeably by Edc3 or Scd6 bound to the same site in the Dcp2 CTT (He et al., 2022). These findings, plus the fact that deleting S. cerevisiae SCD6 and EDC3 simultaneously confers a synthetic growth defect (Decourty et al., 2008), suggest that yeast Scd6 and Edc3 function redundantly in targeting specific mRNAs for decapping and degradation.

Although tethering yeast Dhh1 or Scd6 enhances degradation of reporter mRNAs via Dcp1/Dcp2 (Carroll et al., 2011; Sweet et al., 2012; Zeidan et al., 2018), it is not well understood how these factors are targeted to specific native mRNAs. Dhh1 has been implicated in accelerating degradation associated with non-optimal codons in yeast mRNAs (Presnyak et al., 2015), being required for the rapid turnover conferred by suboptimal codons inserted in reporter mRNAs (Sweet et al., 2012). A queue of slowly elongating ribosomes upstream from non-optimal codons can be recognized by Dhh1, and overexpressing or tethering Dhh1 evokes ribosome stalling at non-optimal codons. Moreover, Dhh1 association and Dhh1-dependent repression of mRNA abundance both correlate with codon non-optimality across the yeast transcriptome (Radhakrishnan et al., 2016). However, the mRNAs most highly up-regulated in dhh1∆ and pat1∆ cells are not enriched for suboptimal codons, suggesting that other features are responsible for their preferential targeting by Dhh1 or Pat1 for decapping/decay (Vijjamarri et al., 2023a).

In addition to enhancing mRNA decay, there is evidence that Pat1, Dhh1, and Scd6 can repress translation. Tethering Dhh1 or Scd6 represses translation of reporter mRNAs in dcp2∆ cells, where the tethered transcripts cannot be decapped and degraded (Carroll et al., 2011; Sweet et al., 2012; Zeidan et al., 2018). Deletion of Dhh1 and Pat1 simultaneously eliminated loss of bulk polysomes evoked by nutrient starvation and also increased initiation rates of certain mRNAs (Holmes et al., 2004; Coller and Parker, 2005; Arribere et al., 2011). Supporting a direct role in repressing translation, overexpressing Dhh1 or Pat1 in non-starved cells evoked polysome disassembly and reduced the initiation rate of specific mRNAs; and addition of Dhh1 (Coller and Parker, 2005) or N-terminally truncated Pat1 (Nissan et al., 2010) to yeast extracts inhibited bulk translation and 48 S preinitiation complex (PIC) assembly in vitro. Ribosome profiling studies of dhh1Δ, pat1Δ and pat1Δdhh1Δ mutants identified hundreds of genes whose transcripts are translationally down-regulated or activated by Dhh1 or Pat1 in nutrient-replete cells (Jungfleisch et al., 2017; Radhakrishnan et al., 2016; Zeidan et al., 2018), which frequently involves cooperation between Dhh1 and Pat1 (Vijjamarri et al., 2023a).

Recently, we showed that Pat1 and Dhh1 function with the decapping enzyme in rich medium to repress the abundance or translation of numerous mRNAs encoding proteins required specifically in media containing an alternative carbon or nitrogen source (Vijjamarri et al., 2023a; Vijjamarri et al., 2023b). These include mitochondrial proteins involved in oxidative phosphorylation (Ox. Phos.) and diverse other proteins known to be transcriptionally repressed by carbon or nitrogen catabolite repression in rich medium.

In this study, we used a multi-omics approach to determine whether Edc3 and Scd6 have largely redundant functions in targeting mRNAs for decapping and attendant degradation, and whether they functionally cooperate with Pat1 or Dhh1 in repressing the abundance or translation of specific mRNAs. We identified a large cohort of mRNAs that are up-regulated in an scd6Δedc3Δ double mutant but not in either single mutant lacking only Scd6 or Edc3, without a commensurate increase in transcription of the cognate genes. These transcripts display a strikingly similar pattern of up-regulation in the dhh1Δ mutant in the manner predicted if Edc3/Scd6 redundantly recruit Dhh1 to Dcp2 for activation of decapping (He et al., 2022). We further observed functional redundancy between Scd6 and Edc3 and extensive cooperation with Dhh1/Pat1 in repressing translation of particular mRNAs, with evidence for interdependent repression by all four decapping factors. Importantly, Edc3/Scd6 contribute to post-transcriptional repression of proteins required for catabolism of non-preferred carbon or nitrogen sources on rich medium, acting collectively to enhance glucose repression, maintain low-level mitochondrial electron transport, and reduce levels of tricarboxylic acid (TCA) and glyoxylate cycle intermediates in glucose-replete cells.

RNA-seq analysis of single and double scd6Δ and edc3Δ mutants has revealed that Scd6 and Edc3 have largely overlapping functions in repressing mRNA abundance, as the presence of either protein alone is sufficient for nearly WT levels of most mRNAs found up-regulated in the double mutant (Figure 1—figure supplement 3A and Figure 1B–C(ii–iii)). Although the mRNAs dysregulated in the scd6Δedc3Δ mutant are enriched for ESR mRNAs; the majority are not ESR transcripts (Figure 1A–B) and are most likely repressed more directly by Scd6/Edc3. Functional redundancy of Scd6/Edc3 is consistent with their similarities in sequence and domain structure, including shared FDF motifs that interact competitively with Dhh1 in animals (Tritschler et al., 2008; Tritschler et al., 2009) and N-terminal LSm domains that compete for binding motifs in the Dcp2 CTT of S. pombe (Fromm et al., 2012), as well as the synthetic growth defect produced by deleting both genes simultaneously (Decourty et al., 2008; Figure 1—figure supplement 1A). Interestingly, a set of 37 mRNAs appears to be repressed by Edc3 exclusively (Figure 1B–C(i)), including the canonical Edc3 targets identified previously, YRA1 and RPS28B (He et al., 2022), and is enriched for genes belonging to the GO category ‘mitochondrion’ (22/37 genes) and the Ox. Phos. categories of electron transport and mitochondrial ATP synthesis (11/37 genes: ATP3 ATP16 ATP5 TIM11 ATP17 COX4 QCR9 CYC1 COX12 ATP18 COX5A). The fact that deleting SCD6 in the double mutant frequently diminishes the up-regulation of these transcripts conferred by deleting EDC3 alone (Figure 1C(i)) might indicate that eliminating both Scd6 and Edc3 together enables a distinct degradation pathway that compensates for loss of Edc3-stimulated decapping/decay.

Several lines of evidence support the conclusion that most of the changes in mRNA abundance in the scd6Δedc3Δ double mutant result from impaired decapping and attendant 5’–3’ degradation by Xrn1. ChIP-seq analysis of Rpb1 shows that Pol II occupancies in the coding sequences increase by much smaller amounts compared to the increased transcript levels for non-iESR mRNAs up-regulated in scd6Δ/edc3Δ cells (Figure 3E), indicating a minor contribution of increased transcription to their up-regulation. The transcriptional activators of Ox-Phos. and CCR genes, many of whose transcripts are up-regulated by scd6Δ/edc3Δ, remain largely inert in this mutant, ruling out inappropriate transcriptional induction of their target genes in glucose-replete scd6Δ/edc3Δ cells. Consistent with mRNA turnover via decapping, most of these transcripts are up-regulated similarly by scd6Δedc3Δ and deletion of DCP2 (Figure 3A–B), exhibit a heightened proportion of decapped isoforms in WT cells that is diminished by deleting SCD6/EDC3 or DHH1 (Figure 3C and Figure 1—figure supplement 3E), and show evidence of co-translational 5’–3’ decay of decapped intermediates by Xrn1 (Figure 3D); none of which was observed for the mRNAs down-regulated in scd6Δ/edc3Δ cells. Similar findings were reported previously for sets of mRNAs up-regulated by dhh1Δ or pat1Δ (Vijjamarri et al., 2023a), consistent with the widespread involvement of Dhh1 and Pat1 in controlling the levels of mRNAs preferentially targeted by Scd6/Edc3.

Supporting this last assertion, most (~70%) of the mRNAs repressed in abundance by Edc3/Scd6 are also repressed by Dhh1 and Pat1, and their efficient repression in WT cells involves independent contributions of similar magnitude by Pat1, Dhh1, and either Edc3 or Scd6 (Figure 2A–B(ii)). Another large set of mRNAs is repressed predominantly by Pat1 with lesser contributions by Dhh1 and Scd6/Edc3 (Figure 2A–B(iii)). Our finding of extensive cooperation among these four decapping factors is consistent with our recent finding that ~55% of the mRNAs up-regulated in the dcp2∆ mutant, and thus targeted by Dcp2 for enhanced degradation, tend to be up-regulated in the pat1∆dhh1∆ and scd6∆edc3∆ mutants, whereas the remaining 45% are generally up-regulated by upf1∆ instead. This finding suggested a major bifurcation of Dcp2 activation by either Pat1/Dhh1/Scd6/Edc3 or the Upf factors responsible for NMD (Vijjamarri et al., 2023b).

Closer examination of the effects of individual mutations on mRNA levels revealed a greater overlap between the mRNAs dysregulated by dhh1Δ and scd6Δ/edc3Δ versus those altered by pat1Δ (Figure 2C–E), consistent with the aforementioned FDF motifs in Scd6 and Edc3 that interact with Dhh1 in animal systems, and with evidence for distinct complexes of the decapping enzyme containing Dhh1 and Edc3 or Scd6 but lacking Pat1. It also supports the recent suggestion that Edc3 and Scd6 act interchangeably to recruit Dhh1 to the Edc3-interaction site in the Dcp2 CTT to stimulate turnover of several Dhh1 target mRNAs (He et al., 2022). Our RNA-seq results support this last proposal in showing that all four Dhh1 target mRNAs examined in that study (EDC1, SDS23, HXT6, and HSP12) are up-regulated in the scd6∆edc3∆ double mutant while changing little in the single mutants (Figure 6—figure supplement 3), two of which (SDS23 and HXT6) were shown previously to have longer half-lives in dhh1∆ vs. WT cells (He et al., 2018). Finding that selective up-regulation in the scd6∆edc3∆ double mutant applies to most mRNAs up-regulated in dhh1∆ cells (Figure 2E), we propose that redundant Scd6/Edc3 targeting is a widespread mechanism of Dhh1-enhanced mRNA degradation in the yeast transcriptome (Figure 8—figure supplement 1). Supporting this, our co-immunoprecipitation analysis revealed diminished Dhh1-Dcp2 association in cell extracts of the scd6Δedc3Δ double mutant but not for either single mutant (Figure 3F).

Examining our Ribo-Seq and TMT-MS data suggests that DHH1 mRNA translation and steady-state abundance are increased ~ twofold in the scd6∆edc3∆ strain, indicating that up-regulation of many of the same mRNAs by scd6∆edc3∆ and dhh1∆ does not result indirectly from reduced levels of Dhh1 in the scd6∆edc3∆ mutant. The increased Dhh1 expression might signify a compensatory response to the absence of Scd6/Edc3. We also observed an ~40% reduction in Dcp2 translation and abundance in the scd6∆edc3∆ strain, which might contribute to the up-regulation of mRNAs dysregulated in this mutant. However, our immunoblot analyses revealed no significant reduction in steady-state Dcp2 levels in scd6∆edc3∆ cells (Input lanes in Figure 3F, Figure 3—figure supplement 2(i–ii)). Moreover, our previous finding that the majority of mRNAs subject to NMD, up-regulated by both upf1∆ and dcp2∆, are not up-regulated by scd6∆edc3∆ (Vijjamarri et al., 2023b) implies that Dcp2 abundance in scd6∆edc3∆ cells is adequate for normal levels of NMD. Accordingly, we favor a direct role for Scd6/Edc3 in accelerating degradation of most transcripts up-regulated in the scd6∆edc3∆ mutant.

Despite strong evidence for the involvement of decapping in mRNA turnover directed by either Scd6/Edc3 or Pat1/Dhh1, it appears that neither enrichment for non-optimal codons nor low translational efficiencies are principal determinants of preferential targeting of mRNAs by these proteins (Figure 3—figure supplement 3A–C). There are probably exceptions to these generalizations among the hundreds of transcripts repressed by these factors; nor can we rule out the involvement of clusters of non-optimal codons in transcripts of average overall codon optimality that generate a queue of slowly elongating ribosomes that triggers decapping. Nevertheless, it seems likely that other sequences or properties of the transcripts most strongly repressed by Scd6/Edc3 or Dhh1/Pat1 frequently underlie their preferential targeting by these factors for decapping/decay. Sequence-specific RNA-binding proteins that actively recruit these decapping activators is an attractive potential mechanism (Figure 8—figure supplement 1). For example, there is evidence that Dhh1 is recruited to mRNAs in association with the Ccr4-NOT deadenylase via RNA-binding protein Puf5 (Goldstrohm et al., 2006). Involvement of RNA-binding proteins would also be consistent with the observed specific targeting of mRNAs whose expression is repressed in response to nutrient abundance.

Ribosome profiling of the single and double scd6Δ and edc3Δ mutants provided evidence that Scd6 and Edc3 also have highly overlapping functions in repressing the translation of ~200 mRNAs, whose TE values are up-regulated substantially only in the double mutant (Figure 4A–B(iii)). The observation that changes in TE (RPF density) generally correlate with changes in protein abundance conferred by scd6Δedc3Δ (Figure 4F) implies that Scd6/Edc3 generally repress translation at the stage of initiation rather than elongation. Many mRNAs translationally repressed by Scd6/Edc3 additionally require Dhh1, and the subset most strongly repressed also requires Pat1 for efficient translational repression (Figure 5B(ii) and D). This last group of mRNAs is translated at very low levels in WT cells on rich medium (Figure 5—figure supplement 1C, cols. 2 & 4), which might reflect the concerted action of all four decapping activators in suppressing translation. The transcript abundance of these mRNAs is also up-regulated in each of the mutants (Figure 5—figure supplement 1A(ii)), indicating enhanced degradation coupled with translational repression by the four decapping activators. One possibility is that a complex of Dcp1:Dcp2 containing Scd6/Edc3, Pat1/Dhh1, or different combinations of these factors (He et al., 2022) is recruited to these mRNAs and impedes recruitment of PICs to diminish translation in parallel with stimulating decapping and 5’–3’ degradation by Xrn1 (Figure 8—figure supplement 1).

The additional sets of mRNAs identified here that are translationally repressed exclusively by Scd6/Edc3 or Pat1/Dhh1 (Figure 5A(i) and (iii)) show much less evidence of transcript degradation promoted by these factors (Figure 5—figure supplement 1A(i) and (iii)), suggesting that inhibition of translation initiation occurs without decapping or involves decapping uncoupled from degradation by Xrn1 (Figure 8—figure supplement 1(ii–iii)). In the latter scenario, the decapped mRNAs would be unable to recruit the cap-binding initiation factors necessary for PIC recruitment and hence persist in WT cells as translationally inert degradation intermediates. Eliminating the decapping activators would diminish decapping and eliminate these fractions of poorly translated uncapped isoforms to confer the increased TE values we observed for the cognate genes in the decapping mutants. This hypothetical mechanism of translational repression via decapping is consistent with the lower than average capped to total mRNA (C/T) ratios found in WT cells for the mRNAs translationally repressed by all four decapping activators or by Pat1/Dhh1 (Figure 5—figure supplement 1D(ii–iii)), indicating accumulation of decapped isoforms in WT cells, as observed previously for a subset of mRNAs translationally repressed by Dhh1 (Vijjamarri et al., 2023b). In contrast, the mRNAs that are translationally repressed exclusively by Scd6/Edc3 display higher than average C/T ratios in WT (Figure 5—figure supplement 1D(i)), which is more compatible with an inhibition of PIC recruitment independently of decapping (Figure 8—figure supplement 1(iii)). Translational repression without decapping could also occur if transcripts bound by decapping complexes are sequestered from the translation initiation machinery in RNA granules where mRNA decapping occurs inefficiently (Figure 8—figure supplement 1(iv)). Finally, it is important to note that mRNA decay occurs apparently without translational control for the much larger groups of ~600 and ~1000 transcripts showing up-regulated mRNA abundance but little evidence of TE changes in the scd6∆edc3∆ and pat1∆dhh1∆ mutants, respectively (Figure 5—figure supplement 1B). It is unclear whether these mRNAs escape translational repression and are targeted exclusively for decapping/degradation (Figure 8—figure supplement 1(i)) or are simply degraded too fast to allow translational repression to be detected by ribosomal profiling of steady-state mRNAs.

Recently, we reported that Pat1 and Dhh1 functionally collaborate with the decapping enzyme to repress genes and cellular pathways normally repressed in rich medium (Vijjamarri et al., 2023a; Vijjamarri et al., 2023b). Here, we found evidence that Scd6 and Edc3 broadly cooperate with Pat1/Dhh1 in this control, acting redundantly to repress the abundance, translation, or both, of mRNAs encoding numerous proteins involved in respiration or utilization of alternative carbon sources (Figure 6A–C, Figure 6—figure supplement 1A–D), without affecting transcription of the cognate genes (Figure 6F, Figure 6—figure supplement 2A–C). Evidence that up-regulation of Ox. Phos. mRNAs/proteins in the scd6∆edc3∆ mutant is sufficient to increase respiration in glucose-replete cells came from our findings of increased mitochondrially-encoded subunit II of ETC component cytochrome c oxidase (Figure 6D) and elevated mitochondrial membrane potential (Figure 6G) in the scd6∆edc3∆ mutant, extending similar findings we made previously for dcp2∆, dhh1∆, and pat1∆ mutants (Vijjamarri et al., 2023a; Vijjamarri et al., 2023b). Consistent with this, our metabolomics analysis revealed elevated steady-state levels of TCA cycle intermediates in all four decapping mutants (Figure 7D), and increased ¹³C carbon incorporation from ¹³C₆-glucose breakdown into TCA cycle intermediates in the same mutant strains (Figure 8A). Analysis of ATP levels further revealed increased proportions of ATP derived from Ox. Phos. in the decapping mutants (Figure 8C), which together provide strong evidence that mitochondrial respiration is inappropriately elevated in glucose-replete cells of decapping activator mutants. It is well established that the enzymes involved in respiration and catabolism of non-glucose carbon sources are repressed at the transcriptional level in glucose-replete yeast (Zaman et al., 2008). Our findings demonstrate that Scd6/Edc3 collaborate with Dhh1/Pat1 to provide an additional layer of post-transcriptional control of these enzymes through enhanced decapping/decay or translational repression to help ensure their complete suppression when glucose is abundant (Figure 8—figure supplement 1).

Ribosome profiling, RNA-Seq, ChIP-Seq and CAGE-Seq data discussed in this publication have been deposited in NCBI's Gene Expression Omnibus and are accessible through GEO Series accession numbers GSE270789 and GSE270790. TMT-MS/MS raw proteomics data for all expressed proteins have been deposited in ProteomeXchange with accession number PXD053307. All other data generated or analyzed during this study are included in the manuscript and supporting files; source data files have been provided for all figures.

1. 1. Kumar R
   2. Zhang F
   3. Vijjamarri AK
   4. Hinnebusch AG

   (2024) NCBI Gene Expression Omnibus

   ID GSE270790. Decapping activators Edc3 and Scd6 act redundantly with Dhh1 in nutrient-replete cells to post-transcriptionally repress starvation-induced pathways [Ribo and RNA-seq].

   https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE270790
2. 1. Kumar R
   2. Zhang F
   3. Vijjamarri AK
   4. Hinnebusch AG

   (2024) ProteomeXchange

   ID PXD053307. Decapping activators Edc3 and Scd6 act redundantly with Dhh1 in nutrient-replete cells to post-transcriptionally repress starvation-induced pathways.

   https://proteomecentral.proteomexchange.org/cgi/GetDataset?ID=PXD053307
3. 1. Kumar R
   2. Zhang F
   3. Vijjamarri AK
   4. Hinnebusch AG

   (2024) NCBI Gene Expression Omnibus

   ID GSE270789. Decapping activators Edc3 and Scd6 act redundantly with Dhh1 in nutrient-replete cells to post-transcriptionally repress starvation-induced pathways [ChIP-seq].

   https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE270789

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   2. Niu X
   3. Zhang F
   4. Qiu H
   5. Gupta N
   6. Lin Z
   7. Hinnebusch AG

   (2023) NCBI Gene Expression Omnibus

   ID GSE220578. Decapping factor Dcp2 controls mRNA abundance and translation to adjust metabolism and filamentation to nutrient availability II.

   https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE220578
2. 1. Vijjamarri AK
   2. Niu X
   3. Zhang F
   4. Qiu H
   5. Gupta N
   6. Lin Z
   7. Hinnebusch AG

   (2023) NCBI Gene Expression Omnibus

   ID GSE216831. Decapping factor Dcp2 controls mRNA abundance and translation to adjust metabolism and filamentation to nutrient availability.

   https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE216831
3. 1. Vijjamarri AK
   2. Gupta N
   3. Niu X
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   (2023) NCBI Gene Expression Omnibus

   ID GSE224774. mRNA decapping activators Pat1 and Dhh1 regulate transcript abundance and translation to tune cellular responses to nutrient availability.

   https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE224774
4. 1. Zhang F
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   ID GSE114892. Conserved mRNA-granule component Scd6 targets Dhh1 to repress translation initiation and activates Dcp2-mediated mRNA decay in vivo.

   https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE114892

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Author details

1. Rakesh Kumar

   Division of Molecular and Cellular Biology, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, United States

   Contribution

   Data curation, Formal analysis, Investigation, Visualization, Writing – review and editing

   Contributed equally with

   Fan Zhang

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0009-0003-0349-0914

2. Fan Zhang

   Division of Molecular and Cellular Biology, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, United States

   Contribution

   Data curation, Formal analysis, Investigation, Visualization, Writing – review and editing

   Contributed equally with

   Rakesh Kumar

   Competing interests

   No competing interests declared

3. Shreyas Niphadkar

   Institute for Stem Cell Science and Regenerative Medicine (DBT-inStem), Bengaluru, India

   Contribution

   Data curation, Formal analysis, Investigation, Visualization, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0009-0002-4028-395X

4. Chisom Onu

   Department of Biological Sciences, Wayne State University, Detroit, United States

   Contribution

   Data curation, Formal analysis, Investigation, Visualization, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-3338-5141

5. Anil Kumar Vijjamarri

   Division of Molecular and Cellular Biology, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, United States

   Contribution

   Data curation, Formal analysis, Investigation, Visualization, Writing – review and editing

   Competing interests

   No competing interests declared

6. Miriam L Greenberg

   Department of Biological Sciences, Wayne State University, Detroit, United States

   Contribution

   Conceptualization, Formal analysis, Supervision, Funding acquisition, Project administration, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-7724-5426

7. Sunil Laxman

   Institute for Stem Cell Science and Regenerative Medicine (DBT-inStem), Bengaluru, India

   Contribution

   Conceptualization, Formal analysis, Supervision, Funding acquisition, Project administration, Writing – review and editing

   Competing interests

   No competing interests declared

8. Alan G Hinnebusch

   Division of Molecular and Cellular Biology, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, United States

   Contribution

   Conceptualization, Formal analysis, Supervision, Funding acquisition, Visualization, Writing – original draft, Project administration, Writing – review and editing

   For correspondence

   ahinnebusch@nih.gov

   Competing interests

   Reviewing editor, eLife

   "This ORCID iD identifies the author of this article:" 0000-0002-1627-8395

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