Genome-Wide High-Resolution Mapping of Exosome Substrates Reveals Hidden Features in the Arabidopsis Transcriptome

Chekanova, Julia A.; Gregory, Brian D.; Reverdatto, Sergey; Chen, Huaming; Kumar, Ravi Shankar; Hooker, Tanya S.; Yazaki, Junshi; Li, Pinghua; Skiba, Nikolai P.; Peng, Qian; Alonso, José M.; Brukhin, Vladimir; Grossniklaus, Ueli; Ecker, Joseph R.; Belostotsky, Dmitry A.

doi:10.1016/j.cell.2007.10.056

Cited by 300 publications

(425 citation statements)

References 56 publications

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“…In Arabidopsis, TRAMP-like and exosome activities have been suggested to be responsible for oligoadenylation and subsequent degradation of intermediates of miRNA biogenesis. However, in contrast to mir-1176 precursors, these short A-tracts were added upstream of the stem-loop harboring the mir-5p/3p duplex [67]. We have previously shown that short A-tails are present in a fraction of the snRNAs as well as on rRNA precursors in D. discoideum [55,68], suggesting that oligoadenylation is a common feature also in D. discoideum .…”

Section: Resultsmentioning

confidence: 99%

Global characterization of the Dicer-like protein DrnB roles in miRNA biogenesis in the social amoeba Dictyostelium discoideum

et al. 2018

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Micro (mi)RNAs regulate gene expression in many eukaryotic organisms where they control diverse biological processes. Their biogenesis, from primary transcripts to mature miRNAs, have been extensively characterized in animals and plants, showing distinct differences between these phylogenetically distant groups of organisms. However, comparably little is known about miRNA biogenesis in organisms whose evolutionary position is placed in between plants and animals and/or in unicellular organisms. Here, we investigate miRNA maturation in the unicellular amoeba Dictyostelium discoideum, belonging to Amoebozoa, which branched out after plants but before animals. High-throughput sequencing of small RNAs and poly(A)-selected RNAs demonstrated that the Dicer-like protein DrnB is required, and essentially specific, for global miRNA maturation in D. discoideum. Our RNA-seq data also showed that longer miRNA transcripts, generally preceded by a T-rich putative promoter motif, accumulate in a drnB knock-out strain. For two model miRNAs we defined the transcriptional start sites (TSSs) of primary (pri)-miRNAs and showed that they carry the RNA polymerase II specific m7G-cap. The generation of the 3ʹ-ends of these pri-miRNAs differs, with pri-mir-1177 reading into the downstream gene, and pri-mir-1176 displaying a distinct end. This 3´-end is processed to shorter intermediates, stabilized in DrnB-depleted cells, of which some carry a short oligo(A)-tail. Furthermore, we identified 10 new miRNAs, all DrnB dependent and developmentally regulated. Thus, the miRNA machinery in D. discoideum shares features with both plants and animals, which is in agreement with its evolutionary position and perhaps also an adaptation to its complex lifestyle: unicellular growth and multicellular development.

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Section: Resultsmentioning

confidence: 99%

Global characterization of the Dicer-like protein DrnB roles in miRNA biogenesis in the social amoeba Dictyostelium discoideum

et al. 2018

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“…In general, uncapped fragments derived from mRNAs in eukaryotic transcriptomes are generated by decapping or endonucleolytic cleavage, and these RNA fragments are then rapidly recognized and degraded by 59 to 39 (e.g., XRN4) (Gazzani et al, 2004) and 39 to 59 (e.g., exosome) (Chekanova et al, 2007) exonucleases. Thus, they represent the degrading fraction of the transcriptome.…”

Section: Resultsmentioning

confidence: 99%

Chemical Modifications Mark Alternatively Spliced and Uncapped Messenger RNAs in Arabidopsis

et al. 2015

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Posttranscriptional chemical modification of RNA bases is a widespread and physiologically relevant regulator of RNA maturation, stability, and function. While modifications are best characterized in short, noncoding RNAs such as tRNAs, growing evidence indicates that mRNAs and long noncoding RNAs (lncRNAs) are likewise modified. Here, we apply our highthroughput annotation of modified ribonucleotides (HAMR) pipeline to identify and classify modifications that affect WatsonCrick base pairing at three different levels of the Arabidopsis thaliana transcriptome (polyadenylated, small, and degrading RNAs). We find this type of modifications primarily within uncapped, degrading mRNAs and lncRNAs, suggesting they are the cause or consequence of RNA turnover. Additionally, modifications within stable mRNAs tend to occur in alternatively spliced introns, suggesting they regulate splicing. Furthermore, these modifications target mRNAs with coherent functions, including stress responses. Thus, our comprehensive analysis across multiple RNA classes yields insights into the functions of covalent RNA modifications in plant transcriptomes.

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“…S1). Likewise, mature miRNA amounts were not affected by defects in core exosome subunits in A. thaliana (29). In contrast, RNAi-mediated suppression of RRP6 (Fig.…”

Section: Mut68 Promotes the Degradation Of Small Rnas By The Rrp6mentioning

confidence: 95%

Uridylation of mature miRNAs and siRNAs by the MUT68 nucleotidyltransferase promotes their degradation in Chlamydomonas

Ibrahim

Rymarquis

Kim

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

124

185

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Regulation of gene expression by small RNAs (∼20-30 nucleotides in length) plays an essential role in developmental pathways and defense responses against genomic parasites in eukaryotes. MicroRNAs (miRNAs) and small interfering RNAs (siRNAs) commonly direct the inactivation of cognate sequences through a variety of mechanisms, including RNA degradation, translation inhibition, and transcriptional repression. Recent studies have provided considerable insight into the biogenesis and the mode of action of miRNAs and siRNAs. However, relatively little is known about mechanisms of quality control and small RNA decay in RNA interference (RNAi) pathways. Here we show that deletion of MUT68, encoding a terminal nucleotidyltransferase in the alga Chlamydomonas reinhardtii, results in elevated miRNA and siRNA levels. We found that MUT68 plays a role in the untemplated uridylation of the 3′ ends of small RNAs in vivo and stimulates their degradation by the RRP6 exosome subunit in vitro. Moreover, RRP6 depletion also leads to accumulation of small RNAs in vivo. We propose that MUT68 and RRP6 cooperate in the degradation of mature miRNAs and siRNAs, as a quality control mechanism to eliminate dysfunctional or damaged small RNA molecules.exosome | RNA interference | miRNA quality control

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Genome-Wide High-Resolution Mapping of Exosome Substrates Reveals Hidden Features in the Arabidopsis Transcriptome

Cited by 300 publications

References 56 publications

Global characterization of the Dicer-like protein DrnB roles in miRNA biogenesis in the social amoeba Dictyostelium discoideum

Global characterization of the Dicer-like protein DrnB roles in miRNA biogenesis in the social amoeba Dictyostelium discoideum

Chemical Modifications Mark Alternatively Spliced and Uncapped Messenger RNAs in Arabidopsis

Uridylation of mature miRNAs and siRNAs by the MUT68 nucleotidyltransferase promotes their degradation in Chlamydomonas

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