MicroRNAs Inhibit the Translation of Target mRNAs on the Endoplasmic Reticulum in Arabidopsis

Li, Shengben; Liu, Lin; Zhuang, Xiaohong; Yu, Yu; Liu, Xigang; Cui, Xia; Ji, Lijuan; Pan, Zhiqiang; Cao, Xiaofeng; Mo, Beixin; Zhang, Fuchun; Raikhel, Natasha V.; Chen, Xuemei

doi:10.1016/j.cell.2013.04.005

Cited by 469 publications

(459 citation statements)

References 68 publications

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“…However, the finding of many miRNA-directed slicing events in Nematostella does not mean that bilaterianlike interactions between the miRNA seed and other transcript targets do not occur in parallel. Moreover, extended miRNA-mRNA matches in plants leading to target slicing were recently shown also to promote substantial translational inhibition, and it is possible that the same also occurs in Cnidaria (Brodersen et al 2008;Yang et al 2012;Li et al 2013).…”

Section: Discussionmentioning

confidence: 99%

Cnidarian microRNAs frequently regulate targets by cleavage

et al. 2014

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In bilaterians, which comprise most of extant animals, microRNAs (miRNAs) regulate the majority of messenger RNAs (mRNAs) via base-pairing of a short sequence (the miRNA ''seed'') to the target, subsequently promoting translational inhibition and transcript instability. In plants, many miRNAs guide endonucleolytic cleavage of highly complementary targets. Because little is known about miRNA function in nonbilaterian animals, we investigated the repertoire and biological activity of miRNAs in the sea anemone Nematostella vectensis, a representative of Cnidaria, the sister phylum of Bilateria. Our work uncovers scores of novel miRNAs in Nematostella, increasing the total miRNA gene count to 87. Yet only a handful are conserved in corals and hydras, suggesting that microRNA gene turnover in Cnidaria greatly exceeds that of other metazoan groups. We further show that Nematostella miRNAs frequently direct the cleavage of their mRNA targets via nearly perfect complementarity. This mode of action resembles that of small interfering RNAs (siRNAs) and plant miRNAs. It appears to be common in Cnidaria, as several of the miRNA target sites are conserved among distantly related anemone species, and we also detected miRNA-directed cleavage in Hydra. Unlike in bilaterians, Nematostella miRNAs are commonly coexpressed with their target transcripts. In light of these findings, we propose that post-transcriptional regulation by miRNAs functions differently in Cnidaria and Bilateria. The similar, siRNA-like mode of action of miRNAs in Cnidaria and plants suggests that this may be an ancestral state.

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Section: Discussionmentioning

confidence: 99%

Cnidarian microRNAs frequently regulate targets by cleavage

et al. 2014

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“…This contradicts a substantial amount of empirical data. Many plant miRNA targets that are perfectly paired in the central region are nonetheless also translationally repressed (Chen, 2004;Yang et al, 2011;Li et al, 2013). Conversely, not all targets that do have central mismatches are translationally repressed: Some are non-coding RNAs that are still sliced despite the central mismatches (Allen et al, 2005), some act as targetmimics (Ivashuta et al, 2011;Liu et al, 2014), while others are simply non-functional, especially when the miRNA levels are not overwhelming (Li et al, 2014a).…”

Section: Conservation and Identification Of Mirna Targetsmentioning

confidence: 99%

Revisiting Criteria for Plant MicroRNA Annotation in the Era of Big Data

2018

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MicroRNAs (miRNAs) are ~21 nucleotide-long regulatory RNAs that arise from endonucleolytic processing of hairpin precursors. Many function as essential post-transcriptional regulators of target mRNAs and long non-coding RNAs. Alongside miRNAs, plants also produce large numbers of short interfering RNAs (siRNAs), which are distinguished from miRNAs primarily by their biogenesis (typically processed from long double-stranded RNA instead of single-stranded hairpins) and functions (typically via roles in transcriptional regulation instead of posttranscriptional regulation). Next-generation DNA sequencing methods have yielded extensive datasets of plant small RNAs, resulting in many miRNA annotations. However, it has become clear that many miRNA annotations are questionable. The sheer number of endogenous siRNAs compared to miRNAs has been a major factor in the erroneous annotation of siRNAs as miRNAs. Here, we provide updated criteria for the confident annotation of plant miRNAs, suitable for the era of "big data" from DNA sequencing. The updated criteria emphasize replication, the minimization of false positives, and they require next-generation sequencing of small RNAs. We argue that improved annotation systems are needed for miRNAs and all other classes of plant small RNAs. Finally, to illustrate the complexities of miRNA and siRNA annotation, we review the evolution and functions of miRNAs and siRNAs in plants.

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“…By contrast, plant miRNAs are highly complementary to their targets, and cleavage in the middle of target sites is the major mode of plant miRNA action (Rhoades et al, 2002). However, growing evidence indicates that plant miRNAs can also inhibit the translation of their targets (Brodersen et al, 2008;Iwakawa and Tomari, 2013;Li et al, 2013bLi et al, , 2013cLiu et al, 2013). In vitro assays of RNA-induced silencing complexes containing Arabidopsis thaliana ARGONAUTE1 (AGO1) demonstrated that plant miRNAs can repress translation initiation uncoupled with deadenylation or mRNA decay (Iwakawa and Tomari, 2013).…”

Section: Introductionmentioning

confidence: 99%

“…Furthermore, miRNA binding sites in ORFs can hinder the movement of ribosomes (Iwakawa and Tomari, 2013). In Arabidopsis, miRNA-mediated translation repression occurs in the endoplasmic reticulum and requires the endoplasmic reticulum protein ALTERED MERISTEM PROGRAM1 (Li et al, 2013c).…”

Section: Introductionmentioning

confidence: 99%

Global Analysis of Truncated RNA Ends Reveals New Insights into Ribosome Stalling in Plants

et al. 2016

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High-throughput approaches for profiling the 59 ends of RNA degradation intermediates on a genome-wide scale are frequently applied to analyze and validate cleavage sites guided by microRNAs (miRNAs). However, the complexity of the RNA degradome other than miRNA targets is currently largely uncharacterized, and this limits the application of RNA degradome studies. We conducted a global analysis of 59-truncated mRNA ends that mapped to coding sequences (CDSs) of Arabidopsis thaliana, rice (Oryza sativa), and soybean (Glycine max). Based on this analysis, we provide multiple lines of evidence to show that the plant RNA degradome contains in vivo ribosome-protected mRNA fragments. We observed a 3-nucleotide periodicity in the position of free 59 RNA ends and a bias toward the translational frame. By examining conserved peptide upstream open reading frames (uORFs) of Arabidopsis and rice, we found a predominance of 59 termini of RNA degradation intermediates that were separated by a length equal to a ribosome-protected mRNA fragment. Through the analysis of RNA degradome data, we discovered uORFs and CDS regions potentially associated with stacked ribosomes in Arabidopsis. Furthermore, our analysis of RNA degradome data suggested that the binding of Arabidopsis ARGONAUTE7 to a noncleavable target site of miR390 might directly hinder ribosome movement. This work demonstrates an alternative use of RNA degradome data in the study of ribosome stalling.

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MicroRNAs Inhibit the Translation of Target mRNAs on the Endoplasmic Reticulum in Arabidopsis

Cited by 469 publications

References 68 publications

Cnidarian microRNAs frequently regulate targets by cleavage

Cnidarian microRNAs frequently regulate targets by cleavage

Revisiting Criteria for Plant MicroRNA Annotation in the Era of Big Data

Global Analysis of Truncated RNA Ends Reveals New Insights into Ribosome Stalling in Plants

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