Interconnections between mRNA degradation and RDR-dependent siRNA production in mRNA turnover in plants

Tsuzuki, Mikio; Motomura, Kazuki; Kumakura, Naoyoshi; Takeda, Atsushi

doi:10.1007/s10265-017-0906-8

Cited by 23 publications

(15 citation statements)

References 130 publications

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“…Through mutant analyses, confocal microscopy, and omics technologies, the integration of mRNA translation, turnover, and sequestration has become recognized as a highly selective regulatory process of individual mRNAs. Due to space limitations, we did not delve upon how mRNA decay protects the cellular transcriptome from inappropriate posttranscriptional silencing of endogenous genes (for review, see Liu and Chen, 2016;Tsuzuki et al, 2017;Zhang and Guo, 2017). We also did not consider nuclear mechanisms of transcript turnover that can involve CBP80 .…”

Section: Resultsmentioning

confidence: 99%

Polysomes, Stress Granules, and Processing Bodies: A Dynamic Triumvirate Controlling Cytoplasmic mRNA Fate and Function

2017

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Section: Resultsmentioning

confidence: 99%

Polysomes, Stress Granules, and Processing Bodies: A Dynamic Triumvirate Controlling Cytoplasmic mRNA Fate and Function

2017

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“…In addition to RNA silencing, RNA decay is another crucial pathway that regulates RNA turnover [ 6 , 7 ]. RNA decay or exonucleolytic RNA turnover is a 5’–3’ and 3’–5’ exoribonuclease-dependent, ubiquitous mechanism in eukaryotic cells by which mRNA molecules are enzymatically degraded [ 6 ].…”

Section: Introductionmentioning

confidence: 99%

“…The degradation process is initiated by deadenylation to progressively remove the 3’ poly(A) tail followed by exosome complex-mediated 3’–5’ cleavage or decapping and subsequent exoribonuclease (XRN)-mediated 5’–3’ decay [ 6 , 7 ]. Deadenylation is catalysed by the conserved poly (A)-specific ribonuclease (PARN) as well as by the conserved carbon catabolite repressor 4 (CCR4) complex [ 8 – 10 ], and the removal of the 5’ cap structure is through concerted action of a set of conserved decapping proteins (DCP) [ 6 , 7 ]. In Arabidopsis thaliana , DCP1, DCP2, DCP5, VARICOSE (VCS) and possibly DEA(D/H)-box RNA helicase 1 (DHH1) constitute the decapping complex [ 11 ].…”

Section: Introductionmentioning

confidence: 99%

RNA decay is an antiviral defense in plants that is counteracted by viral RNA silencing suppressors

Wang

2018

PLoS Pathog

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Exonuclease-mediated RNA decay in plants is known to be involved primarily in endogenous RNA degradation, and several RNA decay components have been suggested to attenuate RNA silencing possibly through competing for RNA substrates. In this paper, we report that overexpression of key cytoplasmic 5’–3’ RNA decay pathway gene-encoded proteins (5’RDGs) such as decapping protein 2 (DCP2) and exoribonuclease 4 (XRN4) in Nicotiana benthamiana fails to suppress sense transgene-induced post-transcriptional gene silencing (S-PTGS). On the contrary, knock-down of these 5’RDGs attenuates S-PTGS and supresses the generation of small interfering RNAs (siRNAs). We show that 5’RDGs degrade transgene transcripts via the RNA decay pathway when the S-PTGS pathway is disabled. Thus, RNA silencing and RNA decay degrade exogenous gene transcripts in a hierarchical and coordinated manner. Moreover, we present evidence that infection by turnip mosaic virus (TuMV) activates RNA decay and 5’RDGs also negatively regulate TuMV RNA accumulation. We reveal that RNA silencing and RNA decay can mediate degradation of TuMV RNA in the same way that they target transgene transcripts. Furthermore, we demonstrate that VPg and HC-Pro, the two known viral suppressors of RNA silencing (VSRs) of potyviruses, bind to DCP2 and XRN4, respectively, and the interactions compromise their antiviral function. Taken together, our data highlight the overlapping function of the RNA silencing and RNA decay pathways in plants, as evidenced by their hierarchical and concerted actions against exogenous and viral RNA, and VSRs not only counteract RNA silencing but also subvert RNA decay to promote viral infection.

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“…Kurihara (2017) and Tsuzuki et al (2017) reviewed and discussed the RNA degradation pathways in plants, and showed many plant-specific regulatory aspects of RNA turnover. Recent Arabidopsis mutant work suggested that the defects in function of 5′-3′ and/or 3′-5′ exoribonucleases can change what has happened on RNA molecules, e.g.…”

mentioning

confidence: 99%

“…mRNA molecules can be recognized by RNA-dependent RNA polymerases to produce siRNA when exoribonuclease-based RNA degradation was impaired (Martínez de Alba et al 2015). So far, many proteins involved in RNA degradation were reported (Tsuzuki et al 2017). To understand further how plant cells manage to regulate RNA metabolism, a detailed functional analysis on these proteins is expected.…”

mentioning

confidence: 99%

Expanding the plant non-coding RNA world

Ohtani

2016

J Plant Res

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in mouse revealed "a new continent in the RNA world", through the novel observation showing that ~73% of genomic regions are used for transcription of non-coding RNAs (Carninci et al. 2005;Katayama et al. 2005). The emergence of next-generation sequencing technologies encouraged this trend to identify a variety of non-coding RNAs. These big successes by non-coding RNA research have generated new RNA biology; now we know that RNA molecules are not only working as the intermediates between DNAs and proteins, but as key players of posttranscriptional and epigenetic regulation of gene expression. This is obviously true in plants, as many experimental reports have indicated the importance of non-coding RNAbased gene regulation in plant development, environmental responses, and biotic and/or abiotic stress responses.In this special issue of JPR Symposium "Expanding the plant non-coding RNA world", our current understanding of biogenesis, metabolisms, and function of plant non-coding RNA is reviewed and discussed with updated review articles, an original paper, and a technical note. First, we tried to provide detailed molecular views of small RNA biogenesis in plants. The siRNA and microRNA (miRNA), classes of small RNA with 18-25 nucleotides (nt) in length, pursue their function as the guides to target specific mRNAs for gene silencing, after incorporation into an RNA-induced silencing complex (RISC). These small RNAs are generated through multiple steps of RNA metabolic regulation; (1) formation of inter-or intramolecular double-stranded RNA (dsRNA) precursors, (2) biogenesis of small RNA duplexes through catalyzing dsRNA by dsRNA-specific endoribonucleases, Dicer-like (DCL) proteins, (3) loading of small RNA duplex onto ARGONAUTE (AGO) proteins, and (4) elimination of miRNA* or passenger siRNA strand, which are complementary strands for guide strand RNAs in small RNA duplex, by unwinding of Ribonucleic acid (RNA) is one of the biopolymers essential for organisms. In the "classical" view of molecular biology, functional RNA species have been categorized into three major groups, such as messenger RNAs (mRNAs), template molecules to biosynthesize proteins, ribosomal RNAs (rRNAs), components of huge molecular machinery ribosome for protein biosynthesis, and transfer RNAs (tRNAs), molecular couriers of amino acids to the ribosome. Function of these RNAs brought the perspective of so-called "central dogma", in which RNA molecules are considered as the mediators of genomic information written within DNA molecules for protein biosynthesis to achieve required cell activity.However, our view of RNA function has been greatly revised with the advent of the post genome era. One notable study was the discovery of small non-coding RNAs, called small interference RNAs (siRNAs), that function in post-transcriptional gene silencing (Fire et al. 1998). Later, the phenomenon known as co-suppression in plants and quelling in fungi, in which transgenes suppress the accumulation of endogenous transcripts based on the homology between tran...

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Interconnections between mRNA degradation and RDR-dependent siRNA production in mRNA turnover in plants

Cited by 23 publications

References 130 publications

Polysomes, Stress Granules, and Processing Bodies: A Dynamic Triumvirate Controlling Cytoplasmic mRNA Fate and Function

Polysomes, Stress Granules, and Processing Bodies: A Dynamic Triumvirate Controlling Cytoplasmic mRNA Fate and Function

RNA decay is an antiviral defense in plants that is counteracted by viral RNA silencing suppressors

Expanding the plant non-coding RNA world

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