Proteasome subunit RPT2a promotes PTGS through repressing RNA quality control in Arabidopsis

Kim, Myung‐Hee; Jeon, Jieun; Lee, Seulbee; Lee, Jae Ho; Gao, Lei; Lee, Byung‐Hoon; Park, Jeong Mee; Kim, Yun Ju; Kwak, June M.

doi:10.1038/s41477-019-0546-1

Cited by 14 publications

(7 citation statements)

References 67 publications

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“…Since SGS3 and DCL4 complexes are partially colocalized ( 40 ), SGS3 could translocate FVE (or vice versa) to the siRNA bodies to modulate the downstream siRNA production. Notably, SGS3 has been recently reported to contribute to translocating proteasome subunits [e.g., the regulatory particle AAA-ATPase 2A (RPT2a)] into the proximity of the siRNA bodies to repress RNA quality control and to promote PTGS ( 49 ). Given these observations, SGS3/FVE might translocate additional presently unidentified targets to siRNA bodies for fine-tuning PTGS activities.…”

Section: Discussionmentioning

confidence: 99%

“…It appears that FVE has an impact on transgene silencing but barely on endogenous RNA silencing. This scenario is also reminiscent of genes such as JMJ14 and RPT2a that appear to only affect transgene siRNA production, but not the abundance of endogenous sRNAs ( 49 , 50 ). One plausible explanation is that the expression of transgenes, but not endogenous loci, might often lead to production of aberrant transcripts that reach the threshold of the RNA quality control machinery.…”

Section: Discussionmentioning

confidence: 99%

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The epigenetic factor FVE orchestrates cytoplasmic SGS3-DRB4-DCL4 activities to promote transgene silencing in Arabidopsis

Sun

et al. 2021

Sci. Adv.

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Posttranscriptional gene silencing (PTGS) is a regulatory mechanism to suppress undesired transcripts. Here, we identified Flowering locus VE (FVE), a well-known epigenetic component, as a new player in cytoplasmic PTGS. Loss-of-function fve mutations substantially reduced the accumulation of transgene-derived small interfering RNAs (siRNAs). FVE interacts with suppressor of gene silencing 3 (SGS3), a master component in PTGS. FVE promotes SGS3 homodimerization that is essential for its function. FVE can bind to single-stranded RNA and double-stranded RNA (dsRNA) with moderate affinities, while its truncated form FVE-8 has a significantly increased binding affinity to dsRNA. These affinities affect the association and channeling of SGS3-RNA to downstream dsRNA binding protein 4 (DRB4)/Dicer-like protein 2/4 (DCL2/4) complexes. Hence, FVE, but not FVE-8, biochemically enhances the DRB4/DCL2/4 activity in vitro. We surmise that FVE promotes production of transgene-derived siRNAs through concertedly tuning SGS3-DRB4/DCL2/4 functions. Thus, this study revealed a noncanonical role of FVE in PTGS.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

The epigenetic factor FVE orchestrates cytoplasmic SGS3-DRB4-DCL4 activities to promote transgene silencing in Arabidopsis

Sun

et al. 2021

Sci. Adv.

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“…Moreover, experiments involving Cardamine hirsuta ABCE2 (also named ChRLI2) revealed it as an important regulator of leaf growth and proposed, for the first time, a link between ABCE2 and ribosomes in plants (Kougioumoutzi et al, 2013). Notably, mRNA surveillance pathways were found to compete with RNA silencing machinery for the substrate (Christie et al, 2011; Liu & Chen, 2016; Szádeczky‐Kardoss et al, 2018a; Kim et al, 2019). Because of the above results, we suggest that AtABCE2 might suppress RNA silencing via positive regulation of mRNA surveillance mechanisms.…”

Section: Discussionmentioning

confidence: 99%

Mutational analysis of Arabidopsis thaliana ABCE2 identifies important motifs for its RNA silencing suppressor function

et al. 2020

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• ATP-binding cassette sub-family E member 1 (ABCE1) is recognized as a strongly conserved ribosome recycling factor, indispensable for translation in archaea and eukaryotes, however, its role in plants remains largely unidentified. Arabidopsis thaliana encodes two paralogous ABCE proteins (AtABCE1 and AtABCE2), sharing 81% identity. We previously reported that AtABCE2 functions as a suppressor of RNA silencing and that its gene is ubiquitously expressed. Here we describe the structural requirements of AtABCE2 for its suppressor function. • Using agroinfiltration assays, we transiently overexpressed mutated versions of AtABCE2 together with GFP, to induce silencing in GFP transgenic Nicotiana benthamiana leaves. The influence of mutations was analysed at both local and systemic levels by in vivo imaging of GFP, Northern blot analysis of GFP siRNAs and observation of plants under UV light. • Mutants of AtABCE2 with impaired ATP binding in either active site I or II failed to suppress GFP RNA silencing. Mutations disrupting ATP hydrolysis influenced the suppression of silencing differently at active site I or II. We also found that the N-terminal iron-sulphur cluster domain of AtABCE2 is crucial for its suppressor function. • Meaningfully, the observed structural requirements of AtABCE2 for RNA silencing suppression were found to be similar to those of archaeal ABCE1 needed for ribosome recycling. AtABCE2 might therefore suppress RNA silencing via supporting the competing RNA degradation mechanisms associated with ribosome recycling.

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“…However, emerging evidences have suggested that these two pathways can functionally interact with each other. There are solid evidences showing that a subset of components involving RNA processing and/or RQC pathways can act as suppressors of RNA silencing ( 30 - 37 ). In Arabidopsis, impaired decapping and deadenylation can restrict RNA silencing ( 33 , 35 , 38 ).…”

Section: Rna Silencing Interacts With Rna Quality Control Pathwaymentioning

confidence: 99%

Crosstalk between RNA silencing and RNA quality control in plants

Kim

2023

BMB Rep

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RNAs are pivotal molecules acting as messengers of genetic information and regulatory molecules for cellular development and survival. From birth to death, RNAs face constant cellular decision for the precise control of cellular function and activity. Most eukaryotic cells employ conserved machineries for RNA decay including RNA silencing and RNA quality control (RQC). In plants, RQC monitors endogenous RNAs and degrades aberrant and dysfunctional species, whereas RNA silencing promotes RNA degradation to repress the expression of selected endogenous RNAs or exogenous RNA derived from transgenes and virus. Interestingly, emerging evidences have indicated that RQC and RNA silencing interact with each by sharing target RNAs and regulatory components. Such interaction should be tightly organized for proper cellular survival. However, it is still elusive that how each machinery specifically recognizes target RNAs. In this review, we summarize recent advances on RNA silencing and RQC pathway and discuss potential mechanisms underlying the interaction between the two machineries.

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Proteasome subunit RPT2a promotes PTGS through repressing RNA quality control in Arabidopsis

Cited by 14 publications

References 67 publications

The epigenetic factor FVE orchestrates cytoplasmic SGS3-DRB4-DCL4 activities to promote transgene silencing in Arabidopsis

The epigenetic factor FVE orchestrates cytoplasmic SGS3-DRB4-DCL4 activities to promote transgene silencing in Arabidopsis

Mutational analysis of Arabidopsis thaliana ABCE2 identifies important motifs for its RNA silencing suppressor function

Crosstalk between RNA silencing and RNA quality control in plants

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