Suppression of endogenous gene silencing by bidirectional cytoplasmic RNA decay in
            <i>Arabidopsis</i>

Zhang, Xinyan; Zhu, Ying; Liu, Xiaodan; Hong, Xinyu; Xu, Yang; Zhu, Ping; Shen, Yang; Wu, Huihui; Ji, Yusi; Xing, Wen; Zhang, Chen; Zhao, Qiong; Wang, Yichuan; Lü, Jian; Guo, Hongwei

doi:10.1126/science.aaa2618

Cited by 154 publications

(212 citation statements)

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“…8, C and F), but were excluded from the nuclei. Cytoplasmic localization of AtSKI2 and AtSKI3, consistent with their roles as auxiliary factors required for exosomal activities in the cytoplasm, has been demonstrated previously (Zhang et al, 2015;Yu et al, 2015), but not their presence in the cytoplasmic granules shown here. This suggests the possibility that one or more activities of the AtSKI proteins might require their association into processing bodies (P bodies), cytoplasmic protein complexes known to be involved in degradation and translational arrest of mRNA (Maldonado-Bonilla, 2014).…”

Section: Atski3 and Atski2 Are Localized To The Cytoplasm And Cytoplasupporting

confidence: 56%

“…In contrast, the N terminus of ScSKI2 that is necessary and sufficient for interaction with ScSKI3 and ScSKI8 in yeast does not exhibit significant homology with the Arabidopsis AtSKI2. This does not, however, preclude successful interactions of AtSKI2 with AtSKI3 and AtSKI8 subunits as demonstrated by pull-down experiments in Arabidopsis (Dorcey et al, 2012;Zhang et al, 2015). It is well-documented that a third component of the SKI complex, named SKI8, is indispensable for the cytoplasmic functions of the exosome (Brown et al, 2000;Orban and Izaurralde, 2005;Dorcey et al, 2012).…”

Section: War7 Is Atski2 the Putative Helicase Of The Ski Complexmentioning

confidence: 96%

“…Positional cloning and analysis of WAR1 and WAR7 genes indicated that they carry mutations in Arabidopsis SUPERKILLER3 (AtSKI3; At1g76630) and AtSKI2 (At3g46960), respectively, that encode components of the SKI complex. In Arabidopsis, as in other eukaryotes studied thus far, SKI proteins have been shown to be required for cytoplasmic 39-to-59 RNA degradation by the exosome (Houseley et al, 2006;Dorcey et al, 2012;Halbach et al, 2013;Lange et al, 2014;Zhang et al, 2015), but evidence for their functional association into a complex is missing. Detailed analyses of the phenotypes of the ski single and ski cer7 double mutants reported here demonstrate that all SKI proteins participate in the CER7/ RRP45B-mediated control of wax deposition in developing Arabidopsis inflorescence stems, and support the notion that they act in the same pathway or complex.…”

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confidence: 99%

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SUPERKILLER complex components are required for the RNA exosome-mediated control of cuticular wax biosynthesis in Arabidopsis inflorescence stems

Zhao

Kunst

2016

Plant Physiol.

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ECERIFERUM7 (CER7)/AtRRP45B core subunit of the exosome, the main cellular 39-to-59 exoribonuclease, is a positive regulator of cuticular wax biosynthesis in Arabidopsis (Arabidopsis thaliana) inflorescence stems. CER7-dependent exosome activity determines stem wax load by controlling transcript levels of the wax-related gene CER3. Characterization of the second-site suppressors of the cer7 mutant revealed that small interfering RNAs (siRNAs) are direct effectors of CER3 expression. To explore the relationship between the exosome and posttranscriptional gene silencing (PTGS) in regulating CER3 transcript levels, we investigated two additional suppressor mutants, wax restorer1 (war1) and war7. We show that WAR1 and WAR7 encode Arabidopsis SUPERKILLER3 (AtSKI3) and AtSKI2, respectively, components of the SKI complex that associates with the exosome during cytoplasmic 39-to-59 RNA degradation, and that CER7-dependent regulation of wax biosynthesis also requires participation of AtSKI8. Our study further reveals that it is the impairment of the exosome-mediated 39-59 decay of CER3 transcript in the cer7 mutant that triggers extensive production of siRNAs and efficient PTGS of CER3. This identifies PTGS as a general mechanism for eliminating highly abundant endogenous transcripts that is activated when 39-to-59 mRNA turnover by the exosome is disrupted. Diminished efficiency of PTGS in ski mutants compared with cer7, as evidenced by lower accumulation of CER3-related siRNAs, suggests that reduced amounts of CER3 transcript are available for siRNA synthesis, possibly because CER3 mRNA that does not interact with SKI is degraded by 59-to-39 XRN4 exoribonuclease.

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Section: Atski3 and Atski2 Are Localized To The Cytoplasm And Cytoplasupporting

confidence: 56%

Section: War7 Is Atski2 the Putative Helicase Of The Ski Complexmentioning

confidence: 96%

mentioning

confidence: 99%

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SUPERKILLER complex components are required for the RNA exosome-mediated control of cuticular wax biosynthesis in Arabidopsis inflorescence stems

Zhao

Kunst

2016

Plant Physiol.

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“…Similar to most miRNAs, 21-nucleotide ta-siRNAs associate with AGO1 to guide cleavage of homologous mRNAs. RNA quality control siRNAs (rqc-siRNAs) and coding transcript siRNAs (ct-siRNAs) derive from the aberrant forms of mRNAs encoded by protein-coding genes, which are converted into dsRNA by cellular RNA-dependent RNA polymerases (RDR) when decapping activity or 5-to-39 and 39-to-59 RNA decay is impaired (Martínez de Alba et al, 2015;Zhang et al, 2015). Virus-activated siRNAs (vasiRNAs) are produced from mRNAs encoded by proteincoding genes, which are converted into dsRNA, mostly by RDR1, when plants are infected by viruses (Cao et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

Arabidopsis RNASE THREE LIKE2 Modulates the Expression of Protein-Coding Genes via 24-Nucleotide Small Interfering RNA-Directed DNA Methylation

Elvira-Matelot

Hachet²,

Shamandi

et al. 2016

Plant Cell

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(J.S.-V.) RNaseIII enzymes catalyze the cleavage of double-stranded RNA (dsRNA) and have diverse functions in RNA maturation. Arabidopsis thaliana RNASE THREE LIKE2 (RTL2), which carries one RNaseIII and two dsRNA binding (DRB) domains, is a unique Arabidopsis RNaseIII enzyme resembling the budding yeast small interfering RNA (siRNA)-producing Dcr1 enzyme. Here, we show that RTL2 modulates the production of a subset of small RNAs and that this activity depends on both its RNaseIII and DRB domains. However, the mode of action of RTL2 differs from that of Dcr1. Whereas Dcr1 directly cleaves dsRNAs into 23-nucleotide siRNAs, RTL2 likely cleaves dsRNAs into longer molecules, which are subsequently processed into small RNAs by the DICER-LIKE enzymes. Depending on the dsRNA considered, RTL2-mediated maturation either improves (RTL2-dependent loci) or reduces (RTL2-sensitive loci) the production of small RNAs. Because the vast majority of RTL2-regulated loci correspond to transposons and intergenic regions producing 24-nucleotide siRNAs that guide DNA methylation, RTL2 depletion modifies DNA methylation in these regions. Nevertheless, 13% of RTL2-regulated loci correspond to protein-coding genes. We show that changes in 24-nucleotide siRNA levels also affect DNA methylation levels at such loci and inversely correlate with mRNA steady state levels, thus implicating RTL2 in the regulation of proteincoding gene expression.

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“…A recent study by Zhang et al indicates that removal of aberrant transcripts by the RNA decay pathway is the key [4].…”

mentioning

confidence: 99%

Protecting genes from RNA silencing by destroying aberrant transcripts

Zhang

Zhu

2015

Sci. China Life Sci.

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Gene expression is intensively regulated at the transcript level. It is the rate of transcription and the rate of degradation that together determine the steady-state level of a specific transcript. A whole-genome study indicates that the half-life of Arabidopsis transcripts varies from 0.2 to >24 h, indicating large variations in the turnover rate of specific transcripts, which is related to their biological functions [1]. While RNA polymerase II is responsible for mRNA production in all eukaryotic organisms, a large repertoire of ribonucleases are involved in mRNA decay [2]. Different components in the RNA degradation pathway usually target specific sets of transcripts. The specificity can be at least partly accounted for by the presence of RNA motifs within the 3′ UTR regions and RNA binding proteins that recognize them. In Arabidopsis, mRNAs targeted for degradation are first deadenylated and subjected to digestion by at least two major classes of exonucleases [3]. The exosome performs 3′5′ degradation, whereas the XRN4 exonuclease acts on further decapped transcripts and digests them from the 5′ end.Both animals and plants utilize small RNAs for posttranscriptional gene silencing (PTGS) and/or transcriptional gene silencing (TGS). Evolutionarily, small RNA-mediated gene silencing is believed to function in defense against foreign nucleic acids, whether they are from viruses, transposons or transgenes. In Arabidopsis, small RNAs are usually 2124 nucleotides in length. Different classes of small RNAs (sRNA) all require a double stranded RNA (dsRNA) precursor that is diced into small fragments by the RNase III-class DICER enzymes. The DICER protein functions like a ruler to determine the size of small RNA products. For example, siRNA generated by DCL2 are usually 22-nt long and siRNA by DCL4 are 21-nt long. When the guide strand of double stranded sRNAs are loaded into ARGONAUTE (AGO) proteins and form the RNA-induced silencing complex (RISC), the RISC complex binds to complementary transcripts, resulting in transcript cleavage or translational inhibition. The cleaved transcript can also be converted into dsRNAs by the RNA-dependent RNA polymerases (RDRs) and produce so-called secondary small interfering RNAs, which increases siRNA levels and ensures silencing.The dsRNA precursor can be generated from different sources. MicroRNA (miRNA) genes produce transcripts that form hairpin-loop structures and are processed into mature miRNAs by DCL1. In other cases, aberrant transcripts are sensed by the cell and converted into dsRNAs by RDRs. For example, TRANS-ACTING SIRNA (TAS) genes are targets of miRNAs. The cleaved transcripts by the

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Suppression of endogenous gene silencing by bidirectional cytoplasmic RNA decay in Arabidopsis

Cited by 154 publications

References 44 publications

SUPERKILLER complex components are required for the RNA exosome-mediated control of cuticular wax biosynthesis in Arabidopsis inflorescence stems

SUPERKILLER complex components are required for the RNA exosome-mediated control of cuticular wax biosynthesis in Arabidopsis inflorescence stems

Arabidopsis RNASE THREE LIKE2 Modulates the Expression of Protein-Coding Genes via 24-Nucleotide Small Interfering RNA-Directed DNA Methylation

Protecting genes from RNA silencing by destroying aberrant transcripts

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