Mimicry of molecular pretenders: The terminal structures of satellites associated with plant RNA viruses

Huang, Ying-Wen; Hu, Chung-Chi; Lin, Na-Sheng; Hsu, Yau-Heiu

doi:10.4161/rna.7.2.11089

Cited by 18 publications

(19 citation statements)

References 72 publications

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“…Despite past efforts, the molecular bases underlying virus-induced diseases symptoms are still poorly understood. Subviral non-coding RNA molecules such as satellite RNAs (satRNAs) or defective interfering (DI) RNAs are often associated with plant viruses and can modify the symptoms induced by helper viruses [1], [2], [3]. Because such subviral RNAs dramatically modify the symptoms induced by helper viruses, they are potential tools for gaining insights into the molecular mechanisms of symptom development.…”

Section: Introductionmentioning

confidence: 99%

A Viral Satellite RNA Induces Yellow Symptoms on Tobacco by Targeting a Gene Involved in Chlorophyll Biosynthesis using the RNA Silencing Machinery

Shimura¹,

Pantaleo

Ishihara³

et al. 2011

PLoS Pathog

259

228

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Symptoms on virus-infected plants are often very specific to the given virus. The molecular mechanisms involved in viral symptom induction have been extensively studied, but are still poorly understood. Cucumber mosaic virus (CMV) Y satellite RNA (Y-sat) is a non-coding subviral RNA and modifies the typical symptom induced by CMV in specific hosts; Y-sat causes a bright yellow mosaic on its natural host Nicotiana tabacum. The Y-sat-induced yellow mosaic failed to develop in the infected Arabidopsis and tomato plants suggesting a very specific interaction between Y-sat and its host. In this study, we revealed that Y-sat produces specific short interfering RNAs (siRNAs), which interfere with a host gene, thus inducing the specific symptom. We found that the mRNA of tobacco magnesium protoporphyrin chelatase subunit I (ChlI, the key gene involved in chlorophyll synthesis) had a 22-nt sequence that was complementary to the Y-sat sequence, including four G-U pairs, and that the Y-sat-derived siRNAs in the virus-infected plant downregulate the mRNA of ChlI by targeting the complementary sequence. ChlI mRNA was also downregulated in the transgenic lines that express Y-sat inverted repeats. Strikingly, modifying the Y-sat sequence in order to restore the 22-nt complementarity to Arabidopsis and tomato ChlI mRNA resulted in yellowing symptoms in Y-sat-infected Arabidopsis and tomato, respectively. In 5′-RACE experiments, the ChlI transcript was cleaved at the expected middle position of the 22-nt complementary sequence. In GFP sensor experiments using agroinfiltration, we further demonstrated that Y-sat specifically targeted the sensor mRNA containing the 22-nt complementary sequence of ChlI. Our findings provide direct evidence that the identified siRNAs derived from viral satellite RNA directly modulate the viral disease symptom by RNA silencing-based regulation of a host gene.

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Section: Introductionmentioning

confidence: 99%

A Viral Satellite RNA Induces Yellow Symptoms on Tobacco by Targeting a Gene Involved in Chlorophyll Biosynthesis using the RNA Silencing Machinery

Shimura¹,

Pantaleo

Ishihara³

et al. 2011

PLoS Pathog

259

228

View full text Add to dashboard Cite

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“…The satBaMV RNA 3′ UTR structure comprises three stem-loops, SLA, SLB, and SLC, and two cis -acting elements responsible for efficient replication [29]. Although the satBaMV 3′ UTR sequence and structural elements mimic those of the BaMV 3′ UTR for recognition by the BaMV RdRp complexes, discrepancies between these two 3′ UTRs are significant, most notably the lack of a pseudoknot structure in the satBaMV RNA 3′ UTR [29], [30]. Thus, whether satBaMV RNA shares the same set of replicase complexes with BaMV or uses another set of replicase complexes (possibly with different host factors) for replication remains an open question.…”

Section: Introductionmentioning

confidence: 99%

Hsp90 Interacts Specifically with Viral RNA and Differentially Regulates Replication Initiation of Bamboo mosaic virus and Associated Satellite RNA

Huang

Liou

et al. 2012

PLoS Pathog

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Host factors play crucial roles in the replication of plus-strand RNA viruses. In this report, a heat shock protein 90 homologue of Nicotiana benthamiana, NbHsp90, was identified in association with partially purified replicase complexes from BaMV-infected tissue, and shown to specifically interact with the 3′ untranslated region (3′ UTR) of BaMV genomic RNA, but not with the 3′ UTR of BaMV-associated satellite RNA (satBaMV RNA) or that of genomic RNA of other viruses, such as Potato virus X (PVX) or Cucumber mosaic virus (CMV). Mutational analyses revealed that the interaction occurs between the middle domain of NbHsp90 and domain E of the BaMV 3′ UTR. The knockdown or inhibition of NbHsp90 suppressed BaMV infectivity, but not that of satBaMV RNA, PVX, or CMV in N. benthamiana. Time-course analysis further revealed that the inhibitory effect of 17-AAG is significant only during the immediate early stages of BaMV replication. Moreover, yeast two-hybrid and GST pull-down assays demonstrated the existence of an interaction between NbHsp90 and the BaMV RNA-dependent RNA polymerase. These results reveal a novel role for NbHsp90 in the selective enhancement of BaMV replication, most likely through direct interaction with the 3′ UTR of BaMV RNA during the initiation of BaMV RNA replication.

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“…lncRNAs acting in cis usually tether RNA polymerase complexes or small regulatory RNAs to the site of active transcription. Guidance in trans is usually facilitated by formation of RNA:DNA duplexes, RNA:DNA:DNA triplexes or recognition of specific chromatin features by lncRNAs (Bonasio, Tu, & Reinberg, 2010;Y. W. Huang, Hu, Lin, & Hsu, 2010).…”

Section: Lncrnas and Their Mechanisms Of Actionmentioning

confidence: 99%

“…The gene regulatory components recruited by lncRNAs include repressive (e.g. polycomb proteins) and activating complexes (e.g.transcription factor IIB) (Bonasio et al, 2010;Y. W. Huang et al, 2010).…”

Section: Lncrnas and Their Mechanisms Of Actionmentioning

confidence: 99%

The role of long non-coding RNAs in hepatitis B virus-related hepatocellular carcinoma

2016

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Mimicry of molecular pretenders: The terminal structures of satellites associated with plant RNA viruses

Cited by 18 publications

References 72 publications

A Viral Satellite RNA Induces Yellow Symptoms on Tobacco by Targeting a Gene Involved in Chlorophyll Biosynthesis using the RNA Silencing Machinery

A Viral Satellite RNA Induces Yellow Symptoms on Tobacco by Targeting a Gene Involved in Chlorophyll Biosynthesis using the RNA Silencing Machinery

Hsp90 Interacts Specifically with Viral RNA and Differentially Regulates Replication Initiation of Bamboo mosaic virus and Associated Satellite RNA

The role of long non-coding RNAs in hepatitis B virus-related hepatocellular carcinoma

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