Differential use of 3’CITEs by the subgenomic RNA of Pea enation mosaic virus 2

Gao, Feng; Simon, Anne

doi:10.1016/j.virol.2017.07.021

Cited by 22 publications

(46 citation statements)

References 60 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…At 3 days postinfiltration (dpi), PEMV2Δp26 gRNA accumulation in local leaves (i.e., infiltrated leaves) was reduced 4-fold compared with WT PEMV2 (Fig. 1B), similarly to what was previously observed using Arabidopsis protoplasts (38) and further supporting the idea of a role for p26 in promoting genome stability independently of long-distance movement.…”

Section: Resultssupporting

confidence: 86%

“…Elimination of p27 expression had no effect on virus accumulation in Arabidopsis protoplasts in a previous study (38). In contrast, mutating the p26 start codon (PEMV2Δp26) resulted in a 4-fold decrease in viral RNA levels, suggesting that the p26 long-distance MP has an additional function that enhances accumulation of PEMV2 gRNA in single cells (38). To determine if similar effects would be apparent in planta, wild-type (WT) PEMV2 or PEMV2Δp26 was subjected to agroinfiltration along with the p14 RNA silencing suppressor from Pothos latent virus (PLV) (39) into leaves of young Nicotiana benthamiana plants, which are widely used as laboratory hosts for a large number of plant viruses.…”

Section: Resultsmentioning

confidence: 71%

“…1A) (37). Elimination of p27 expression had no effect on virus accumulation in Arabidopsis protoplasts in a previous study (38). In contrast, mutating the p26 start codon (PEMV2Δp26) resulted in a 4-fold decrease in viral RNA levels, suggesting that the p26 long-distance MP has an additional function that enhances accumulation of PEMV2 gRNA in single cells (38).…”

Section: Resultsmentioning

confidence: 90%

See 2 more Smart Citations

The Multifunctional Long-Distance Movement Protein of Pea Enation Mosaic Virus 2 Protects Viral and Host Transcripts from Nonsense-Mediated Decay

May

Johnson

Ilyas

et al. 2020

mBio

Self Cite

View full text Add to dashboard Cite

The nonsense-mediated decay (NMD) pathway presents a challenge for RNA viruses with termination codons that precede extended 3= untranslated regions (UTRs). The umbravirus Pea enation mosaic virus 2 (PEMV2) is a nonsegmented, positive-sense RNA virus with an unusually long 3= UTR that is susceptible to NMD. To establish a systemic infection, the PEMV2 long-distance movement protein p26 was previously shown to both stabilize viral RNAs and bind them for transport through the plant's vascular system. The current study demonstrated that p26 protects both viral and nonviral messenger RNAs from NMD. Although p26 localizes to both the cytoplasm and nucleolus, p26 exerts its anti-NMD effects exclusively in the cytoplasm independently of long-distance movement. Using a transcriptome-wide approach in the model plant Nicotiana benthamiana, p26 protected a subset of cellular NMD target transcripts, particularly those containing long, structured, GC-rich 3= UTRs. Furthermore, transcriptome sequencing (RNA-seq) revealed that the NMD pathway is highly dysfunctional during PEMV2 infection, with 1,820 (48%) of NMD targets increasing in abundance. Widespread changes in the host transcriptome are common during plant RNA virus infections, and these results suggest that, in at least some instances, virus-mediated NMD inhibition may be a major contributing factor. IMPORTANCE Nonsense-mediated decay (NMD) represents an RNA regulatory pathway that degrades both natural and faulty messenger RNAs with long 3= untranslated regions. NMD targets diverse families of RNA viruses, requiring that viruses counteract the NMD pathway for successful amplification in host cells. A protein required for long-distance movement of Pea enation mosaic virus 2 (PEMV2) is shown to also protect both viral and host mRNAs from NMD. RNA-seq analyses of the Nicotiana benthamiana transcriptome revealed that PEMV2 infection significantly impairs the host NMD pathway. RNA viruses routinely induce large-scale changes in host gene expression, and, like PEMV2, may use NMD inhibition to alter the host transcriptome in an effort to increase virus amplification.

show abstract

Section: Resultssupporting

confidence: 86%

Section: Resultsmentioning

confidence: 71%

Section: Resultsmentioning

confidence: 90%

See 1 more Smart Citation

The Multifunctional Long-Distance Movement Protein of Pea Enation Mosaic Virus 2 Protects Viral and Host Transcripts from Nonsense-Mediated Decay

May

Johnson

Ilyas

et al. 2020

mBio

Self Cite

View full text Add to dashboard Cite

show abstract

“…Functional base-pairing subsequently repositions 3 0 -CITE-loaded ribosomes proximal to 5 0 UTR structural elements (Nicholson and White 2014). Multiple 3 0 -CITEs in pea enation mosaic virus recruit both 40S and 60S subunits (Gao et al 2014(Gao et al , 2017. By adopting alternate conformations induced by viral RNA polymerase binding, CITEs also repress translation to facilitate RNA replication ).…”

Section: Mechanisms Of Cap-independent Translation Used By Virusesmentioning

confidence: 99%

Translational Control in Virus-Infected Cells

Stern-Ginossar

Thompson

Mathews

et al. 2018

Cold Spring Harb Perspect Biol

156

164

View full text Add to dashboard Cite

As obligate intracellular parasites, virus reproduction requires host cell functions. Despite variations in genome size and configuration, nucleic acid composition, and their repertoire of encoded functions, all viruses remain unconditionally dependent on the protein synthesis machinery resident within their cellular hosts to translate viral messenger RNAs (mRNAs). A complex signaling network responsive to physiological stress, including infection, regulates host translation factors and ribosome availability. Furthermore, access to the translation apparatus is patrolled by powerful host immune defenses programmed to restrict viral invaders. Here, we review the tactics and mechanisms used by viruses to appropriate control over host ribosomes, subvert host defenses, and dominate the infected cell translational landscape. These not only define aspects of infection biology paramount for virus reproduction, but continue to drive fundamental discoveries into how cellular protein synthesis is controlled in health and disease.

show abstract

“…Thus, it is imperative to understand the life cycle of MCMV, including translation, to identify molecular targets for genetic approaches to control this virus. All tombusvirids that have been studied contain a 3’ CITE [35, 40, 60, 69, 70], yet these are not predictable because the class of 3’ CITE a tombusvirid possesses does not always correlate with phylogeny [35, 52]. Moreover, we were unable to predict the class of 3’ CITE in MCMV RNA using ViennaFold or MFOLD.…”

Section: Discussionmentioning

confidence: 97%

The RNA of maize chlorotic mottle virus - the essential virus in maize lethal necrosis disease - is translated via a panicum mosaic virus-like cap-independent translation element

Carino

Scheets

Miller

2020

Preprint

View full text Add to dashboard Cite

Maize chlorotic mottle virus (MCMV) combines with a potyvirus in maize lethal necrosis disease (MLND), an emerging disease worldwide that often causes catastrophic yield loss. To inform resistance strategies, we characterized the translation initiation mechanism of MCMV. We report that, like other tombusvirids, MCMV RNA contains a cap-independent translation element (CITE) in its 3’ untranslated region (UTR). The MCMV 3’ CITE (MTE) was mapped to nucleotides 4164-4333 in the genomic RNA. SHAPE probing revealed that the MTE is a variant of the panicum mosaic virus-like 3’ CITE (PTE). Like the PTE, electrophoretic mobility shift assays (EMSAs) indicated that eukaryotic translation initiation factor 4E (eIF4E) binds the MTE despite the absence of a m7GpppN cap structure, which is normally required for eIF4E to bind RNA. The MTE interaction with eIF4E suggests eIF4E may be a soft target for engineered resistance to MCMV. Using a luciferase reporter system, mutagenesis to disrupt and restore base pairing revealed that the MTE interacts with the 5’ UTRs of both genomic RNA and the 3’-coterminal subgenomic RNA1 via long-distance kissing stem-loop base pairing to facilitate translation in wheat germ extract and in protoplasts. However, the MTE is a relatively weak stimulator of translation and has a weak, if any, pseudoknot, which is present in the most active PTEs. Most mutations designed to form a pseudoknot decreased translation activity. Mutations in the viral genome that reduced or restored translation prevented and restored virus replication, respectively, in maize protoplasts and in plants. We propose that MCMV, and some other positive strand RNA viruses, favors a weak translation element to allow highly efficient viral RNA synthesis.Author SummaryIn recent years, maize lethal necrosis disease has caused massive crop losses in East Africa and Ecuador. It has also emerged in East Asia. Maize chlorotic mottle virus (MCMV) infection is required for this disease. While some tolerant maize lines have been identified, there are no known resistance genes that confer full immunity to MCMV. In order to design better resistance strategies against MCMV, we focused on how the MCMV genome is translated, the first step of gene expression required for infection by all positive strand RNA viruses. We identified a structure (cap-independent translation element) in the 3’ untranslated region of the viral RNA genome that allows the virus to usurp a host translation initiation factor in a way that differs from host mRNA interactions with the translational machinery. This difference may guide engineering of – or breeding for – resistance to MCMV. Moreover, this work adds to the diversity of known eukaryotic translation initiation mechanisms, as it provides more information on mRNA structural features that permit noncanonical interaction with a translation factor. Finally, owing to the conflict between ribosomes translating and viral replicase copying viral RNA, we propose that MCMV has evolved a relatively weak translation element in order to permit highly efficient RNA synthesis, and that this replication-translation trade-off may apply to other positive strand RNA viruses.

show abstract

Differential use of 3’CITEs by the subgenomic RNA of Pea enation mosaic virus 2

Cited by 22 publications

References 60 publications

The Multifunctional Long-Distance Movement Protein of Pea Enation Mosaic Virus 2 Protects Viral and Host Transcripts from Nonsense-Mediated Decay

The Multifunctional Long-Distance Movement Protein of Pea Enation Mosaic Virus 2 Protects Viral and Host Transcripts from Nonsense-Mediated Decay

Translational Control in Virus-Infected Cells

The RNA of maize chlorotic mottle virus - the essential virus in maize lethal necrosis disease - is translated via a panicum mosaic virus-like cap-independent translation element

Contact Info

Product

Resources

About