The Triticum Mosaic Virus Internal Ribosome Entry Site Relies on a Picornavirus-Like YX-AUG Motif To Designate the Preferred Translation Initiation Site and To Likely Target the 18S rRNA

Jaramillo-Mesa, Helena; Gannon, Megan; Holshbach, Elijah; Zhang, Jincan; Roberts, R. H.; Buettner, Matthew J.; Rakotondrafara, Aurélie M.

doi:10.1128/jvi.01705-18

Cited by 14 publications

(35 citation statements)

References 54 publications

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“…On the RNA side of the interaction, we know of one example of structural similarity between viruses of different kingdoms that facilitates cap-independent translation. In this case, the large IRES in the 5′ UTR of Triticum mosaic virus ( Potyviridae ) contains the same Y n X m -AUG motif that is present in IRESes of picornaviruses [56], which infect vertebrates.…”

Section: Discussionmentioning

confidence: 99%

The 3′ Untranslated Region of a Plant Viral RNA Directs Efficient Cap-Independent Translation in Plant and Mammalian Systems

et al. 2019

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Many plant viral RNA genomes lack a 5′ cap, and instead are translated via a cap-independent translation element (CITE) in the 3′ untranslated region (UTR). The panicum mosaic virus-like CITE (PTE), found in many plant viral RNAs, binds and requires the cap-binding translation initiation factor eIF4E to facilitate translation. eIF4E is structurally conserved between plants and animals, so we tested cap-independent translation efficiency of PTEs of nine plant viruses in plant and mammalian systems. The PTE from thin paspalum asymptomatic virus (TPAV) facilitated efficient cap-independent translation in wheat germ extract, rabbit reticulocyte lysate, HeLa cell lysate, and in oat and mammalian (BHK) cells. Human eIF4E bound the TPAV PTE but not a PTE that did not stimulate cap-independent translation in mammalian extracts or cells. Selective 2′-hydroxyl acylation analyzed by primer extension (SHAPE) footprinting revealed that both human and wheat eIF4E protected the conserved guanosine (G)-rich domain in the TPAV PTE pseudoknot. The central G plays a key role, as it was found to be required for translation and protection from SHAPE modification by eIF4E. These results provide insight on how plant viruses gain access to the host’s translational machinery, an essential step in infection, and raise the possibility that similar PTE-like mechanisms may exist in mRNAs of mammals or their viruses.

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Section: Discussionmentioning

confidence: 99%

The 3′ Untranslated Region of a Plant Viral RNA Directs Efficient Cap-Independent Translation in Plant and Mammalian Systems

et al. 2019

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“…The mechanism of operation of this IRES is poorly understood, however it has been shown to bind eIF4G [ 155 ]. This, as well as the presence of polypyrimidine sequence important for translation in front of the initiation codon, possibly makes it similar to picornavirus IRESs of types I and II [ 156 ], but conclusion is not final yet.…”

Section: Internal Translation Initiationmentioning

confidence: 99%

Non-Canonical Translation Initiation Mechanisms Employed by Eukaryotic Viral mRNAs

Sorokin

Vassilenko

Terenin

et al. 2021

Biochemistry Moscow

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Viruses exploit the translation machinery of an infected cell to synthesize their proteins. Therefore, viral mRNAs have to compete for ribosomes and translation factors with cellular mRNAs. To succeed, eukaryotic viruses adopt multiple strategies. One is to circumvent the need for m 7 G-cap through alternative instruments for ribosome recruitment. These include internal ribosome entry sites (IRESs), which make translation independent of the free 5′ end, or cap-independent translational enhancers (CITEs), which promote initiation at the uncapped 5′ end, even if located in 3′ untranslated regions (3′ UTRs). Even if a virus uses the canonical cap-dependent ribosome recruitment, it can still perturb conventional ribosomal scanning and start codon selection. The pressure for genome compression often gives rise to internal and overlapping open reading frames. Their translation is initiated through specific mechanisms, such as leaky scanning, 43S sliding, shunting, or coupled termination-reinitiation. Deviations from the canonical initiation reduce the dependence of viral mRNAs on translation initiation factors, thereby providing resistance to antiviral mechanisms and cellular stress responses. Moreover, viruses can gain advantage in a competition for the translational machinery by inactivating individual translational factors and/or replacing them with viral counterparts. Certain viruses even create specialized intracellular “translation factories”, which spatially isolate the sites of their protein synthesis from cellular antiviral systems, and increase availability of translational components. However, these virus-specific mechanisms may become the Achilles’ heel of a viral life cycle. Thus, better understanding of the unconventional mechanisms of viral mRNA translation initiation provides valuable insight for developing new approaches to antiviral therapy.

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“…It recruits eIF4G/iso4G with higher affinity than eIF4E/iso4E (Roberts, Mayberry, Browning, & Rakotondrafara, 2017). Moreover, a polypyrimidine stretch upstream of the actual translation start codon may basepair with the 18S rRNA (Jaramillo‐Mesa et al, 2019), another typical feature of animal IRESs. Taken together, while 3' CITEs and 5' IRESs are characteristic for plant and animal viruses, respectively, it now appears that both paradigms occur in both kingdoms.…”

Section: Rna Featuresmentioning

confidence: 99%

Translational gene regulation in plants: A green new deal

2020

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The molecular machinery for protein synthesis is profoundly similar between plants and other eukaryotes. Mechanisms of translational gene regulation are embedded into the broader network of RNA-level processes including RNA quality control and RNA turnover. However, over eons of their separate history, plants acquired new components, dropped others, and generally evolved an alternate way of making the parts list of protein synthesis work. Research over the past 5 years has unveiled how plants utilize translational control to defend themselves against viruses, regulate translation in response to metabolites, and reversibly adjust translation to a wide variety of environmental parameters. Moreover, during seed and pollen development plants make use of RNA granules and other translational controls to underpin developmental transitions between quiescent and metabolically active stages. The economics of resource allocation over the daily light-dark cycle also include controls over cellular protein synthesis. Important new insights into translational control on cytosolic ribosomes continue to emerge from studies of translational control mechanisms in viruses. Finally, sketches of coherent signaling pathways that connect external stimuli with a translational response are emerging, anchored in part around TOR and GCN2 kinase signaling networks. These again reveal some mechanisms that are familiar and others that are different from other eukaryotes, motivating deeper studies on translational control in plants.

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The Triticum Mosaic Virus Internal Ribosome Entry Site Relies on a Picornavirus-Like YX-AUG Motif To Designate the Preferred Translation Initiation Site and To Likely Target the 18S rRNA

Cited by 14 publications

References 54 publications

The 3′ Untranslated Region of a Plant Viral RNA Directs Efficient Cap-Independent Translation in Plant and Mammalian Systems

The 3′ Untranslated Region of a Plant Viral RNA Directs Efficient Cap-Independent Translation in Plant and Mammalian Systems

Non-Canonical Translation Initiation Mechanisms Employed by Eukaryotic Viral mRNAs

Translational gene regulation in plants: A green new deal

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