3' Cap-independent Translation Enhancers of Plant Viruses

Overview

Journal Annu Rev Microbiol

Publisher Annual Reviews

Specialty Microbiology

Date 2013 May 21

PMID 23682606

Citations 113

Authors

Anne E Simon

W Allen Miller

Affiliations

Soon will be listed here.

Abstract

In the absence of a 5' cap, plant positive-strand RNA viruses have evolved a number of different elements in their 3' untranslated region (UTR) to attract initiation factors and/or ribosomes to their templates. These 3' cap-independent translational enhancers (3' CITEs) take different forms, such as I-shaped, Y-shaped, T-shaped, or pseudoknotted structures, or radiate multiple helices from a central hub. Common features of most 3' CITEs include the ability to bind a component of the translation initiation factor eIF4F complex and to engage in an RNA-RNA kissing-loop interaction with a hairpin loop located at the 5' end of the RNA. The two T-shaped structures can bind to ribosomes and ribosomal subunits, with one structure also able to engage in a simultaneous long-distance RNA-RNA interaction. Several of these 3' CITEs are interchangeable and there is evidence that natural recombination allows exchange of modular CITE units, which may overcome genetic resistance or extend the virus's host range.

Citing Articles

The pseudoknot structure of a viral RNA reveals a conserved mechanism for programmed exoribonuclease resistance.

Gezelle J, Korn S, McDonald J, Gong Z, Erickson A, Huang C bioRxiv. 2025; .

PMID: 39763890 PMC: 11702639. DOI: 10.1101/2024.12.17.628992.

Edited eukaryotic translation initiation factors confer resistance against maize lethal necrosis.

Wen Z, Lu F, Jung M, Humbert S, Marshall L, Hastings C Plant Biotechnol J. 2024; 22(12):3523-3535.

PMID: 39403866 PMC: 11606411. DOI: 10.1111/pbi.14472.

Non-canonical translation in cancer: significance and therapeutic potential of non-canonical ORFs, mA-modification, and circular RNAs.

Deng X, Yu Y, Jin Y Cell Death Discov. 2024; 10(1):412.

PMID: 39333489 PMC: 11437038. DOI: 10.1038/s41420-024-02185-y.

Non-canonical mRNA translation initiation in cell stress and cancer.

Mahe M, Rios-Fuller T, Katsara O, Schneider R NAR Cancer. 2024; 6(2):zcae026.

PMID: 38828390 PMC: 11140632. DOI: 10.1093/narcan/zcae026.

Host-like RNA Elements Regulate Virus Translation.

Khan D, Fox P Viruses. 2024; 16(3).

PMID: 38543832 PMC: 10976276. DOI: 10.3390/v16030468.

References

Robaglia C, Caranta C . Translation initiation factors: a weak link in plant RNA virus infection. Trends Plant Sci. 2005; 11(1):40-5. DOI: 10.1016/j.tplants.2005.11.004. View

Scheets K, Redinbaugh M . Infectious cDNA transcripts of Maize necrotic streak virus: infectivity and translational characteristics. Virology. 2006; 350(1):171-83. DOI: 10.1016/j.virol.2006.02.004. View

Reineke L, Lloyd R . Animal virus schemes for translation dominance. Curr Opin Virol. 2012; 1(5):363-72. PMC: 3272495. DOI: 10.1016/j.coviro.2011.10.009. View

Stupina V, Yuan X, Meskauskas A, Dinman J, Simon A . Ribosome binding to a 5' translational enhancer is altered in the presence of the 3' untranslated region in cap-independent translation of turnip crinkle virus. J Virol. 2011; 85(10):4638-53. PMC: 3126203. DOI: 10.1128/JVI.00005-11. View

Yuan X, Shi K, Young M, Simon A . The terminal loop of a 3' proximal hairpin plays a critical role in replication and the structure of the 3' region of Turnip crinkle virus. Virology. 2010; 402(2):271-80. PMC: 2891086. DOI: 10.1016/j.virol.2010.03.036. View

Yoshii M, Yoshioka N, Ishikawa M, Naito S . Isolation of an Arabidopsis thaliana mutant in which the multiplication of both cucumber mosaic virus and turnip crinkle virus is affected. J Virol. 1998; 72(11):8731-7. PMC: 110288. DOI: 10.1128/JVI.72.11.8731-8737.1998. View

Karetnikov A, Keranen M, Lehto K . Role of the RNA2 3' non-translated region of Blackcurrant reversion nepovirus in translational regulation. Virology. 2006; 354(1):178-91. DOI: 10.1016/j.virol.2006.06.028. View

Mizumoto H, Tatsuta M, Kaido M, Mise K, Okuno T . Cap-independent translational enhancement by the 3' untranslated region of red clover necrotic mosaic virus RNA1. J Virol. 2003; 77(22):12113-21. PMC: 254280. DOI: 10.1128/jvi.77.22.12113-12121.2003. View

Treder K, Pettit Kneller E, Allen E, Wang Z, Browning K, Miller W . The 3' cap-independent translation element of Barley yellow dwarf virus binds eIF4F via the eIF4G subunit to initiate translation. RNA. 2007; 14(1):134-47. PMC: 2151041. DOI: 10.1261/rna.777308. View

10.

Nieto C, Rodriguez-Moreno L, Rodriguez-Hernandez A, Aranda M, Truniger V . Nicotiana benthamiana resistance to non-adapted Melon necrotic spot virus results from an incompatible interaction between virus RNA and translation initiation factor 4E. Plant J. 2011; 66(3):492-501. DOI: 10.1111/j.1365-313X.2011.04507.x. View

11.

Wang Z, Kraft J, Hui A, Miller W . Structural plasticity of Barley yellow dwarf virus-like cap-independent translation elements in four genera of plant viral RNAs. Virology. 2010; 402(1):177-86. PMC: 2905845. DOI: 10.1016/j.virol.2010.03.025. View

12.

Wang A, Krishnaswamy S . Eukaryotic translation initiation factor 4E-mediated recessive resistance to plant viruses and its utility in crop improvement. Mol Plant Pathol. 2012; 13(7):795-803. PMC: 6638641. DOI: 10.1111/j.1364-3703.2012.00791.x. View

13.

Ishibashi K, Naito S, Meshi T, Ishikawa M . An inhibitory interaction between viral and cellular proteins underlies the resistance of tomato to nonadapted tobamoviruses. Proc Natl Acad Sci U S A. 2009; 106(21):8778-83. PMC: 2678887. DOI: 10.1073/pnas.0809105106. View

14.

Fabian M, White K . Analysis of a 3'-translation enhancer in a tombusvirus: a dynamic model for RNA-RNA interactions of mRNA termini. RNA. 2006; 12(7):1304-14. PMC: 1484428. DOI: 10.1261/rna.69506. View

15.

Wang Z, Treder K, Miller W . Structure of a viral cap-independent translation element that functions via high affinity binding to the eIF4E subunit of eIF4F. J Biol Chem. 2009; 284(21):14189-202. PMC: 2682867. DOI: 10.1074/jbc.M808841200. View

16.

Carpenter C, Simon A . In vivo restoration of biologically active 3' ends of virus-associated RNAs by nonhomologous RNA recombination and replacement of a terminal motif. J Virol. 1996; 70(1):478-86. PMC: 189836. DOI: 10.1128/JVI.70.1.478-486.1996. View

17.

Batten J, Desvoyes B, Yamamura Y, Scholthof K . A translational enhancer element on the 3'-proximal end of the Panicum mosaic virus genome. FEBS Lett. 2006; 580(11):2591-7. DOI: 10.1016/j.febslet.2006.04.006. View

18.

Niedzwiecka A, Marcotrigiano J, Stepinski J, Jankowska-Anyszka M, Wyslouch-Cieszynska A, Dadlez M . Biophysical studies of eIF4E cap-binding protein: recognition of mRNA 5' cap structure and synthetic fragments of eIF4G and 4E-BP1 proteins. J Mol Biol. 2002; 319(3):615-35. DOI: 10.1016/S0022-2836(02)00328-5. View

19.

Dreher T, Miller W . Translational control in positive strand RNA plant viruses. Virology. 2005; 344(1):185-97. PMC: 1847782. DOI: 10.1016/j.virol.2005.09.031. View

20.

Shen R, Miller W . The 3' untranslated region of tobacco necrosis virus RNA contains a barley yellow dwarf virus-like cap-independent translation element. J Virol. 2004; 78(9):4655-64. PMC: 387721. DOI: 10.1128/jvi.78.9.4655-4664.2004. View