Structural Plasticity of Barley Yellow Dwarf Virus-like Cap-independent Translation Elements in Four Genera of Plant Viral RNAs

Overview

Journal Virology

Specialty Microbiology

Date 2010 Apr 16

PMID 20392470

Citations 36

Authors

Zhaohui Wang

Jelena J Kraft

Alice Y Hui

W Allen Miller

Affiliations

Soon will be listed here.

Abstract

The 3' untranslated regions (UTRs) of many plant viral RNAs contain cap-independent translation elements (3' CITEs). Among the 3' CITEs, the Barley yellow dwarf virus (BYDV)-like translation elements (BTEs) form a structurally variable and widely distributed group. Viruses in three genera were known to harbor 3' BTEs, defined by the presence of a 17-nt consensus sequence. To understand BTE function, knowledge of phylogenetically conserved structure is essential, yet the secondary structure has been determined only for the BYDV BTE. Here we show that Rose spring dwarf-associated luteovirus, and two viruses in a fourth genus, Umbravirus, contain functional BTEs, despite deviating in the 17nt consensus sequence. Structure probing by selective 2'-hydroxyl acylation and primer extension (SHAPE) revealed conserved and highly variable structures in BTEs in all four genera. We conclude that BTEs tolerate striking evolutionary plasticity in structure, while retaining the ability to stimulate cap-independent translation.

Citing Articles

Structure of saguaro cactus virus 3' translational enhancer mimics 5' cap for eIF4E binding.

Ojha M, Vogt J, Das N, Redmond E, Singh K, Banna H Proc Natl Acad Sci U S A. 2024; 121(4):e2313677121.

PMID: 38241435 PMC: 10823258. DOI: 10.1073/pnas.2313677121.

Crystal structure of a cap-independent translation enhancer RNA.

Lewicka A, Roman C, Jones S, Disare M, Rice P, Piccirilli J Nucleic Acids Res. 2023; 51(16):8891-8907.

PMID: 37548413 PMC: 10484670. DOI: 10.1093/nar/gkad649.

Engineering resistance against Cucumber mosaic virus in through virus derived transgene expressing hairpin RNA.

Vinodhini J, Rajendran L, Karthikeyan G 3 Biotech. 2023; 13(5):143.

PMID: 37124993 PMC: 10140202. DOI: 10.1007/s13205-023-03576-1.

Different RNA Elements Control Viral Protein Synthesis in Polerovirus Isolates Evolved in Separate Geographical Regions.

Miras M, Aranda M, Truniger V Int J Mol Sci. 2022; 23(20).

PMID: 36293360 PMC: 9603980. DOI: 10.3390/ijms232012503.

Eukaryotic initiation factor 4F promotes a reorientation of eukaryotic initiation factor 3 binding on the 5' and the 3' UTRs of barley yellow dwarf virus mRNA.

Powell P, Bhardwaj U, Goss D Nucleic Acids Res. 2022; 50(9):4988-4999.

PMID: 35446425 PMC: 9122605. DOI: 10.1093/nar/gkac284.

References

Filbin M, Kieft J . Toward a structural understanding of IRES RNA function. Curr Opin Struct Biol. 2009; 19(3):267-76. PMC: 2757110. DOI: 10.1016/j.sbi.2009.03.005. View

Wang S, Guo L, Allen E, Miller W . A potential mechanism for selective control of cap-independent translation by a viral RNA sequence in cis and in trans. RNA. 1999; 5(6):728-38. PMC: 1369800. DOI: 10.1017/s1355838299981979. View

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

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

Mo X, Qin X, Wu J, Yang C, Wu J, Duan Y . Complete nucleotide sequence and genome organization of a Chinese isolate of tobacco bushy top virus. Arch Virol. 2003; 148(2):389-97. DOI: 10.1007/s00705-002-0919-y. View

Miller W, Wang Z, Treder K . The amazing diversity of cap-independent translation elements in the 3'-untranslated regions of plant viral RNAs. Biochem Soc Trans. 2007; 35(Pt 6):1629-33. PMC: 3081161. DOI: 10.1042/BST0351629. View

Sarawaneeyaruk S, Iwakawa H, Mizumoto H, Murakami H, Kaido M, Mise K . Host-dependent roles of the viral 5' untranslated region (UTR) in RNA stabilization and cap-independent translational enhancement mediated by the 3' UTR of Red clover necrotic mosaic virus RNA1. Virology. 2009; 391(1):107-18. DOI: 10.1016/j.virol.2009.05.037. View

Rakotondrafara A, Polacek C, Harris E, Miller W . Oscillating kissing stem-loop interactions mediate 5' scanning-dependent translation by a viral 3'-cap-independent translation element. RNA. 2006; 12(10):1893-906. PMC: 1581982. DOI: 10.1261/rna.115606. View

Truniger V, Nieto C, Gonzalez-Ibeas D, Aranda M . Mechanism of plant eIF4E-mediated resistance against a Carmovirus (Tombusviridae): cap-independent translation of a viral RNA controlled in cis by an (a)virulence determinant. Plant J. 2008; 56(5):716-27. DOI: 10.1111/j.1365-313X.2008.03630.x. View

10.

Pettit Kneller E, Rakotondrafara A, Miller W . Cap-independent translation of plant viral RNAs. Virus Res. 2005; 119(1):63-75. PMC: 1880899. DOI: 10.1016/j.virusres.2005.10.010. View

11.

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

12.

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

13.

Jan E . Divergent IRES elements in invertebrates. Virus Res. 2005; 119(1):16-28. DOI: 10.1016/j.virusres.2005.10.011. View

14.

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

15.

Wilkinson K, Merino E, Weeks K . Selective 2'-hydroxyl acylation analyzed by primer extension (SHAPE): quantitative RNA structure analysis at single nucleotide resolution. Nat Protoc. 2007; 1(3):1610-6. DOI: 10.1038/nprot.2006.249. View

16.

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

17.

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

18.

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

19.

Niepel M, Gallie D . Identification and characterization of the functional elements within the tobacco etch virus 5' leader required for cap-independent translation. J Virol. 1999; 73(11):9080-8. PMC: 112940. DOI: 10.1128/JVI.73.11.9080-9088.1999. View

20.

Mortimer S, Weeks K . A fast-acting reagent for accurate analysis of RNA secondary and tertiary structure by SHAPE chemistry. J Am Chem Soc. 2007; 129(14):4144-5. DOI: 10.1021/ja0704028. View