Structural Alteration of a BYDV-like Translation Element (BTE) That Attenuates P35 Expression in Three Mild Tobacco Bushy Top Virus Isolates

Overview

Journal Sci Rep

Specialty Science

Date 2017 Jun 25

PMID 28646195

Citations 8

Authors

Deya Wang

Chengming Yu

Shanshan Liu

Guolu Wang

Kerong Shi

Xiangdong Li

Xuefeng Yuan

Affiliations

Soon will be listed here.

Abstract

To identify the molecular effects of Tobacco bushy top virus (TBTV) evolution on the degeneration of tobacco bushy top disease, three TBTV isolates with mild virulence were compared with wild-type TBTV to assess the translation of p35, which relies on a BYDV-like translation element (BTE) in a cap-independent manner. The in vitro expression of p35 in the mild isolates was only 20% to 40% of the expression observed in wt TBTV. Based on translation data from chimeric TBTV RNA, low-level p35 expression in the three mild isolates was associated with two regions: the 5' terminal 500 nt region (RI) and the 3' internal region (RV), which included the BTE. For the RV region, low level p35 expression was mainly associated with structural alterations of the BTE instead of specific sequence mutations within the BTE based on SHAPE structural probing and mutation analysis. Additionally, structural alteration of the TBTV BTE resulted from mutations outside of the BTE, implying structural complexity of the local region surrounding the BTE. This study is the first report on the structural alteration of the 3' cap-independent translation element among different isolates of a given RNA virus, which is associated with variations in viral virulence.

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References

Holland J, Spindler K, Horodyski F, Grabau E, Nichol S, VandePol S . Rapid evolution of RNA genomes. Science. 1982; 215(4540):1577-85. DOI: 10.1126/science.7041255. View

Guo L, Allen E, Miller W . Base-pairing between untranslated regions facilitates translation of uncapped, nonpolyadenylated viral RNA. Mol Cell. 2001; 7(5):1103-9. DOI: 10.1016/s1097-2765(01)00252-0. View

Ryabov E, Robinson D, Taliansky M . Umbravirus-encoded proteins both stabilize heterologous viral RNA and mediate its systemic movement in some plant species. Virology. 2001; 288(2):391-400. DOI: 10.1006/viro.2001.1078. 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

Ryabov E, Roberts I, Palukaitis P, Taliansky M . Host-specific cell-to-cell and long-distance movements of cucumber mosaic virus are facilitated by the movement protein of groundnut rosette virus. Virology. 1999; 260(1):98-108. DOI: 10.1006/viro.1999.9806. View

Gao F, Kasprzak W, Szarko C, Shapiro B, Simon A . The 3' untranslated region of Pea Enation Mosaic Virus contains two T-shaped, ribosome-binding, cap-independent translation enhancers. J Virol. 2014; 88(20):11696-712. PMC: 4178710. DOI: 10.1128/JVI.01433-14. View

Jackson R, Hellen C, Pestova T . The mechanism of eukaryotic translation initiation and principles of its regulation. Nat Rev Mol Cell Biol. 2010; 11(2):113-27. PMC: 4461372. DOI: 10.1038/nrm2838. View

Villordo S, Alvarez D, Gamarnik A . A balance between circular and linear forms of the dengue virus genome is crucial for viral replication. RNA. 2010; 16(12):2325-35. PMC: 2995394. DOI: 10.1261/rna.2120410. View

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

10.

Liu F, Tan G, Li X, Chen H, Li R, Li F . Simultaneous detection of four causal agents of tobacco bushy top disease by a multiplex one-step RT-PCR. J Virol Methods. 2014; 205:99-103. DOI: 10.1016/j.jviromet.2014.05.003. View

11.

Taliansky M, Robinson D . Molecular biology of umbraviruses: phantom warriors. J Gen Virol. 2003; 84(Pt 8):1951-1960. DOI: 10.1099/vir.0.19219-0. View

12.

Wells S, Hillner P, Vale R, Sachs A . Circularization of mRNA by eukaryotic translation initiation factors. Mol Cell. 1998; 2(1):135-40. DOI: 10.1016/s1097-2765(00)80122-7. View

13.

Firth A, Brierley I . Non-canonical translation in RNA viruses. J Gen Virol. 2012; 93(Pt 7):1385-1409. PMC: 3542737. DOI: 10.1099/vir.0.042499-0. View

14.

Gao F, Kasprzak W, Stupina V, Shapiro B, Simon A . A ribosome-binding, 3' translational enhancer has a T-shaped structure and engages in a long-distance RNA-RNA interaction. J Virol. 2012; 86(18):9828-42. PMC: 3446580. DOI: 10.1128/JVI.00677-12. View

15.

Domingo E, Sheldon J, Perales C . Viral quasispecies evolution. Microbiol Mol Biol Rev. 2012; 76(2):159-216. PMC: 3372249. DOI: 10.1128/MMBR.05023-11. View

16.

Gao F, Gulay S, Kasprzak W, Dinman J, Shapiro B, Simon A . The kissing-loop T-shaped structure translational enhancer of Pea enation mosaic virus can bind simultaneously to ribosomes and a 5' proximal hairpin. J Virol. 2013; 87(22):11987-2002. PMC: 3807929. DOI: 10.1128/JVI.02005-13. View

17.

Aitken C, Lorsch J . A mechanistic overview of translation initiation in eukaryotes. Nat Struct Mol Biol. 2012; 19(6):568-76. DOI: 10.1038/nsmb.2303. View

18.

Andino R, Domingo E . Viral quasispecies. Virology. 2015; 479-480:46-51. PMC: 4826558. DOI: 10.1016/j.virol.2015.03.022. View

19.

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

20.

Nicholson B, White K . 3' Cap-independent translation enhancers of positive-strand RNA plant viruses. Curr Opin Virol. 2012; 1(5):373-80. DOI: 10.1016/j.coviro.2011.10.002. View