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Pathogens 2019, 8(1), 28; https://doi.org/10.3390/pathogens8010028

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

1
Department of Plant Pathology and Microbiology, Iowa State University, Ames, IA 50011, USA
2
Department of Genetics, Development and Cell Biology, Iowa State University, Ames, IA 50011, USA
3
Department of Biochemistry, Biophysics and Molecular Biology, Iowa State University, Ames, IA 50011, USA
4
Yerkes National Primate Research Center, Emory Vaccine Center 2009, 954 Gatewood Rd NE, Atlanta, GA 30329, USA
5
Dura-Line, 1355 Carden Farm Dr., Clinton, TN 37716, USA
6
Department of Orthopaedic Surgery, Washington University School of Medicine, St. Louis, MO 63110, USA
7
Interdepartmental Plant Biology Program, Iowa State University, Ames, IA 50011, USA
8
Department of Plant Pathology, University of Wisconsin, Madison, WI 53706, USA
9
Laboratory of Molecular Diagnostic and Biochemistry, Bonin Research Center, Plant Breeding and Acclimatization Institute–National Research Institute, 76-009 Bonin, Poland
10
Department of Veterinary Microbiology and Preventive Medicine, College of Veterinary Medicine, Iowa State University, Ames, IA 50011, USA
*
Author to whom correspondence should be addressed.
Received: 9 January 2019 / Revised: 3 February 2019 / Accepted: 23 February 2019 / Published: 28 February 2019
(This article belongs to the Special Issue Plant-Pathogen Interactions)
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Abstract

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. View Full-Text
Keywords: 5′ cap; translation initiation; RNA binding protein; Tombusviridae; plant virus; 3′ untranslated region; pseudoknot; cap-independent translation 5′ cap; translation initiation; RNA binding protein; Tombusviridae; plant virus; 3′ untranslated region; pseudoknot; cap-independent translation
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Kraft, J.J.; Peterson, M.S.; Cho, S.K.; Wang, Z.; Hui, A.; Rakotondrafara, A.M.; Treder, K.; Miller, C.L.; Miller, W.A. The 3′ Untranslated Region of a Plant Viral RNA Directs Efficient Cap-Independent Translation in Plant and Mammalian Systems. Pathogens 2019, 8, 28.

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