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Three-Dimensional Structure of Victorivirus Hvv190s Suggests Coat Proteins in Most Totiviruses Share a Conserved Core Sarah E

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Three-Dimensional Structure of Victorivirus Hvv190s Suggests Coat Proteins in Most Totiviruses Share a Conserved Core Sarah E University of Kentucky UKnowledge Plant Pathology Faculty Publications Plant Pathology 3-14-2013 Three-dimensional Structure of Victorivirus HvV190S Suggests Coat Proteins in Most Totiviruses Share a Conserved Core Sarah E. Dunn University of California - San Diego Hua Li University of Kentucky, [email protected] Giovanni Cardone University of California - San Diego Max L. Nibert Harvard University Said A. Ghabrial University of Kentucky, [email protected] See next page for additional authors Right click to open a feedback form in a new tab to let us know how this document benefits oy u. Follow this and additional works at: https://uknowledge.uky.edu/plantpath_facpub Part of the Plant Pathology Commons Repository Citation Dunn, Sarah E.; Li, Hua; Cardone, Giovanni; Nibert, Max L.; Ghabrial, Said A.; and Baker, Timothy S., "Three-dimensional Structure of Victorivirus HvV190S Suggests Coat Proteins in Most Totiviruses Share a Conserved Core" (2013). Plant Pathology Faculty Publications. 9. https://uknowledge.uky.edu/plantpath_facpub/9 This Article is brought to you for free and open access by the Plant Pathology at UKnowledge. It has been accepted for inclusion in Plant Pathology Faculty Publications by an authorized administrator of UKnowledge. For more information, please contact [email protected]. Authors Sarah E. Dunn, Hua Li, Giovanni Cardone, Max L. Nibert, Said A. Ghabrial, and Timothy S. Baker Three-dimensional Structure of Victorivirus HvV190S Suggests Coat Proteins in Most Totiviruses Share a Conserved Core Notes/Citation Information Published in PLoS Pathogens, v. 9, no. 3, e1003225. © 2013 Dunn et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Digital Object Identifier (DOI) http://dx.doi.org/10.1371/journal.ppat.1003225 This article is available at UKnowledge: https://uknowledge.uky.edu/plantpath_facpub/9 Three-dimensional Structure of Victorivirus HvV190S Suggests Coat Proteins in Most Totiviruses Share a Conserved Core Sarah E. Dunn1, Hua Li2, Giovanni Cardone1, Max L. Nibert3, Said A. Ghabrial2*, Timothy S. Baker1,4* 1 Department of Chemistry and Biochemistry, University of California San Diego, La Jolla, California, United States of America, 2 Department of Plant Pathology, University of Kentucky, Lexington, Kentucky, United States of America, 3 Department of Microbiology and Immunobiology, Harvard Medical School, Boston, Massachusetts, United States of America, 4 Division of Biological Sciences, University of California San Diego, La Jolla, California, United States of America Abstract Double-stranded (ds)RNA fungal viruses are currently assigned to six different families. Those from the family Totiviridae are characterized by nonsegmented genomes and single-layer capsids, 300–450 A˚ in diameter. Helminthosporium victoriae virus 190S (HvV190S), prototype of recently recognized genus Victorivirus, infects the filamentous fungus Helminthosporium victoriae (telomorph: Cochliobolus victoriae), which is the causal agent of Victoria blight of oats. The HvV190S genome is 5179 bp long and encompasses two large, slightly overlapping open reading frames that encode the coat protein (CP, 772 aa) and the RNA-dependent RNA polymerase (RdRp, 835 aa). To our present knowledge, victoriviruses uniquely express their RdRps via a coupled termination–reinitiation mechanism that differs from the well-characterized Saccharomyces cerevisiae virus L-A (ScV-L-A, prototype of genus Totivirus), in which the RdRp is expressed as a CP/RdRp fusion protein due to ribosomal frameshifting. Here, we used transmission electron cryomicroscopy and three-dimensional image reconstruction to determine the structures of HvV190S virions and two types of virus-like particles (capsids lacking dsRNA and capsids lacking both dsRNA and RdRp) at estimated resolutions of 7.1, 7.5, and 7.6 A˚, respectively. The HvV190S capsid is thin and smooth, and contains 120 copies of CP arranged in a ‘‘T = 2’’ icosahedral lattice characteristic of ScV-L-A and other dsRNA viruses. For aid in our interpretations, we developed and used an iterative segmentation procedure to define the boundaries of the two, chemically identical CP subunits in each asymmetric unit. Both subunits have a similar fold, but one that differs from ScV-L-A in many details except for a core a-helical region that is further predicted to be conserved among many other totiviruses. In particular, we predict the structures of other victoriviruses to be highly similar to HvV190S and the structures of most if not all totiviruses including, Leishmania RNA virus 1, to be similar as well. Citation: Dunn SE, Li H, Cardone G, Nibert ML, Ghabrial SA, et al. (2013) Three-dimensional Structure of Victorivirus HvV190S Suggests Coat Proteins in Most Totiviruses Share a Conserved Core. PLoS Pathog 9(3): e1003225. doi:10.1371/journal.ppat.1003225 Editor: Jack Johnson, The Scripps Research Institute, United States of America Received September 28, 2012; Accepted January 19, 2013; Published March 14, 2013 Copyright: ß 2013 Dunn et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This work was supported in part by NIH grants R37 GM033050 and 1S10 RR020016 as well as support from UCSD and the Agouron Foundation (all to TSB) and by grant KSEF-2178-RDE-013 from the Kentucky Science & Engineering Foundation (to SAG). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected] (SAG); [email protected] (TSB) Introduction all these viruses have an overall, spherical morphology and are constructed from an icosahedrally symmetric arrangement of one The encapsidated, double-stranded (ds)RNA viruses infect a or more capsid proteins. Most of these capsids are single-shelled wide range of hosts including bacteria, plants, fungi, insects, and and range in diameter from ,300 to ,450 A˚ , with the exception humans and other vertebrates [1,2]. Viruses that infect and of the larger, double-shelled reoviruses (600–850 A˚ ) [4]. All the replicate in fungi (mycoviruses) have no known natural vectors and single-shelled capsids (except those of chrysoviruses), as well as the are spread vertically or horizontally by intracellular means [3,4]. inner capsids of reoviruses, consist of 120, chemically identical Despite lacking an extracellular phase [4], mycoviruses are subunits arranged in a so-called ‘‘T = 2’’, icosahedral lattice [10]. successfully disseminated through all major groups of fungi [5,6]. In addition, all dsRNA viruses, including those that infect fungi, As such, fungal viruses have been touted as potentially beneficial, must package one or more virally encoded RNA-dependent RNA biological control agents of pathogenic fungi that infect econom- polymerase (RdRp) molecules that replicate and transcribe the ically important agricultural crops. This has added significance viral genome, since dsRNA cannot function as mRNA [1]. because fungicides in current use pose health hazards and Totiviruses are the simplest encapsidated dsRNA mycoviruses environmental risks [4]. in containing a single genome segment that encodes only two Encapsidated dsRNA mycoviruses are currently classified in six proteins: coat protein (CP) and either RdRp or a CP/RdRp fusion families. Each member of family Totiviridae has a nonsegmented [9]. Members of family Totiviridae therefore provide a simple model genome, but members of families Partitiviridae, Megabirnaviridae, system for studying mycoviruses, as well as dsRNA viruses more Chrysoviridae, Quadriviridae, and Reoviridae have genomes comprising generally. Family Totiviridae comprises five current genera: 2, 2, 4, 4, and 11–12 segments, respectively [4,7–9]. The capsids of Totivirus, Victorivirus, Giardiavirus, Leishmaniavirus, and Trichomonasvirus PLOS Pathogens | www.plospathogens.org 1 March 2013 | Volume 9 | Issue 3 | e1003225 3-dimensional Structure of Victorivirus HvV190S Author Summary consequent to ribosomal frameshifting [25]. HvV190S, in contrast, expresses its RdRp as a separate, nonfused protein, using a Of the known dsRNA fungal viruses, the best characterized coupled termination/reinitiation (stop/restart) strategy that in- is Saccharomyces cerevisiae virus L-A (ScV-L-A), prototype volves an AUGA motif in which CP terminates at UGA and of the genus Totivirus, family Totiviridae. Until the current translation restarts at AUG to make RdRp. [26,27]. The RNA study, there have been no subnanometer structures of sequence requirements for the stop/restart mechanism include a dsRNA fungal viruses from the genus Victorivirus, which is 32-nt region that contains a predicted pseudoknot and lies close to the largest in family Totiviridae. The 3D cryo-reconstruction the downstream AUGA motif [27]. presented here of prototype victorivirus Helminthospor- ˚ Though the HvV190S genome contains just two ORFs, SDS- ium victoriae virus 190S (HvV190S) approaches 7-A PAGE of purified HvV190S virions reveals the presence of three resolution and shows the asymmetric unit of the capsid forms of CP, which have been shown by peptide analysis to be closely is a dimer
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