University of Kentucky UKnowledge Plant Pathology Faculty Publications Plant Pathology 1-2-2017 The aF mily Rhabdoviridae: Mono- and Bipartite Negative-Sense RNA Viruses with Diverse Genome Organization and Common Evolutionary Origins Ralf G. Dietzgen The University of Queensland, Australia Hideki Kondo Okayama University, Japan Michael M. Goodin University of Kentucky, [email protected] Gael Kurath US Geological Survey Nikos Vasilakis University of Texas FRoigllohtw c licthiks t aond ope addn ait feionedalba wckork fosr mat :inh att nps://uknoew tab to lewtle usdg kne.ukowy .hedu/pow thilasn documtpath_faenct pubbenefits oy u. Part of the Genetics and Genomics Commons, Plant Pathology Commons, and the Viruses Commons Repository Citation Dietzgen, Ralf G.; Kondo, Hideki; Goodin, Michael M.; Kurath, Gael; and Vasilakis, Nikos, "The aF mily Rhabdoviridae: Mono- and Bipartite Negative-Sense RNA Viruses with Diverse Genome Organization and Common Evolutionary Origins" (2017). Plant Pathology Faculty Publications. 89. https://uknowledge.uky.edu/plantpath_facpub/89 This Review 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]. The Family Rhabdoviridae: Mono- and Bipartite Negative-Sense RNA Viruses with Diverse Genome Organization and Common Evolutionary Origins Notes/Citation Information Published in Virus Research, v. 227, p. 158-170. © 2016 Elsevier B.V. All rights reserved. This manuscript version is made available under the CC‐BY‐NC‐ND 4.0 license https://creativecommons.org/licenses/by-nc-nd/4.0/. The document available for download is the author's post-peer-review final draft of the ra ticle. Digital Object Identifier (DOI) https://doi.org/10.1016/j.virusres.2016.10.010 This review is available at UKnowledge: https://uknowledge.uky.edu/plantpath_facpub/89 HHS Public Access Author manuscript Author ManuscriptAuthor Manuscript Author Virus Res Manuscript Author . Author manuscript; Manuscript Author available in PMC 2018 January 02. Published in final edited form as: Virus Res. 2017 January 2; 227: 158–170. doi:10.1016/j.virusres.2016.10.010. The family Rhabdoviridae: mono- and bipartite negative-sense RNA viruses with diverse genome organization and common evolutionary origins Ralf G. Dietzgena,*, Hideki Kondob, Michael M. Goodinc, Gael Kurathd, and Nikos Vasilakise aQueensland Alliance for Agriculture and Food Innovation, The University of Queensland, St. Lucia, Queensland 4072, Australia bInstitute of Plant Science and Resources, Okayama University, Kurashiki 710-0046, Japan cDepartment of Plant Pathology, University of Kentucky, Lexington KY 40546, USA dU.S. Geological Survey, Western Fisheries Research Centre, Seattle WA, USA eInstitute for Human Infection and Immunity, University of Texas Medical Branch, Galveston TX, 77555, USA Abstract The family Rhabdoviridae consists of mostly enveloped, bullet-shaped or bacilliform viruses with a negative-sense, single-stranded RNA genome that infect vertebrates, invertebrates or plants. This ecological diversity is reflected by the diversity and complexity of their genomes. Five canonical structural protein genes are conserved in all rhabdoviruses, but may be overprinted, overlapped or interspersed with several novel and diverse accessory genes. This review gives an overview of the characteristics and diversity of rhabdoviruses, their taxonomic classification, replication mechanism, properties of classical rhabdoviruses such as rabies virus and rhabdoviruses with complex genomes, rhabdoviruses infecting aquatic species, and plant rhabdoviruses with both mono- and bipartite genomes. Graphical abstract *Corresponding author: Ralf G. Dietzgen, QAAFI, The University of Queensland, St. Lucia QLD 4072, Australia, Tel.: +61733466503, Fax: +61733466503, [email protected]. Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. Dietzgen et al. Page 2 Author ManuscriptAuthor Keywords Manuscript Author Manuscript Author Manuscript Author Rhabdovirus; Negative-sense RNA virus; Genome organization; Diversity; Replication; Taxonomy 1. Introduction – Properties and diversity of rhabdoviruses Rhabdoviruses are a large and ecologically diverse group of viruses, which infect terrestrial and aquatic vertebrates, invertebrates and plants. They include many pathogens of significance to public health, agriculture and fisheries (Dietzgen and Kuzmin, 2011). The majority of rhabdoviruses are transmitted by arthropods to vertebrate or plant hosts, but lyssaviruses (e.g. rabies virus) and novirhabdoviruses (e.g. infectious hematopoietic necrosis virus) have evolved to circulate among vertebrates without a biological vector, and sigmaviruses (e.g. Drosophila melanogaster sigma virus) are congenitally transmitted in fruit flies. High throughput host genome sequencing has revealed the integration of rhabdovirus- like elements into the genomes of some arthropods and plants (Ballinger et al., 2012; Fort et al., 2012; Chiba et al., 2011; Katzourakis and Gifford, 2010; Li et al., 2015), suggesting an ancient evolutionary origin and long-standing association of rhabdoviruses with their hosts. Rhabdoviruses are taxonomically classified in thirteen genera in the family Rhabdoviridae, order Mononegavirales, which also includes families Bornaviridae, Filoviridae, Paramyxoviridae and recently established Nyamiviridae (Dietzgen et al., 2011; Walker et al., 2015). The name is based on their characteristic shape and derived from the Ancient Greek word rhabdos meaning “rod or wand”. Classic rhabdoviruses typified by vesicular stomatitis virus (VSV) and sonchus yellow net virus (SYNV) form characteristic bullet- or cone- shaped (animal host; Ge et al., 2010) or bacilliform (plant host; Jackson et al., 2005) enveloped virions that contain non-segmented, negative-sense, single-stranded (ss) RNA genomes of 11–16 kb in length (Figs. 1 and 2). Virions range in size from 100 to 430 × 45 to 100 nm. The basic genome organisation shared by all rhabdoviruses includes five canonical genes that encode (from 3′ to 5′) the nucleoprotein (or nucleocapsid protein, N), phosphoprotein (P), matrix protein (M), glycoprotein (G) and large protein (L, RNA- dependent RNA polymerase) (Fig. 2). This group of structural protein genes is flanked by regulatory 3′ leader and 5′ trailer sequences that show terminal complementarity and contain promoter sequences to initiate replication. The individual genes are flanked by conserved transcription stop and start signals separated by short untranscribed intergenic sequences (Dietzgen and Kuzmin, 2012). The infectious nucleocapsid core [a ribonucleoprotein (RNP) complex], which is active in transcription and replication, consists of the genomic RNA that is always tightly associated with N protein, together with P and L proteins. M protein is responsible for condensation of RNP complex during virion assembly at the host plasma membrane, and the transmembrane spike protein G likely plays an important role in assembly, budding and host cell entry (Dietzgen and Kuzmin, 2012). Rhabdovirus genomes are diverse and often complex because the five canonical genes may be overprinted, overlapped or interspersed with a range of novel accessory genes, such that the number of genes range from 5–10 or more (Walker et al., 2011; 2015; Fig. 3). Among RNA viruses, rhabdovirus genomes have an unusual capacity for plasticity and appear to Virus Res. Author manuscript; available in PMC 2018 January 02. Dietzgen et al. Page 3 have frequently acquired and lost new genes during evolution (Walker et al., 2015). Author ManuscriptAuthor Manuscript Author Manuscript Author Manuscript Author Furthermore, two groups of plant-infecting rhabdoviruses (genera Dichorhavirus and Varicosavirus) were recently found to have a divided genome with the L gene located on a separate RNA segment (Dietzgen et al., 2014; Kormelink et al., 2011). For other reviews on rhabdoviruses see Blondel et al. (2015), Walker et al. (2011), Dietzgen and Kuzmin (2011), Dietzgen et al. (2011), Ammar et al. (2009) and Jackson et al. (2005). 2. Taxonomic classification – past, present and future Rhabdovirus taxonomy is evolving rapidly in an effort to incorporate ever-increasing numbers of new viral sequences obtained through high throughput technologies and to harmonize classifications across genera and families in the order Mononegavirales. In the 9th report of the International Committee on Taxonomy of Viruses (ICTV) the family Rhabdoviridae comprised six genera (Dietzgen et al., 2011). In the 2015 Taxonomy Release [http://www.ictvonline.org/virusTaxonomy.asp], thirteen genera were recognised: Cytorhabdovirus, Dichorhavirus, Ephemerovirus, Lyssavirus, Novirhabdovirus, Nucleorhabdovirus, Perhabdovirus, Sigmavirus, Sprivivirus, Tibrovirus, Tupavirus, Varicosavirus and Vesiculovirus (Fig. 4). Among these, in the recently recognized Dichorhavirus and Varicosavirus genera (Afonso et al., 2016; Adams et al., 2016) for the first