ANRV363-EN54-23 ARI 23 October 2008 14:4 Cellular and Molecular Aspects of Rhabdovirus Interactions with Insect and Plant Hosts∗ El-Desouky Ammar,1 Chi-Wei Tsai,3 Anna E. Whitfield,4 Margaret G. Redinbaugh,2 and Saskia A. Hogenhout5 1Department of Entomology, 2USDA-ARS, Department of Plant Pathology, The Ohio State University-OARDC, Wooster, Ohio 44691; email: [email protected], [email protected] 3Department of Environmental Science, Policy, and Management, University of California, Berkeley, California 94720; email: [email protected] 4Department of Plant Pathology, Kansas State University, Manhattan, Kansas 66506; email: [email protected] 5Department of Disease and Stress Biology, The John Innes Centre, Norwich, NR4 7UH, United Kingdom; email: [email protected] Annu. Rev. Entomol. 2009. 54:447–68 Key Words First published online as a Review in Advance on Cytorhabdovirus, Nucleorhabdovirus, insect vectors, virus-host September 15, 2008 interactions, transmission barriers, propagative transmission The Annual Review of Entomology is online at ento.annualreviews.org Abstract This article’s doi: The rhabdoviruses form a large family (Rhabdoviridae) whose host ranges 10.1146/annurev.ento.54.110807.090454 include humans, other vertebrates, invertebrates, and plants. There are Copyright c 2009 by Annual Reviews. at least 90 plant-infecting rhabdoviruses, several of which are economi- by U.S. Department of Agriculture on 12/31/08. For personal use only. All rights reserved cally important pathogens of various crops. All definitive plant-infecting 0066-4170/09/0107-0447$20.00 and many vertebrate-infecting rhabdoviruses are persistently transmit- Annu. Rev. Entomol. 2009.54:447-468. Downloaded from arjournals.annualreviews.org ∗The U.S. Government has the right to retain a ted by insect vectors, and a few putative plant rhabdoviruses are trans- nonexclusive, royalty-free license in and to any mitted by mites. Plant rhabdoviruses replicate in their plant and arthro- copyright covering this paper. pod hosts, and transmission by vectors is highly specific, with each virus species transmitted by one or a few related insect species, mainly aphids, leafhoppers, or planthoppers. Here, we provide an overview of plant rhabdovirus interactions with their insect hosts and of how these in- teractions compare with those of vertebrate-infecting viruses and with the Sigma rhabdovirus that infects Drosophila flies. We focus on cellular and molecular aspects of vector/host specificity, transmission barriers, and virus receptors in the vectors. In addition, we briefly discuss recent advances in understanding rhabdovirus-plant interactions. 447 ANRV363-EN54-23 ARI 23 October 2008 14:4 INTRODUCTION sociated with Maize mosaic virus (MMV), Lettuce necrotic yellows virus (LNYV), Strawberry crinkle Rhabdoviruses (Rhabdoviridae) are membrane- virus (SCV), and Orchid fleck virus (OFV) (44, SiV: Sigma virus bound, negative-sense RNA viruses that infect 71), among others. vastly divergent hosts. More than 160 species RV: Rabies virus Plant rhabdoviruses require insect or mite of rhabdoviruses have been described, many of OFV: Orchid fleck virus vectors for their transmission and spread in na- which are a threat to human, animal, or plant Persistent: describes ture; these viruses are not seed transmitted, and health (29, 43, 44). The family Rhabdoviridae viruses for which most are not easily transmitted mechanically to includes six genera (29), with members of each inoculativity by the their host plants (37, 44). The definitive plant vector is retained for genus infecting one or two groups of organ- rhabdoviruses with known vectors (Table 1) long periods (days to isms. Phylogenetic analysis of rhabdoviruses are transmitted by hemipteran insects, namely weeks) often based on the most conserved polymerase (L) throughout the aphids (Aphididae), leafhoppers (Cicadellidae), gene indicates that the plant-infecting genera, vector’s life span and is or delphacid planthoppers (Delphacidae) in a Nucleorhabdovirus and Cytorhabdovirus, cluster retained after molting persistent-propagative mode: Following virus together and infect plants and vector insects, Propagative: acquisition from diseased plants, a latent period whereas the genera Lyssavirus, Ephemerovirus, describes viruses that ensues (for a few days to a few weeks) during invade and replicate in and Vesiculovirus group together and in- which the virus replicates in the vector, which various tissues of their fect mainly vertebrate animals (Supplemental later becomes inoculative with virus for most vectors Figure 1; follow the Supplemental Material of its remaining life span (8, 38, 44, 91). Some Transovarial: link from the Annual Reviews home page at putative plant rhabdoviruses have other arthro- describes transmission http://www.annualreviews.org). The last two of viruses from female pod vectors: is transmitted genera were assigned to the dimarhabdovirus Beet leaf curl virus parent to offspring by a heteropteran bug ( ), and (dipteran-mammal associated rhabdovirus) su- Piesma quadratum through the ovaries OFV, and pergroup because they cluster separately from Citrus leprosis virus, Coffee ringspot are transmitted by spp. mites the lyssaviruses and are transmitted to their ver- virus Brevipalpus (Acarina) (16, 43). Mite-vectored rhabdoviruses tebrate hosts by hematophagous dipteran in- are similarly transmitted in a persistent, possi- sects. The L gene sequence is not yet avail- bly propagative, mode by their vectors (77). A able for the Drosophila-infecting rhabdovirus, few plant rhabdoviruses are transmitted verti- Sigma virus (SiV). However, on the basis of cally, i.e., transovarially from infected female phylogenetic relationships of other less con- vectors to their progeny, normally at a low rate served genes, SiV appears to be closest to the (91). dimarhabdoviruses, and although the branches Plant and animal (vertebrate-infecting) are not well supported (29), this is consistent rhabdoviruses share several characteristic fea- with SiV biological characteristics because it by U.S. Department of Agriculture on 12/31/08. For personal use only. tures. Their genomes have similar organiza- also has a dipteran host. The genus Novirhab- tions (29) (Supplemental Figure 2), they both dovirus forms a separate cluster, the members of replicate in and invade the nervous system of Annu. Rev. Entomol. 2009.54:447-468. Downloaded from arjournals.annualreviews.org which infect only aquatic animals. their insect hosts (6, 38, 44, 91), and rhab- Rhabdoviruses can negatively affect humans dovirus gene function is generally conserved and wild animals and reduce yields in live- among different viruses (29). Furthermore, the stock and crop production systems. For ex- vesiculovirus Vesicularstomatitis virus (VSV) was ample, Rabies virus (RV) kills approximately reported to replicate in the planthopper vector 55,000 people each year, mostly in poor areas of MMV (50) as well as in grasshoppers, with the of Africa and Asia (10), whereas vesiculoviruses latter possibly playing a role in VSV epidemi- and ephemeroviruses can cause severe produc- ology in nature (66). The invertebrates might tion losses in the livestock industry (29, 66). In be viewed as the key to evolution and diversity addition, at least 90 confirmed or tentative plant of the rhabdoviruses, as suggested by Sylvester rhabdoviruses infect mono- and dicotyledonous & Richardson (91), because they constitute a plants (43, 44). Serious yield losses have been as- 448 Ammar et al. ANRV363-EN54-23 ARI 23 October 2008 14:4 Table 1 Plant-infecting rhabdoviruses assigned to the Cytorhabdovirus and Nucleorhabdovirus genera and their plant hosts and insect vectorsa Virus species Acronyme Plant host Vector family Vector genera/spp. Genus: Cytorhabdovirus Barley yellow striate mosaic virus BYSMV Monocot Delphacidae Laodelphax striatellus Broccoli necrotic yellows virus BNYV Dicotd Aphididae Brevicoryne brassicae Northern cereal mosaic virus NCMV Monocot Delphacidae Laodelphax, Muellrianella, Ribautodelphax, Unkanodes Festuca leaf streak virus FLSV Monocot – – Lettuce necrotic yellows virus LNYV Dicotd Aphididae Hyperomyzus lactucae Lettuce yellow mottle virus LYMV Dicotd – – Sonchus virus SonV Dicotd – – Strawberry crinkle virus SCV Dicotd Aphididae Chaetosiphon spp. Wheat American striate mosaic virus WASMV Monocot Cicadellidae Elymana virescens, Endria inimica Genus: Nucleorhabdovirus Cereal chlorotic mottle virus CCMoV Monocot Cicadellidae Nesoclutha, Cicadulina Datura yellow vein virus DYVV Dicot – – Eggplant mottled dwarf virusb EMDV Dicotd Cicadellidae Agallia vorobjevi Maize fine streak virus MFSV Monocot Cicadellidae Graminella nigrifrons Maize mosaic virus MMV Monocot Delphacidae Peregrinus maidis Potato yellow dwarf virus PYDV Dicotd Cicadellidae Agallia constricta, A. quadripunctata, Aceratagallia sanguinolenta Rice yellow stunt virusc RYSV Monocot Cicadellidae Nephotettix spp. Sonchus yellow net virus SYNV Dicotd Aphididae Aphis coreopsis Sowthistle yellow vein virus SYVV Dicot Aphididae Hyperomyzus lactucae Taro vein chlorosis virus TaVCV Monocot – – aModified from References 8, 44, 71, 91, with added references for LYMV (36), EMDV (9), and TaVCV (74). bEMDV has two synonyms: Pittosporum vein yellowing virus and Tomato vein clearing virus (TVCV). cRYSV has one synonym: Rice transitory yellowing virus (RTYV). dThese viruses can be mechanically transmitted to their plant hosts (61). eAcronyms in this table are used for plant rhabdoviruses throughout the text. –,