Cellular and Molecular Aspects of Rhabdovirus Interactions with Insect and Plant Hosts∗

Home , Chaetosiphon (aphid), Elymana, Piesma, Potexvirus, Ribautodelphax, Sindbis virus

ANRV363-EN54-23 ARI 23 October 2008 14:4

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 interactions 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.

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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-

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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. –, indicates that no vector has been identified. by U.S. Department of Agriculture on 12/31/08. For personal use only. common host for both plant- and vertebrate- shed light on the remaining mysteries of these infecting rhabdoviruses. interactions and provide suggestions for future Annu. Rev. Entomol. 2009.54:447-468. Downloaded from arjournals.annualreviews.org Several recent reviews of plant rhab- studies. doviruses have focused on their molecular biology and plant-host interactions (43, 44, 71). This review summarizes current knowledge on GENOME ORGANIZATION transmission barriers of plant rhabdoviruses AND GENE FUNCTION IN RHABDOVIRUSES Vector specificity/ in insect vectors and molecular determinants vector competence: of vector specificity, in comparison with the Rhabdoviruses have monocistronic negative- the comparative ability Drosophila-infecting SiV, and where possible sense RNA genomes (29), except for OFV, of certain species, we make comparisons with vertebrate-infecting whose genome consists of two single-stranded, biotypes, or lines of insect vectors to viruses. By reviewing the current aspects of negative-sense RNA molecules (48) (Supple- transmit a certain virus rhabdovirus-vector interactions, we hope to mental Figure 2). The gene orders on the

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positive-sense (antigenomic) RNA strands are CELLULAR INTERACTIONS OF 5 N-P-M-G-L 3 , in which N encodes the nu- PLANT RHABDOVIRUSES AND cleocapsid protein, P the phosphoprotein, M TRANSMISSION BARRIERS IN G protein: glycoprotein the matrix protein, G the glycoprotein, and L THEIR VECTORS the RNA-dependent RNA polymerase. The N, Rhabdoviruses replicate in and systemically in- P, M and G proteins show little conservation vade their plant and animal hosts (Figure 1 among the rhabdoviruses, although they have and Figure 2). They have bacilliform or bullet- similar biological functions in their hosts (55). shaped virions with a host-derived envelope The N proteins function in the encapsidation (43, 44) (Figure 1a). The two genera of plant of the viral genomic RNA and are part of vi- rhabdoviruses, Cytorhabdovirus and Nucleorhab- roplasms and polymerase complexes (55). The dovirus, have been classified according to their P proteins play key roles in replication by in- morphogenesis in host cells. In plant and insect teraction with N and L, suppression of gene cells, the cytorhabdoviruses, such as LNYV, silencing, and intercellular movement of N and appear to mature similarly to the vertebrate- L (43, 44). The M protein functions during infecting rhabdoviruses, as they bud through virus morphogenesis by mediating membrane- cytoplasmic membranes, i.e., the endoplasmic lipid interactions with the G protein and is in- reticulum and associated cytoplasmic cister- volved in the shut down of host gene expres- nae where mature particles accumulate (19, 44, sion and interacts with mitochondria (43, 45). 91). In contrast, nucleorhabdoviruses, such as The large L protein is capable of mRNA tran- MMV and SYNV, multiply in plant cell nu- scription and antigenomic and genomic RNA clei; their virions mature by budding through replication. The G protein is exposed to the the inner nuclear membrane and accumulate surfaces of virus particles and is crucial for in perinuclear space between the inner and gaining entry into the cytoplasm of host cells outer nuclear envelope (Figure 1a). In the in- through receptor binding and the subsequent sect host, however, nucleorhabdoviruses bud on initiation of virus-induced membrane fusion both nuclear and cytoplasmic membranes (7) (17). (Figure 1b,e, f ). All plant rhabdoviruses contain at least one A high degree of vector specificity has been additional gene between and (Supple- P M reported for plant rhabdoviruses, with most of mental Figure 2). Sc4 of Sonchus yellow net them transmitted naturally by one or only a few (SYNV), 4b of LNYV, 3 of MMV and virus closely related insect species (Table 1). Addi- (RYSV), and 4 of Rice yellow stunt virus Maize tionally, within the same insect species, some (MFSV) are likely to function fine streak virus races/biotypes may be more efficient vectors

by U.S. Department of Agriculture on 12/31/08. For personal use only. in cell-to-cell movement in plants based on than others, and also within some virus species structural similarities to the Tobacco mosaic virus some strains are more efﬁciently transmitted (TMV) 30 K superfamily of cell-to-cell move-

Annu. Rev. Entomol. 2009.54:447-468. Downloaded from arjournals.annualreviews.org than others by the same vector (3, 8, 91). Ge- ment proteins and functional analyses of RYSV netic experiments with Potato yellow dwarf virus protein 3 (43, 44). Some viruses also contain (PYDV) have shown that highly efficient and short open reading frames between the and G inefficient leafhopper vectors can be selected genes (Supplemental Figure 2). Of these, L by breeding (44). RYSV 6 is incorporated into virus particles and The vector specificity and vector compe- is produced during infection of the insect vector tence observed for many rhabdoviruses may be but not in plants, suggesting a role of this pro- partly explained by transmission barriers in in- tein in invasion of insect tissues (43, 44). The sects. For a persistent-propagative virus to be molecular steps necessary for assembly of rhab- transmitted by an insect vector, following in- doviruses, particularly VSV, in vertebrate and gestion during feeding on a diseased host, the insect tissues have been reviewed by Jayakar virus must first infect epithelial cells of the et al. (45).

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cycy iiss m ssvv by U.S. Department of Agriculture on 12/31/08. For personal use only.

Figure 1

Annu. Rev. Entomol. 2009.54:447-468. Downloaded from arjournals.annualreviews.org Ultrathin sections in plant and insect hosts of Maize mosaic virus (MMV). (a) MMV virions (red V’s) budding through the inner nuclear membrane (red arrows) and on cytoplasmic membranes (double red arrows) around the nucleus (nu) in a maize leaf cell. (b) MMV virions (red V’s) in cytoplasmic cisternae around the nucleus (nu) in a midgut cell of the vector Peregrinus maidis.(c, d ) Ultrastructure of the anterior diverticulum (c) and the midgut epithelium (d )inP. maidis, showing the lumen (lu), microvilli (mv), peritrophic envelope (blue arrows), epithelial cells (ec), basal plasma membrane (pm), basal lamina (bl), and muscle cells (mc). (e) MMV virions (red arrows) around the nucleus (nu) and in the cytoplasm (cy) of nerve cells in P. maidis; the inset shows a virion budding through axon membranes (red arrowhead ). ( f ) MMV virions budding through the plasma membranes (red arrows) in secretory cells of the salivary gland in P. maidis and accumulating in intercellular space (is) and in secretory vesicles (sv, arrowhead in the inset). Other abbreviations: ax, axon; cw, cell wall; im, inner nuclear membrane; m, mitochondrion; mf, muscle ﬁbers; om, outer nuclear membrane. Scale bars: a, f : 500 nm; b–e:1μm; inset in e: 250 nm.

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a b ep ep me vb vb me

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asg es ad cg psg

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Figure 2 Immunofluorescence localization of some rhabdoviruses in their plant or insect hosts; plant sections (a and b) and insect organs (c–h) were incubated with virus-specific antibodies, then with a secondary antibody by U.S. Department of Agriculture on 12/31/08. For personal use only. conjugated to Alexa Fluor 488 ( green), the nuclear stain propidium iodide (red ), and (in panels c–h) with an actin stain, Phalloidin (blue/purple). (a) Perinuclear accumulations of Maize fine streak virus (MFSV) ( green)in various tissues of infected maize leaf cells. ( ) Section from a healthy (control) maize leaf. ( ) Annu. Rev. Entomol. 2009.54:447-468. Downloaded from arjournals.annualreviews.org b c–e Maize mosaic virus (MMV) localization in the midgut (mg), anterior diverticulum (ad), esophagus (es), compound ganglion (cg), nerve cord (nc), nerves (ne), trachea (tr), and the accessory (asg) and principal salivary glands (psg) of the planthopper vector Peregrinus maidis.(f, g) MFSV localization in the esophagus (es), filter chamber (fc), anterior (amg) and posterior midgut (pmg), hindgut (hg), lobes of the principal salivary glands (psg), compound ganglion (cg), and nerves (ne) of the leafhopper vector Graminella nigrifrons.(h) Sigma virus localization in the esophagus (es), cardia (car), nerve ganglia (ng), and nerves (ne) of an infected Drosophila. Additional abbreviations: ep, epidermis; me, mesophyll; mf, muscle fibers; vb, vascular bundle. Scale bars: 40 μm.

alimentary canal, exit/escape this tissue, and (Figure 2 and Figure 3). The inability of an move to the salivary glands, and then it must insect to transmit a virus could thus be due to ﬁnally be ejected with the salivary secretions failure of the virus to enter, replicate in, move during insect feeding on a susceptible host between, or escape from insect cells, organs, or

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organelles, and each of these features may be rayado fino virus (Marafivirus), respectively, than interdicted by innate defense response to virus are the adults of these species (63). invasion of the vector (3, 35, 44, 83). The fol- The existence of a midgut infection or Circulative: describes lowing is a comparison of transmission barri- midgut escape barrier has been indirectly viruses that move from ers in vectors of plant rhabdoviruses with bar- demonstrated with some plant rhabdoviruses. the gut into the riers for other propagative plant and animal Intrathoracic injection of MMV or Maize hemolymph and other viruses. Iranian mosaic virus (MIMV) in planthoppers tissues of their vectors and SCV in aphids resulted in a much higher before they can be transmitted proportion of infected individuals than when Midgut Infection and Escape Barriers insects acquired virus by feeding on diseased MStV: Maize stripe virus Among the rhabdovirus vectors, there is great plants (5, 25, 91). Direct evidence of midgut diversity in the gross morphology of the gut. infection, midgut escape, and salivary gland MIMV: Maize Iranian mosaic virus For example, the leafhoppers possess a filter infection barriers for MMV in P. maidis has chamber (Figure 2f and Figure 3a) that is been obtained using immunofluorescence lacking in aphids, planthoppers, and dipterans, microscopy of dissected insect organs (6) and the planthoppers uniquely possess an ante- (Figure 2c–e). Following a 1- to 3-week ac- rior diverticulum (Figure 1c, Figure 2c, and quisition access period on diseased plants, only Figure 3b), which is essentially a narrower, 28% of P.maidis had infected midguts, and a sig- blind-ended, anterior extension of the midgut nificantly lower proportion (20%) had infected (2). The basic midgut ultrastructure, however, salivary glands. The proportion of infected is similar in various insect groups (15). The guts was significantly higher following 3-week midgut consists mainly of a single layer of ep- acquisition (35%), compared with that follow- ithelial cells, with extensive microvilli on the ing 1-week acquisition (24%), which suggests inner (lumen) side and highly invaginated basal that midgut infection with MMV may be dose plasma membrane on the outer side, covered dependent. However, even after the prolonged with the basal lamina surrounded by mus- (3 week) feeding on MMV-infected plants, al- cle fibers (Figure 1b–d ). In Hemiptera, the most two-thirds of the planthopper population midgut lumen is lined with a multilayer of tested appeared to resist MMV infection at the laminae (Figure 1c,d ) that is probably analo- midgut infection level. The ability of P. maidis gous to the peritrophic envelope/matrix found to transmit MMV seems to be a genetic trait. in Diptera and other insects. The peritrophic A Hawaiian biotype of P. maidis transmitted matrix is a semipermeable extracellular chitin- MMV at almost twice the rate as that of a and protein-containing layer produced by the Florida biotype under similar conditions (4).

by U.S. Department of Agriculture on 12/31/08. For personal use only. midgut epithelium and apparently protects the Midgut infection and escape barriers have been gut microvilli from food material and from also demonstrated for some other plant and invasion by viral or bacterial pathogens (15). animal viruses including VSV in black flies (3, Annu. Rev. Entomol. 2009.54:447-468. Downloaded from arjournals.annualreviews.org Thus, the peritrophic envelope/laminae, not 8, 35, 37, 39). Several hypotheses have been the midgut microvilli, are likely to be the proposed to explain the midgut infection bar- first barrier that circulative/propagative viruses rier to propagative viruses in their vectors (35). must cross to infect the midgut. This may partly These include inactivation of virus by digestive explain the frequently observed phenomenon enzymes in the midgut lumen, occlusion of that several propagative viruses are transmitted virus by the peritrophic envelope, absence or more efficiently by younger insects, in which reduced number of cellular receptor sites of this envelope is thinner or not fully developed virus attachment on the microvillar membrane, (15), than by older ones. For example, nymphs and/or abortive replication of virus in midgut of Nephotettix cincticeps, P. maidis, and Dalbu- epithelial cells. In addition, we propose that lus maidis are more efficient vectors of RYSV, some insects may resist infection because of a Maize stripe virus (MStV, Tenuivirus) and Maize specific innate immune response to the virus,

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a Filter chamber Midgut te Hindgut Esophagus rou ph ym ol e cord em Hemocoel Nerv Brain H Principal route salivary Neurotropic gland

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Brain MMV route by U.S. Department of Agriculture on 12/31/08. For personal use only.

Compound ganglion Midgut Annu. Rev. Entomol. 2009.54:447-468. Downloaded from arjournals.annualreviews.org

Nerve cor Esophagus d Cibarium Salivary duct Salivary pump P. maidis Precibarium

Stylets: Food canal Labium Salivary canal

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possibly similar to that recently reported for the basal lamina between the midgut and the Drosophila against SiV (95). hemolymph (Figure 1b,c) seems to be a sub- On the basis of studies of animal and stantial barrier to this route. plant virus infection of insect cell monolayers, Recent investigations on plant and animal rhabdoviruses are presumed to enter epithelial viruses indicate that other possible routes ex- cells of the midgut by receptor-mediated en- ist, especially through neural, tracheal, or mus- docytosis (44). An electron microscopic study cle tissues, for virus movement from the vec- of VSV indicated that virions enter vertebrate tor’s midgut into the salivary glands. In insects, and insect cell lines through coated pits and including hemipterans and dipterans, the gut coated vesicles (90). Also, inhibition of PYDV epithelia are surrounded by visceral muscles infection of vector cell monolayers by some (Figure 1b,c) and are closely associated with the lysosomotropic agents suggested that PYDV tracheal system. Muscles of the foregut and an- enters these cells by adsorptive endocytosis (1). terior midgut are innervated principally from Although the virus glycoprotein (G protein) the stomatogastric nervous system (15). seems to be involved in this process (30), the Spatial and temporal distribution of VSV entry mechanism of rhabdoviruses into the in orally infected midges (Culicoides sonorensis) gut cells of their vectors has not been fully was studied by Drolet et al. (23), who indicated described. that the circulation of VSV in the hemolymph by day 3 post-acquisition coincided with infection of several tissues including the salivary Dissemination of Virus from the glands and nerve ganglia. Neural infections Midgut into Other Tissues were detected in the subabdominal ganglia For circulative/propagative transmission of innervating the midgut in 33% of insects 1 plant and animal viruses, the virus infection day post-acquisition in the absence of positive must spread from the alimentary canal to other staining in the hemolymph or surrounding organs, most importantly the salivary glands. tissues. Thus, the authors suggested a ret- It has been generally assumed that virus is dis- rograde axonal transport infection route for seminated from the midgut into other tissues of these ganglia from the midgut, similar to that the vector through the hemolymph. This be- previously reported for VSV in the mouse lief is based mainly on experiments in which brain. Because a lower proportion of insects such viruses can be transmitted by their vec- had virus in the nerve ganglia than in salivary tors following injection of virus extracts into glands, they concluded that infection of the their hemocoel (body cavity). However, Hardy nerve ganglia from surrounding cells and

by U.S. Department of Agriculture on 12/31/08. For personal use only. (35) noted that the pore size of the (mosquito) tissues is not efﬁcient and that the hemolymph midgut basal lamina is approximately 10 nm, was the likely source of virus for infecting and this is much smaller than virions of most the salivary glands. However, RV reaches Annu. Rev. Entomol. 2009.54:447-468. Downloaded from arjournals.annualreviews.org arboviruses including rhabdoviruses. Thus, al- the salivary glands of its vertebrate hosts and though the hemolymph route (Figure 3a) has vectors through invasion of the nervous system not been thoroughly investigated or ruled out, (21). ←−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−

Figure 3 (a) A stylized diagram showing two possible routes for plant rhabdovirus movement in a leafhopper vector. Virions are acquired from plant cells through the food canal inside the stylets and enter the lumen of the filter chamber and midgut. The virus then replicates in midgut epithelial cells and later invades the principal salivary glands moving through the hemolymph (brown arrow) and/or the nervous system (blue arrows) (modified from Reference 38). (b) A proposed neurotropic route (blue arrows) for Maize mosaic virus (MMV) in its planthopper vector Peregrinus maidis. Following oral acquisition of MMV from infected plants, the virus moves from the anterior part of the midgut to the anterior diverticulum and the esophagus, and from these to the compound ganglion, then through nerves to the principal salivary glands (modified from Reference 6).

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A recent study of the temporal and spatial and visceral muscles, that facilitate virus distribution of MMV in its planthopper vec- movement through the basal lamina of the tor was conducted by Ammar & Hogenhout midgut. Ultrastructural studies of the mosquito TSWV: Tomato spotted (6). Following a 1-week acquisition feeding pe- midgut revealed evidence for possible complete wilt virus riod of P. maidis on infected plants, the first penetration of the basal lamina by tracheal cells infection sites were epithelial cells of the an- and regions of modified basal lamina associated terior part of the midgut and the anterior di- with visceral muscles. Muscle fibers supplied verticulum (Figure 2c). Subsequently MMV with tracheae and nerve axons were also found spread to the esophagus, nerve cord and nerve in various lobes of the salivary glands of ganglia at least one week before being detected P. maidis (2). These provide potential routes in the hemocytes, tracheae, salivary glands, for movement of virus from the midgut to or other tissues of P. maidis (Figure 2c–e). the salivary glands. Another enveloped virus, MMV is neurotropic in its insect host, with Tomato spotted wilt virus (TSWV, Bunyaviridae), more extensive infection detected in the ner- infects visceral muscles of the midgut and vous system than in other tissues. Neural tissues foregut of the thrips vector, and the ligaments infected with MMV in P. maidis included brain, connecting the anterior midgut with the compound ganglion (amalgamated mesotho- salivary glands were suggested as a possible racic, metathoracic, and abdominal ganglia), dissemination route for TSWV in its vector and compound eye cells. In this vector, as in (62). In addition, the tracheal system is a major other planthoppers, the esophagus and ante- conduit for the spread of some other viruses rior diverticulum are sandwiched between the that replicate in insects, e.g., baculoviruses in compound ganglion and the salivary glands (2). the larvae of Trichoplusia ni (24). On the basis of the above results, the authors postulated that MMV may overcome midgut escape or salivary gland infection barriers in Salivary Gland Infection and Escape Barriers P. maidis by proceeding from the anterior midgut to the anterior diverticulum and esoph- Morphological, physiological, and chemical agus, and from these to the salivary glands differences in the salivary glands or salivary se- via the nervous system (Figure 3b). How- cretions of arthropods are potential factors that ever, other possible routes including the might explain the salivary gland infection and hemolymph, as suggested for VSV in its escape barriers reported for some propagative dipteran host (23), may play a role in dissemi- plant and animal viruses in their vectors (2, 6, nation of MMV from the midgut to other tis- 8, 35). In addition, as discussed for the midgut,

by U.S. Department of Agriculture on 12/31/08. For personal use only. sues. With another enveloped virus, Rift Valley the basal laminae of the salivary gland must be fever virus (Bunyaviridae), the foregut/anterior breached by the virus for successful transmis- midgut junction, which is also extensively in- sion to occur. The mechanism(s) used by viruses Annu. Rev. Entomol. 2009.54:447-468. Downloaded from arjournals.annualreviews.org fected with MMV in P. maidis (Figure 2c), is for overcoming this barrier to enter the salivary the site where virus apparently is disseminated glands is not well documented, but the neural into the hemocoel of the mosquito Culex pipiens and tracheal systems are also good candidates (78). for such mechanisms (6, 35, 62). After invad- Other proposed dissemination routes ing and replicating in the salivary glands, the for propagative plant and animal viruses in last physical barrier that a virus must cross, to their vectors are the tracheal system and the escape the salivary gland cells and enter into visceral muscles associated with the insect the saliva for introduction into plants during midgut. Results by Romoser et al. (79), with insect feeding, is the plasma membrane of the Venezuelan equine encephalitis virus (Togaviridae) salivary gland secretory cells (Figure 1f ). A in mosquitoes, indicated the operation of salivary gland escape barrier has not been ex- tissue conduits, possibly involving tracheae plicitly reported for plant rhabdoviruses but has

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been demonstrated for several other propaga- vent sieve tube plugging in plant hosts during tive viruses in their vectors. With La Crosse virus feeding, which is likely to result in a more ef- (Bunyaviridae), 65% of Aedes hendersoni had in- ficient acquisition and inoculation of phloem- fected salivary glands but only 5% transmit- limited viruses by insect vectors. With tick- ted the virus (35). Similarly, with the Tenuivirus borne viruses, saliva-activated transmission has MStV, of 31 P. maidis individuals with infected been demonstrated by enhanced transmission salivary glands as indicated by enzyme-linked of infectivity when the pathogen plus salivary immunosorbent assay, 24 insects failed to trans- gland extract is injected into a vertebrate host, mit the virus to host plants (64). compared with the level of infectivity when the The ability of rhabdoviruses to bud from pathogen alone is injected (67). Similarly, with plasma membranes, rather than the endoplas- VSV, treatment of mouse fibroblast cells with mic reticulum or nuclear membranes of the in- mosquito salivary gland homogenates resulted sect salivary gland cells, is likely important for in a significant increase in virus growth kinetics overcoming the salivary gland escape barrier. compared with untreated controls. On the basis In most tissues of P. maidis, MMV virions bud of these and other results, Limesand et al. (54) mainly through nuclear membranes and accu- suggested that modulation of interferon (antivi- mulate in the perinuclear space and in dilated ral factor) by mosquito saliva may be a critical cisternae in the cytoplasm (7) as they do in determinant of the transmission and pathogen- plant cells (Figure 1a,b). However, in secretory esis of VSV.Future investigations should reveal cells of the principal salivary gland, MMV viri- whether insect salivary gland proteins also aid ons bud mainly through the plasma membranes or hinder plant rhabdovirus infection of plant and accumulate in intercellular and extracellu- or insect hosts. lar spaces (Figure 1f ). These spaces are apparently connected with secretory vesicles and eventually with the salivary ducts (2, 7). A sim- MOLECULAR DETERMINANTS ilar difference in the budding sites of RV in the OF VIRUS-INSECT fox brain and salivary gland cells has been re- HOST SPECIFICITY ported, and plasma membrane budding in sali- The Role of Viral Glycoproteins vary gland cells is considered essential for bite transmission of this virus (61). Viral G proteins play an important role in virus Other possible mechanisms that may ac- entry into host cells, assembly of virions, and count for a salivary gland escape barrier are that escape from host cells. Viruses use conserved too little virus is produced in the salivary glands pathways to enter host cells, and virus entry

by U.S. Department of Agriculture on 12/31/08. For personal use only. or secreted during the feeding process to in- generally requires the interaction between a vi- fect the host (35), or that virus may be inacti- ral G protein and a receptor displayed on the vated by salivary secretions of the vector. The surface of the host cell. Rhabdovirus entry is Annu. Rev. Entomol. 2009.54:447-468. Downloaded from arjournals.annualreviews.org possible role(s) of chemical and physiological mediated by the sole surface G protein, and conditions of the salivary secretions in enhanc- the steps in this process are well deﬁned for ing or obstructing plant virus transmission by vertebrate-infecting rhabdoviruses (56). The G insect vectors remains largely uninvestigated. protein functions as the viral attachment pro- Inhibitory effects of the salivary secretions of tein by binding to a cellular receptor, and the vi- aphids on some aphid-nontransmissible viruses, ral fusion protein functions by initiating fusion including TMV, Potato virus X, and Turnip mo- between the viral and host membrane. The G saic virus, have been reviewed by Nishi (65). protein is a determinant of host speciﬁcity and Conversely, the vector’s salivary secretions may virulence (31, 49, 56, 69). Because gene func- aid virus transmission by the vector or virus in- tion is generally conserved among members of a fection of plants. For example, Will et al. (102) virus family, G proteins of plant-infecting rhab- reported that aphid saliva has the ability to pre- doviruses likely play similar roles during virus

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entry into insect vector cells. It is not yet clear been suggested that RV and VSV bind neg- whether the G proteins of these rhabdoviruses atively charged lipids, and evidence indicates are essential for plant infection. that highly sialylated gangliosides are part of Rhabdovirus G proteins are integral the cellular membrane receptor structures for membrane proteins and they generally have the attachment of infective RV (89). However, a transmembrane domain composed of ap- it is possible that cell surface molecules such proximately 20 hydrophobic amino acids, an as G proteins or glycolipids also participate N-terminal signal sequence, and N- and/or as components of a receptor structure for RV. O-linked glycans. Rhabdovirus G proteins Phosphatidylserine has been implicated as a oligomerize into homotrimers and this is the receptor for VSV and the ubiquitous distri- form that interacts with cellular receptors bution of this molecule partially explains the (87). The crystal structure of the low-pH and large tissue tropism of VSV (31). In contrast, prefusion forms of VSV G protein has been RV is a strict neuropathogen in vivo but has an resolved and has revealed that rhabdovirus extensive range in vitro, infecting mammalian G proteins represent a new class of fusion and avian cell types. Several proteins found on proteins (75, 76). Viruses in the families Rhab- the surface of neurons have been implicated as doviridae and Herpesviridae encode G proteins possible RV receptors including the nicotinic categorized as Class III fusion proteins and acetylcholine receptor, neural cell adhesion they share similar conformational features molecule (CD56), and the low-afﬁnity nerve (75). Viral fusion proteins contain hydrophobic growth factor receptor p75NTR. Studies of regions, named fusion domains, that insert into rhabdovirus entry have focused on vertebrate host membranes and initiate the merging of cells, but entry into insect vectors is not virus and host lipid bilayers. The rhabdovirus extensively studied. Because plant-infecting G protein fusion domain is bipartite and is rhabdoviruses infect a diverse array of insect composed of two noncontiguous loops (75). tissues (i.e., epithelial cells and neurons), it is The functional importance of the fusion loop likely that a ubiquitous molecule or more than in membrane fusion has been conﬁrmed by one molecule can function as the virus receptor. mutational analysis, and the loop is conserved That VSV can replicate in the planthopper between divergent rhabdoviruses (88). The G P. maidis, vector of MMV, after microinjection protein can assume three different states: the (50) suggests that at least some of the host native state on the viral surface at neutral pH, requirements for these divergent viruses are the activated hydrophobic state, and the inac- similar. tive postfusion conformation. Rhabdovirus G

by U.S. Department of Agriculture on 12/31/08. For personal use only. proteins are unique because the conformational changes that occur at low pH are reversible Molecular Analysis of Insect even after interaction with the host membrane Barriers to Infection Annu. Rev. Entomol. 2009.54:447-468. Downloaded from arjournals.annualreviews.org (31, 56). The resolution of the VSV G protein The insect midgut and salivary glands are im- structure will enable comparative analysis of portant barriers to the acquisition and transmis- nucleorhabdovirus and cytorhabdovirus G sion of plant and animal rhabdoviruses (3, 6, 8, protein structure and function relationships. 35). This may be due to the absence of virus receptors, the inability of the virus to replicate in the midgut or salivary glands, or the antiviral in- Rhabdovirus Receptors nate defense responses. In other insect-microbe The receptors for vertebrate-infecting rhab- interactions, a substantial number of genes are doviruses have been identiﬁed and receptor differentially regulated upon pathogen inva- usage varies with virus and tissue. Both RV sion of midguts, including immune-response and VSV bind to receptors that are widely genes; insect epithelia serve as physical and distributed among many cell types (56). It has functional barriers to pathogens; and insects

458 Ammar et al. ANRV363-EN54-23 ARI 23 October 2008 14:4

mount a strong immune response against mi- invertebrate animals (11), the LC8-P interac- croorganisms (94, 97). Furthermore, it is possi- tion may also be important for rhabdovirus in- ble that host microRNAs (miRNAs) play a role fection of insect neuronal cells. VSV: Vesicular in rhabdovirus-host interactions as has been Plant rhabdoviruses apparently multiply at stomatitis virus shown for VSV in mice (68). Although these a much lower rate in insect cells than in plant areas of research are relatively unexplored for cells. Whereas large accumulations of virions of plant rhabdoviruses, the availability of relatively MMV, MIMV, and MFSV, sometimes packed new model systems, including MMV with the into paracrystalline arrays, were found in al- planthopper P. maidis, MFSV with the leafhop- most all maize leaf cell types (Figure 1a and per vector Graminella nigrifrons, and SiV with Figure 2a) (5, 58, 72), much smaller accumu- Drosophila, will enable scientists to determine lations of MMV virions, and no paracrystalline the nature of the infection barriers and define arrays, were observed in cells of the insect vec- the viral and vector components involved in tor (7) (Figure 1a,b,e, f ). Furthermore, in spite these interactions (38, 72, 73, 95, 96). The de- of the systemic infection of MMV in its vec- velopment of recombinant forms of MMV and tor, no major cytopathological effects on neu- MFSV G proteins will enable studies that exam- ral or other tissues have been detected, and ine the specificity of G protein binding to vec- no marked differences in longevity or egg pro- tors (100). The advent of new genomic infor- duction have been observed in MMV-infected mation, particularly for P. maidis (80), will en- P. maidis (7, 8). Similarly, no marked effects able comparative studies between SiV-infected on the longevity or reproduction of aphids Drosophila and MMV-infected P. maidis as well orally infected with several rhabdoviruses have as the identification of conserved and unique been reported, although some harmful effects features of the infection cycle of these two rhab- may occur in virus-injected or transovarially in- doviruses in their hosts. fected aphids (91). However, infection of the nervous system may have less detectable effects in these vectors, for example, on the feeding NEUROTROPISM AND or other behavioral aspects that have not been PATHOGENESIS thoroughly studied so far. IN INSECT HOSTS With propagative plant and animal viruses, Plant- and vertebrate-infecting rhabdoviruses modulating factors appear to be involved in lim- appear to be primarily neurotropic in their in- iting the replication and pathogenic effects of sect hosts, although they can invade many other such viruses on their vectors, in contrast to their tissues of their vectors (7, 23, 32). In addition to much more severe effect on their plant or ver-

by U.S. Department of Agriculture on 12/31/08. For personal use only. MMV neurotropism in its planthopper vector tebrate hosts (3, 8, 35). The noncytopathic per- (6), another nucleorhabdovirus, MFSV, was re- sistent infection of VSV in insect cells was stud- cently found to be neurotropic in its leafhopper ied and compared with VSV-infected Drosophila Annu. Rev. Entomol. 2009.54:447-468. Downloaded from arjournals.annualreviews.org vector G. nigrifrons (Figure 2f,g). SiV also in- and mammalian cells. Host cell control on the fects the nervous system in addition to several maturation and synthesis of VSV G protein in other tissues of Drosophila ﬂies (93) (Figure 2h). Drosophila cells caused a low virus production Viral infection of neural cells is an important de- rate that was required for maintaining a carrier terminant of RV pathogenesis in animals. For (persistent) state in insect cells. Frequent abor- infection of neuronal cells by RV, interaction of tion of the replication step of VSV in Drosophila the host dynein light chain (LC8) and the P pro- cells also ensured the low virus titer in a car- tein of RV appears to be required (92). Indeed, rier state. It is possible that defective interfering deletion of the LC8 binding region of P has a (DI) particles limit rhabdovirus replication. DI signiﬁcant negative effect on de novo transcrip- particles are subgenomic deletion mutants that tion of viral genes in neuronal cells (92). Be- lack parts of the viral genome and are common cause LC8 is conserved among vertebrate and in animal rhabdovirus infections, including

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arbovirus infections of mosquito cells (35). DI lated with replication of the virus in the thoracic particles have been reported in plant hosts of ganglia (13). SiV infects almost all Drosophila PYDV and SYNV and are likely involved in tissues (Figure 2h) especially nervous tissue DCV: Drosophila C virus the recovery during chronic stages of virus in- including the brain and other nerve ganglia fection in plants (19). DI particles of plant rhab- (93, 95). DXV: Drosophila X virus doviruses may also limit replication in insect At least six polymorphic genes confer resis- vectors. Furthermore, the insect hosts are prob- tance to SiV infection in natural populations ably capable of mounting an effective immune of D. melanogaster (93). Among these, ref(2)P, response to rhabdovirus infection, evidence for which is necessary for male fertility (18), is the which is provided by studies on SiV-Drosophila best-characterized gene. The Ref(2)P protein interactions (95). shares a conformation-dependent epitope with the SiV N protein and forms a complex with the viral P protein (104). This complex for- INTERACTION BETWEEN SIGMA mation with the P protein is probably one of VIRUS AND DROSOPHILA the mechanisms by which ref(2)P renders re- The Drosophila-infecting rhabdovirus SiV oc- sistance to SiV infection, as the P protein is curs naturally in several Drosophila species and essential for rhabdovirus replication. Recently, is maintained in fly populations through ver- Carre-Mlouka´ et al. (14) reported that resistant tical transmission via germ cells (28, 103). In genotypes to SiV have three amino acid replace- France, 10%–20% of natural Drosophila popu- ments (Q28N29 by G, I32 by V, and Q43 by L) lations are infected with SiV (28). Similar SiV in the Phox and Bem 1 (PB1) domain compared infection rates in wild-caught D. athabasca and with a permissive counterpart. However, the D. affinis were reported in the United States Drosophila-fertility-related function of Ref(2)P (103). In wild Drosophila populations, SiV in- is not located in the PB1 domain (14). fection does not appear to affect the fertility, Drosophila immune responses to various longevity, or sexual selection of D. melanogaster, bacterial and fungal pathogens are well char- but SiV-infected flies that are maintained in acterized at the molecular level (52), but the the laboratory have reduced egg viability and elucidation of Drosophila immune responses to slightly lower overwintering fitness (27). SiV virus infections began relatively recently (22, strains selected for high replication rates ad- 99, 106). Tsai et al. (95) analyzed the expres- versely affected the fertility and egg viabil- sion of D. melanogaster immunity genes in SiV- ity of Drosophila under laboratory conditions infected versus healthy flies using real-time re- (84, 85). verse transcriptase PCR and compared these

by U.S. Department of Agriculture on 12/31/08. For personal use only. SiV-infected flies are sensitive to CO2 and expression data with the immune responses the expression of CO2 sensitivity is corre- of Drosophila infected with Drosophila C virus lated with SiV titer in flies (85, 93). After (DCV) (22) and Drosophila X virus (DXV) (106). Annu. Rev. Entomol. 2009.54:447-468. Downloaded from arjournals.annualreviews.org CO2 anesthetization, the SiV-infected flies re- The comparison showed upregulation of dif- main irreversibly paralyzed and eventually die, ferent peptidoglycan recognition and antimi- whereas uninfected flies paralyzed by exposure crobial peptide genes in SiV-infected versus

to CO2 recover their motility shortly follow- DCV- and DXV-infected ﬂies, in which the ing their return to fresh air (12, 93). This lethal Drosophila responses to DCV and DXV infec- dose of CO2 is seldom encountered in nature tions appear to be more similar to each other (93). The CO2 sensitivity was also observed than to the Drosophila response to SiV infection when Drosophila ﬂies were injected with various (95). Thus, the Drosophila immune system has vesiculoviruses (93), and temporary CO2 sen- the ability to recognize diverse viruses. This is sitivity was reported in aphid vectors infected perhaps expected as SiV differs from DCV and with some plant rhabdoviruses (91). Sensitivity DXV in its mode of transmission, morphology,

of the SiV-infected ﬂies to CO2 has been corre- tissue tropism, and virulence (28, 93, 106). SiV

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particles are bound by a lipid envelope with prising that specific changes in gene expres- transmembrane G protein spikes (93), whereas sion can be detected in Nicotiana benthamiana DCV and DXV are nonenveloped viruses. It has plants inoculated with SYNV (86). Microarray been proposed that the peptidoglycan recog- analyses of plants challenged with viruses in- nition proteins of flies recognize, bind, and dicate common upregulation of plant defense catalytically cleave specific surface components and stress response genes and genes involved in of pathogens, thereby inducing different im- hormone responses and development (101). In mune signaling cascades (81), providing an ex- a comparative study of plants inoculated with planation for the differential gene expression in the tospovirus Impatiens necrotic spot virus and SiV- versus DCV/DXV-infected flies. For the SYNV, approximately 25 genes were specifi- expression level of antimicrobial peptide genes, cally induced in the SYNV-inoculated plants, the SiV infection appears to be most similar to including some involved in defense, protein tar- that of Drosophila infected with gram-negative geting, and signaling pathways (86). Although bacteria, as both induce Diptericin, Attacin, these results are intriguing, further research is Cecropin and Drosocin, but not Drosomycin and needed to tie changes in gene expression to Metchnikowin (42, 95). specific infection process events and to deter- It is apparent that Drosophila use various mine whether these responses are unique to strategies to limit SiV infection. Because high the N. benthamiana–SYNV system or whether SiV titers have negative effects on Drosophila they are common responses of plant hosts to fitness, these strategies appear to be crucial rhabdoviruses. for assuring Drosophila survival. The SiV–D. melanogaster interaction has become a good model system for investigating the molecular Subcellular Localization aspects of rhabdovirus pathogenesis (68, 105) of and Interactions among as well as for increasing our understanding of Rhabdoviral Proteins plant rhabdovirus interactions with their insect Interactions among rhabdoviral proteins are vectors. likely required for virus replication and morphogenesis. For example, the N, P, and L pro- MOLECULAR INTERACTIONS teins were proposed to interact to form the WITH PLANT HOSTS replicase complex in the plant cell nucleus (98). Formation of the N-P-L complex and the pro- Interactions between the plant host and virus cess of nucleorhabdovirus maturation require can lead to virus susceptibility or virus re- that viral proteins and RNAs move between the sistance. As in animals, the obligate parasitic

by U.S. Department of Agriculture on 12/31/08. For personal use only. cytoplasm and the nucleus. Nucleorhabdoviral nature of viruses requires interactions of vi- proteins do accumulate in speciﬁc subnuclear ral RNAs and proteins with plant proteins localizations that depend on the protein and the

Annu. Rev. Entomol. 2009.54:447-468. Downloaded from arjournals.annualreviews.org for virus protein synthesis, genome replica- context in which the protein is expressed (33, tion, virion assembly, and virus movement be- 44, 96). In SYNV-infected plants, the SYNV tween cells and organs. There are also molec- G protein is localized in the periphery of the ular interactions that occur between the virus nucleus (57). The SYNV and MFSV N and M and plant host that can lead to virus resistance proteins have nuclear localization signals that that are analogous to interactions that occur in are sufﬁcient to direct ﬂuorescent fusion pro- D. melanogaster for resistance to SiV (93). teins to the nucleus in virus-free N. benthamiana (96). The N protein interacts with the P protein Plant Responses in a yeast two-hybrid system, and coexpression to Rhabdovirus Infection of the two proteins results in a punctate subnu- Given the complex set of interactions that oc- clear or nucleolar localization of the two pro- cur between virus and plant host, it is not sur- teins (44, 96). Fluorescent fusion proteins for

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SYNV N, P,M, and G have substantially differ- fense response known as virus-induced gene ent subnuclear localizations in SYNV-infected silencing (82). This triggers the sequence- plants than in virus-free plants (33). Virus in- specific degradation of viral RNA transcripts fection also induces formation of nuclear mem- and genomes and spreads systemically through- branes that are contiguous to the endoplasmic out the plant in response to localized virus in- reticulum (33, 34). The localization of SYNV fection. Nearly all plant viruses have evolved proteins relative to these membranes suggests counter-defensive proteins known as silencing that viral replication and morphogenesis within suppressors. Many viral silencing suppressors the nucleus are spatially separated (33). were previously shown to be important for systemic or long-distance virus movement in the Movement/Silencing Suppression plant (44). Transient expression of SYNV P and Host Resistance protein released green fluorescent protein silencing in N. benthamiana (44), suggesting that Proteins that facilitate cell-to-cell and sys- this protein is a silencing suppressor. This re- temic movement have been identified for many sult is somewhat surprising, as the P protein is plant viruses (59). Because virus movement is a core protein found in all rhabdoviruses. Si- fundamentally different in plants and animals lencing suppressors in animal-infecting viruses and because all known plant rhabdoviruses en- have been identified (53). Pathogen-derived re- code more than the five core proteins present sistance, in which expression of viral transgenes in VSV, these additional genes/proteins are triggers virus-induced gene silencing, has been thought to be involved with virus movement demonstrated for a number of viruses and in or silencing suppression (38, 44). a wide range of plant hosts, and rice plants ex- In contrast to movement by receptor- pressing the RYSV RNAs were resistant to virus mediated endocytosis that occurs for viruses infection (26). in animal systems, plant viruses move between The use of genetically resistant plants is plant cells via the symplast, the continuous pro- considered the most economically and envi- toplasm connecting plant cells through plasmo- ronmentally sustainable approach for virus dis- desmata. Plant viruses encode one or more ease control in crops (47). Resistance to several movement proteins. These proteins function plant-infecting rhabdoviruses, including those by enlarging the size exclusion limit of plasmo- infecting wheat, maize, and raspberry, has been desmata and/or by participating in the tubule- described (46, 60, 70, 72). MMV causes disease guided movement of viruses through highly in tropical and subtropical areas worldwide, and modified plasmodesmata (51). The SYNV sc4, a major quantitative trait locus for MMV resis- LYNV 4b, RYSV 3, and Taro vein chlorosis virus

by U.S. Department of Agriculture on 12/31/08. For personal use only. tance, Mv1, was identified (60). (TaVCV) 3 proteins have homology to well- characterized movement proteins and occupy PERSPECTIVES AND Annu. Rev. Entomol. 2009.54:447-468. Downloaded from arjournals.annualreviews.org homologous positions in their respective viral genomes (Supplemental Figure 2) (20, 40, FUTURE ISSUES 41, 74). Localization of a sc4- green fluores- Numerous studies indicate that plant- and cent protein in plant cells and complementa- vertebrate-infecting rhabdoviruses have several tion experiments with the homologous RYSV 3 biological characteristics in common, includ- in movement-deficient potexvirus indicate that ing similar genome organization aside from an these are movement proteins (40, 44). Further- extra gene(s) between the P and M genes in more the RYSV 3 protein interacts with the N plant rhabdovirus genomes that are required protein, which suggests that the virus moves as for cell-to-cell movement in plants but not for a movement protein–nucleocapsid complex in invasion of insect hosts. Similar to RV and plants (40). VSV, plant rhabdoviruses can replicate in ani- Plant rhabdoviruses are also likely to en- mal (insect) nerve cells. MMV appears to use code proteins that suppress the plant de- its insect vector nervous system for reaching

462 Ammar et al. ANRV363-EN54-23 ARI 23 October 2008 14:4

the salivary glands, as does RV in humans sequence data for P. maidis; soluble, recombi- and animals. Proteins of vertebrate and inver- nant forms of plant rhabdovirus G proteins; tebrate nerve cells are frequently conserved. and development of RNA interference (RNAi) RNA interference These include receptors and other proteins in- tools for hemipteran insect hosts. These tools (RNAi): a mechanism volved in rhabdovirus invasion. Examples are will facilitate more in-depth studies on plant triggered by acetylcholine receptors and LC8. The conser- rhabdovirus-vector interaction, including the double-stranded RNA vation of these genes in vertebrate and inver- role of receptor molecules in vector/host speci- that inhibits gene tebrate animals and their documented role in ﬁcity. Finally, further research is needed on expression or degrades viral RNA rhabdovirus infection suggest that they may the possible roles of chemical and physiological also be involved in rhabdovirus neurotropism in conditions in the hemolymph and of salivary insects. Important tools that have become avail- secretions on enhancing or obstructing virus able include the SiV-Drosophila system; EST transmission by insect vectors.

SUMMARY POINTS 1. There are more than 160 viral species in the family Rhabdoviridae, many of which pose a threat to human, animal, or plant health. At least 90 rhabdoviruses infect monocotyle- donous or dicotyledonous plants. 2. Plant rhabdoviruses require hemipteran insect or mite vectors for their transmission and spread in nature, and they are transmitted in a persistent propagative mode by these vectors. 3. Most plant rhabdoviruses are transmitted by one or a few related vector species. This vector speciﬁcity is due at least partly to the existence of midgut infection and escape barriers as well as salivary gland infection and escape barriers in the arthropod vectors. In addition, the ability of the virus to escape from and minimize induction of the insect host immune system may play a role. 4. Plant rhabdoviruses can infect the nervous system of their insect hosts. A neurotropic route for MMV from the midgut to the salivary glands of the planthopper vector P.maidis has been postulated. Other possible routes for propagative plant and animal rhabdoviruses in their vectors may be through the hemolymph and/or tracheal and muscle tissues. 5. Rhabdovirus entry into host cells is mediated by the surface G protein, that binds to a cellular receptor and initiates fusion of viral and host membranes. Hence, the G protein by U.S. Department of Agriculture on 12/31/08. For personal use only. is a likely determinant of host speciﬁcity and virulence. 6. Plant and animal rhabdoviruses generally have no obvious deleterious effects on longevity Annu. Rev. Entomol. 2009.54:447-468. Downloaded from arjournals.annualreviews.org or reproduction of their insect hosts as opposed to their more severe pathogenic effects on their plant or vertebrate hosts. Virus-derived modulating factors and the effectiveness of the immune response of the insects are likely involved in limiting the replication and pathogenic effects of such viruses on their vectors. 7. Molecular interactions between rhabdoviruses and their plant hosts can lead to virus resistance, analogous to those that occur in D. melanogaster for resistance to SiV. 8. Novel tools, such as the availability of the SiV-Drosophila system; EST sequence data for P. maidis; soluble, recombinant forms of plant rhabdovirus G proteins; and development of RNAi tools for hemipteran insect hosts, should allow more in-depth studies on plant rhabdovirus-insect vector interactions.

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DISCLOSURE STATEMENT The authors are not aware of any biases that might be perceived as affecting the objectivity of this review.

ACKNOWLEDGMENTS We thank Jane Todd, Omprakash Mittapalli, Valdir Correa, and Dorith Rotenberg for their valuable comments on this manuscript. Work in our laboratories was supported by OARDC, USDA-NRI, USDA-ARS, and Consortium for Plant Biotechnology Research. This is Kansas State Experiment Station Contribution No. 09-063-J.

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Frontispiece Edward S. Ross pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppxiv Lifelong Safari: The Story of a 93-Year-Old Peripatetic Insect Hunter Edward S. Ross ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp1 Ecology and Geographical Expansion of Japanese Encephalitis Virus Andrew F. van den Hurk, Scott A. Ritchie, and John S. Mackenzie ppppppppppppppppppppppp17 Species Interactions Among Larval Mosquitoes: Context Dependence Across Habitat Gradients Steven A. Juliano pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp37 Role of Glucosinolates in Insect-Plant Relationships and Multitrophic Interactions Richard J. Hopkins, Nicole M. van Dam, and Joop J.A. van Loon pppppppppppppppppppppppp57 Conﬂict, Convergent Evolution, and the Relative Importance of Immature and Adult Characters in Endopterygote Phylogenetics Rudolf Meier and Gwynne Shimin Lim ppppppppppppppppppppppppppppppppppppppppppppppppppppp85 Gonadal Ecdysteroidogenesis in Arthropoda: Occurrence and Regulation by U.S. Department of Agriculture on 12/31/08. For personal use only. Mark R. Brown, Douglas H. Sieglaff, and Huw H. Rees ppppppppppppppppppppppppppppppppp105 Roles of Thermal Adaptation and Chemical Ecology in Liriomyza Annu. Rev. Entomol. 2009.54:447-468. Downloaded from arjournals.annualreviews.org Distribution and Control Le Kang, Bing Chen, Jia-Ning Wei, and Tong-Xian Liu pppppppppppppppppppppppppppppppp127 Fitness Costs of Insect Resistance to Bacillus thuringiensis Aaron J. Gassmann, Yves Carrière, and Bruce E. Tabashnik ppppppppppppppppppppppppppppp147 Insect Herbivore Nutrient Regulation Spencer T. Behmer ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp165 Manipulation of Host Behavior by Parasitic Insects and Insect Parasites Frederic Libersat, Antonia Delago, and Ram Gal ppppppppppppppppppppppppppppppppppppppppp189 Bionomics of Bagworms (Lepidoptera: Psychidae) Marc Rhainds, Donald R. Davis, and Peter W. Price ppppppppppppppppppppppppppppppppppppp209

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