244
July 1981		Family: Rhabdoviridae
Genus:
Species:
Acronym:

Plant rhabdovirus group

D. Peters
Agricultural University, Department of Virology, Binnenhaven 11, 6709 PD Wageningen, The Netherlands

Contents

Type Member
Main Characteristics
Members
Geographical Distribution etc
Association with Vectors
Ecology
Relations with Cells and Tissues
Particle Properties
Genome Properties
Replication
Satellites
Defective-Interfering RNA
Relationships within the Taxon
Notes on Tentative Members
Affinities with Other Groups
Notes
References
Acknowledgements
Figures

Type Member

Subgroup I: lettuce necrotic yellows virus (cytoplasm-associated)
Subgroup II: potato yellow dwarf virus (nucleus-associated)

Main Characteristics

Bacilliform and/or bullet-shaped particles normally 200 to 350 nm long and 70 to 95 nm in diameter, sedimenting at 1,000 to 1,200 S. The particles possess a unit membrane envelope which surrounds the nucleocapsid and from which 5 to 12 nm-long spikes protrude. The nucleocapsid forms a precisely coiled helix with a hemispherical and a blunt end. Particles of plant rhabdoviruses contain at least four proteins; all have proteins designated N (‘nucleocapsid protein’, M. Wt 55 to 64 x 103) and G (‘glycoprotein’, M. Wt 71 to 92 x 103); in addition, some have proteins L (‘large’, M. Wt 145 x 103), M (‘matrix’, M. Wt 22 to 25 x 103) and Ns (‘non-structural’, M. Wt 40 x 103) whereas others have proteins M1 and M2 (M. Wts 27 to 44 x 103 and 22 to 39 x 103), together with some undefined proteins in minor quantities. The particles contain single-stranded RNA of negative polarity. A RNA dependent RNA polymerase is associated with the nucleocapsid. Infectivity in sap survives 10 min at 50 to 52°C, less than 1 day at 4 to 25°C; concentration in sap is 1 to 10 mg/l. Transmission occurs by plant-sucking arthropods in a circulative (propagative) manner; some members can be transmitted mechanically. Host range of individual members is often limited to one or a few plant and vector species. The viruses cause various types of symptom in monocotyledonous and dicotyledonous plants. In plant and vector cells, the virus particles occur either scattered through the cytoplasm or in large aggregates in the perinuclear space.

Data on plant-infecting rhabdoviruses are reviewed by Francki, Kitajima & Peters (1981), Francki & Randles (1980) and Jackson, Milbrath & Jedlinski (1981).

Members

Table 1 lists definitive and tentative members with some of their properties. Those listed as tentative have typical particle morphology in plant cell sections but have not been studied further.

Table 1. Definitive and tentative members of the plant rhabdovirus group

Virus (or host if virus not named) Desc. no. or ref. Size and shape (nm) Main cellular
site of
accumulation*		 Vector Transmitted by sap inoculation?
(a) Definitive members
Barley yellow striate mosaic (BYSMV) a 45 x 330 cyt (Au) Laodelphax striatellus No
Beet leafcurl (BLCV) b 80 x 250 nuc (Gy) Piesma quadratum No
Broccoli necrotic yellows (BNYV) 85 64 x 297 cyt (Ap) Brevicoryne brassicae Yes
Carrot latent (CLV) c 70 x 220 nuc (Ap) Semiaphis heraclei No
Cereal chlorotic mottle (CCMV) d 65 x 230 nuc (Au) Nesoclutha pallida No
Coffee ringspot (CRV) e 65 x 183 nuc (Ac) Brevipalpus phoenicis Yes
Colocasia bobone disease (CBDV) f 50/55 x 300/335 nuc (Au) Tarophagus proserpina No
Cow-parsnip mosaic g 90 x 265 nuc - Yes
Cynara h 75 x 260 cyt - Yes
Digitaria striate (DSV) i 55 x 280 cyt (Au) Sogatella kalophon No
Eggplant mottled dwarf (EMDV) 115 66 x 220 nuc - Yes
Euonymus fasciation j - cyt - No
Festuca leaf streak k 61 x 330 cyt - No
Finger millet mosaic l 80 x 285 nuc (Au) Sogatella longifurcifera No
Gomphrena (GV) m 75 x 230/250 nuc - Yes
Laburnum yellow vein n 89 x 245 nuc - -
Lettuce necrotic yellows (LNYV) 26 52 x 360 cyt (Ap) Hyperomyzus lactucae Yes
Lucerne enation (LEV) o 85 x 250 nuc (Ap) Aphis craccivora No
Maize mosaic (MMV) 94 75 x 300 nuc (Au) Peregrinus maidis No
Melilotus latent (MLV) p 80 x 330/350 nuc - -
Northern cereal mosaic (NCMV) q 60 x 300/350 cyt (Au) Laodelphax striatellus No
Oat striate mosaic (OSMV) r 75 x 210 nuc (Au) Graminella nigrifons No
Parsley latent (PLV) s 87 x 214 cyt (Ap) Cavariella aegopodii Yes
Pelargonium vein clearing t 70 x 250 nuc - Yes
Pisum u 45 x 240 cyt - Yes
Pittosporum vein yellowing (PVYV) v 80 x 245 nuc - Yes
Plantago lanceolata w 63 x 330 - - -
Potato yellow dwarf (PYDV) 35 75 x 380 nuc (Au) Aceratagallia sanguinolenta,
Agallia constricta & others 		Yes
Raspberry vein chlorosis (RVCV) 174 65/80 x 430/500 cyt (Ap) Aphis idaei No
Rice transitory yellowing (RTYV) 100 93 x 325 nuc (Au) Nephotettix apicalis No
Sonchus yellow net (SYNV) 205 94 x 248 nuc (Ap) Aphis coreopsidis Yes
Sonchus (SV) x 50/70 x 250/300 cyt - Yes
Sowthistle yellow vein (SYVV) 62 95 x 220 nuc (Ap) Hyperomyzus lactucae No
Strawberry crinkle (SCV) 163 69 x 190/380 cyt (Ap) Chaetosiphon fragaefolii No
Wheat chlorotic streak mosaic (WCSMV) y 55 x 355 cyt (Au) Laodelphax striatellus No
Wheat rosette stunt (WRSV) z 50/55 x 320/400 cyt (Au) Laodelphax striatellus No
Wheat (American) striate mosaic (WSMV) 99 75 x 250 nuc/cyt (Au) Endria inimica No
Winter wheat (Russian) mosaic (WWMV) aa 60 x 260 - (Au) Psammotettix striatus & others No
 
(b) Tentative members
Atropa belladonna bb 55 x 310 - - -
Cajanus cajan cc - - - -
Callistephus chinensis dd - - - -
Chandrilla juncea ee 58 x 135 nuc - -
Chrysanthemum sp. dd - - - -
Clover enation ff 80 x 200 nuc - -
Dendrobium sp.† gg - - - -
Gerbera sp. hh 60/70 x 150/300 - - -
Holcus lanatus ii - - - -
Iris germanica jj 52 x 320 cyt - -
Ivy vein-clearing kk 55 x 325 cyt - -
Laelia red leafspot ll 80 x 280 - - -
Lemon scented thyme mm 72 x 219 nuc - -
Lotus streak nn 90 x 300/340 cyt? - -
Lupin yellow vein oo 82/89 x 250 - - -
Manihot esculenta dd - - - -
Melon variegation pp 60 x 320 cyt - -
Pineapple chlorotic leaf streak qq 60/70 x 200/250 nuc - -
Phalaenopsis sp.† gg - - - -
Pogostemon patchouli dd - - - -
Ranunculus repens ii - - - -
Raphanus sp. dd - cyt - -
Red clover mosaic (RCMV) rr 65 x 300 nuc - -
Ryegrass bacilliform ss 68 x 287 nuc - -
Saintpaulia leaf necrosis tt 60/65 x 200/220 - - -
Sambucus vein clearing uu 80 x 275 - - -
Sarracenia purpurea vv - - - -
Triticum aestivum ww - - - -
Vigna sinensis xx - - - -
Zea mays yy 50 x 325 cyt - -

* Virus accumulates predominantly in the perinuclear space (nuc) or cytoplasm (cyt)
† See also ‘Affinities with Other Groups’

(a) Conti & Appiano, 1973; (b) Eisbein, 1976; (c) Ohki, Doi & Yora, 1978; (d) Greber & Gowanlock, 1979; (e) Chagas, 1980; (f) Gollifer et al., 1977; (g) Polák, Králik & Limberk, 1977; (h) Russo, Martelli & Rana, 1975; (i) Greber, 1979; (j) Codaccioni & Cossard, 1975; (k) Lundsgaard & Albrechtsen, 1972; (l) Maramorosch, Govindu & Kondo, 1977; (m) Kitajima & Costa, 1966; (n) Plese, 1979; (o) Leclant, Alliot & Signoret, 1973; (p) Kitajima et al., 1969; (q) Toriyama,1976; (r) Jedlinski, 1976; (s) Tomlinson & Webb, 1974; (t) Franco, Russo & Martelli, 1979; (u) Caner, July & Vicente,1976; (v) Rana & Franco, 1979; (w) Hitchborn, Hills & Hull, 1966; (x) Vega et al., 1976; (y) Signoret et al., 1978; (z) Anon, 1979; (aa) Razvyaskina & Polyakova, 1967; (bb) Lesemann, 1972; (cc) Maramorosch et al., 1974; (dd) Kitajima & Costa, 1979; (ee) Hasan, Giannotti & Vago, 1973; (ff) Rubio-Huertos & Bos, 1969; (gg) Lawson & Ali, 1975; (hh) Chang,Doi & Yora, 1976; (ii) Amici, Faoro & Tornaghi, 1978; (jj) Rubio-Huertos, 1978a; (kk) Russo, Castellano & Martelli,1979; (ll) Peters, 1977; (mm) Schultz, Harrap & Land, 1975; (nn) Yamashita et al., 1978; (oo) Tomlinson, Webb & Faithfull, 1972; (pp) Rubio-Huertos & Peña-Iglesias, 1973; (qq) Kitajima, 1975; (rr) Vela & Rubio-Huertos, 1974; (ss) Plumb & James, 1975; (tt) Ciampor & Dokoupil, 1974; (uu) Kusonoki et al., 1977; (vv) Barckhaus & Weinert, 1975; (ww) Kitajima, Cupertino & Caetano, 1976; (xx) E. W. Kitajima & A. S. Costa, personal communication; (yy) Rubio-Huertos, 1978b.

Geographical Distribution etc

Rhabdoviruses have been reported from most parts of the world including tropical, subtropical and temperate regions. Some viruses, such as MMV, RVCV and SCV, are fairly widespread. BNYV has been reported from most parts of the world. Many individual rhabdoviruses seem to have restricted distributions and this probably reflects the distributions of their vectors. Plant host ranges of most individual members are narrow. Rhabdoviruses have been reported in grasses from all parts of the world, but their relationships have not been studied. BYSMV, NCMV, WCSMV and WWMV have similar host ranges.

Association with Vectors

Transmitted by plant-sucking arthropods. Of 25 members whose vectors are known, all except two are transmitted by species of Hemiptera. BLCV is transmitted by larvae and adults of the beet bug Piesma quadratum (Proeseler, 1978) and CRV by the mite Brevipalpus phoenicis (Chagas, 1980). The vector-virus relationship is highly specific with often only one vector species and possibly some related species involved. However, the aphid Hyperomyzus lactucae transmits two rhabdoviruses, LNYV and SYVV, and the leafhopper Laodelphax striatellus transmits four, BYSMV, NCMV, WCSMV and WRSV. There is direct evidence that NCMV, PYDV, RTYV, SCV, SYVV and WSMV multiply in their vectors (Yamada & Shikata, 1969; Chiu et al., 1970; Hsieh, 1969; Sylvester, Richardson & Frazier, 1974; Sylvester & Richardson, 1969; Sinha & Chiykowski, 1967). Other viruses, for example BYSMV, CCMV, DSMV, LNYV, MMV, RVCV and WWMV, are circulative and virus particles have been seen in thin sections of vector tissues (Francki & Randles, 1980; Jackson, Milbrath & Jedlinski, 1981; Murant & Roberts, 1980). The efficiency of transmission increases with the length of acquisition and inoculation access periods. The incubation period is temperature-dependent and ranges from 4 days for WSMV, or 5 to 8 days for SYVV and LNYV, to an average of 24 days for OSMV in Graminella nigrifrons (Slykhuis & Sherwood, 1964; Duffus, 1963; Boakye & Randles, 1974; Jackson et al., 1981). The vector may remain viruliferous for life but transmits less efficiently with increasing age. Transmission through the egg has been reported for SYVV (Sylvester, 1969) and LNYV (Boakye & Randles, 1974) in the aphid H. lactucae; BYSMV and WWMV are reported to pass through the eggs of the leafhoppers L. striatellus and Psammotettix striatus (Conti, 1969; Shaskolskaya, 1962).

Ecology

Each virus must survive between crops in populations of its specific vector(s), or in weed, perennial or volunteer host plants. RTYV is destructive when transmitted from the first of two seasonal rice crops to seedlings of the second (Su, 1969). Infection of beet with BLCV occurs by overwintering young adults of the beet bug (Proeseler, 1980); larvae that acquire the virus can also transmit (Schmutterer, 1980). LNYV is spread to lettuce from sowthistle by H. lactucae during host-seeking migration in which the aphid is stimulated by starvation and desiccation to settle and probe on lettuce (Boakye & Randles, 1974). Some rhabdoviruses, such as SCV and RVCV, may be disseminated in infected planting material and can be controlled by planting virus-free stocks. Seed transmission has not been reported. Some rhabdoviruses (but none of those infecting species of Gramineae) are transmissible by mechanical techniques, but spread in this way is of no importance in field conditions. All known rhabdoviruses infecting species of Gramineae are transmitted by either leafhoppers or planthoppers.

Relations with Cells and Tissues

Plant symptoms often increase in severity with age of infection; recovery has been reported for OSMV. The rhabdoviruses infect nearly all organs and tissues of their host plants, the parenchymatous cells of vascular bundles often being preferred.

The particles of most plant rhabdoviruses bud at the inner nuclear membrane and accumulate in the perinuclear space. Extensive virus aggregation in the perinuclear space can lead to production of cytoplasmic and nuclear invaginations filled with virus particles (Lee, 1967; Martelli & Russo, 1977). Particles of some viruses that accumulate in the perinuclear space, such as EMDV (Martelli & Castellano, 1970), RCMV (Vela & Rubio-Huertos, 1974) and WSMV (Sinha, 1971), occur also in the cytoplasm, dispersed singly, in groups or in large aggregations, either bound by a membrane or free.

Particles of other rhabdoviruses mature in the cytoplasm; some, such as those of LYNV (Wolanski & Chambers, 1971) and BNYV (Hills & Campbell, 1968), occur in association with the endoplasmic reticulum and accumulate almost exclusively in vesicles. Those of others, such as BYSMV (Conti & Appiano, 1973) and NCMV (Toriyama, 1976), are found in membrane-bound viroplasms and accumulate in vacuole-like spaces.

In addition to the variation in site of assembly and accumulation, the viruses cause diverse types of aberration in the infected cell. Many induce the formation of membraneous vesicles in the cytoplasm or perinuclear space. With EMDV (Martelli & Russo, 1977) and SYVV (Lee & Peters, 1972), the nuclei are the only organelles seriously affected: chromatin disappears, the nucleolus swells and a uniform granular nucleoplasm appears. In cells infected with BNYV the mitochondria are swollen and contain few cristae (Hills & Campbell, 1968). No particles of any plant rhabdovirus have been found in the mitochondria or chloroplasts. Occasionally, structures resembling viral nucleocapsids are observed in the nucleoplasm (Kitajima, Lauritis & Swift, 1969; Rubio-Huertos & Bos. 1969).

In most instances, the cellular location of rhabdovirus particles in vectors appears to be the same as in their plant hosts. However, BNYV accumulates in the perinuclear space of insect cells, whereas in plant cells it accumulates mainly in the cytoplasm (Garrett & O’Loughlin, 1977). The reverse has been noticed for RTYV (Chen & Shikata, 1972). With LNYV (O’Loughlin & Chambers, 1967) and SYVV (Sylvester & Richardson, 1970) many more uncoated nucleoprotein particles are observed in cells of insect vectors than in plant cells. PYDV induces fusion of Aceratagallia sanguinolenta cells in culture (Hsu, 1978).

Particle Properties

Plant rhabdoviruses contain c. 70% protein, 25% lipids, 4% polysaccharides and 1% RNA and consist of a nucleocapsid surrounded by a membrane. The nucleocapsid, shaped like a hollow bullet 130 to 300 nm long and 45 to 65 nm wide, is formed by a helically wound nucleoprotein strand composed of a single-stranded RNA genome and a nucleocapsid protein (N). The tubular part of the nucleocapsid consists of c. 40 turns of the helix with a pitch of 4.0 to 4.5 nm; the structure of the hemispherical end is not determined. Table 2 gives the M. Wt of the proteins reported in the particles of some plant rhabdoviruses, in comparison with those found in the particles of vesicular stomatitis virus (VSV), the best studied animal-infecting rhabdovirus (J. L. Dale & D. Peters, unpublished data). Proteins N and G are found in all the viruses; protein G forms a hexagonal array over the outside of the membrane. Proteins L and Ns, which in VSV are associated with the nucleocapsid and possess polymerase activity (Wagner et al., 1975) have been detected in some plant rhabdoviruses. In VSV, protein M forms the inner surface of the membrane and bridges the G and N proteins; protein M occurs in WSMV and LNYV but not in PYDV, SYNV or SYVV, which instead have proteins M1 and M2. Thus, in the protein composition of their particles, plant rhabdoviruses budding in the cytoplasm resemble VSV but those budding at the nuclear membrane are somewhat different.

Table 2. Comparison of structural protein species found in plant rhabdoviruses with those found in vesicular stomatitis virus (VSV).

Virus     Proposed
subgroup		 Cellular
site of
accumulation*		 M.Wt. of structural proteins (x 10-3) Ref.
L G N Ns M   M1     M2  
 
VSV		 cyt 150
(20-
50)†		 75
(500-
1500)		 56
(1000-
2000)		 45
(100-
300)		 25
(1600-
4000)		 a
LNYV I cyt 170 71 56 38 19 b
SV I cyt 170 72 55 38 19 b
BNYV I cyt 93 60 18 c
WSMV I? nuc/cyt 145 92 59 25 d
EMDV II nuc 83 61 27 21 b
PYDV II nuc 78 56 33 22 e
SYNV II nuc 77 64 44 39 f
SYVV II nuc 83 60 44 36 g

* cyt = cytoplasm; nuc = perinuclear space
† Figures in parenthesis are number of molecules of each protein estimated to occur in each particle (Brown et al., 1979)

(a) Brown et al., 1979; (b) J. L. Dale & D. Peters, unpublished results; (c) D. Peters, unpublished results; (d) Trefzger-Stevens & Lee, 1977; (e) Knudson & MacLeod, 1972; (f) Jackson & Christie, 1977; (g) Ziemiecki & Peters, 1976.

Rhabdovirus particles disrupt in organic solvents. When LNYV particles are disrupted with nonionic detergent and then centrifuged on to a cushion of 20% sucrose the supernatant fraction consists mainly of membrane proteins and the pellet fraction contains nucleocapsid material (Toriyama & Peters, 1980). The pellet fraction has polymerase activity if the particles were disrupted under low salt conditions. If they were disrupted under high salt conditions the pellet fraction lacks polymerase activity but regains it when mixed with the supernatant fraction. In this behaviour, LNYV resembles VSV (Emerson & Wagner, 1972).

Genome Properties

The plant rhabdoviruses contain one single-stranded RNA species of M. Wt c. 4 x 106, which has negative polarity (i.e. it is complementary to its messenger RNA (mRNA) species produced in cells). The genome RNA by itself is not infective but the nucleocapsid released by non-ionic detergent is. Little information is available on the genome RNA for any plant rhabdovirus but a general similarity is to be expected to the genome RNA of VSV which terminates at the 5' end in GAAGCAppp and has the complementary sequence - CUUCGU - OH at the 3' end (Keene, Schubert & Lazzarini, 1977). The mRNA molecules of this virus are capped at the 5' end with the structure 7mGpppAm ACAG and carry poly-A at the 3' end; mRNA of SYNV appears also to be polyadenylated (Milner & Jackson, 1979). The gene-order in VSV is 5' -L, G, M, Ns, N - 3' (Ball & White, 1976). The several monocistronic mRNA species that occur in cells infected with VSV or in the in vitro product of VSV-RNA transcription can be translated into the G, N, Ns and M proteins (Knipe, Rose & Lodish, 1975).

Replication

Little is known about the site and mechanism of replication of the rhabdoviruses infecting plants. Experiments with LNYV suggest that the nucleus is involved (Wolanski & Chambers, 1971). RNA molecules complementary to SYNV-RNA are found in the cytoplasm of infected tobacco cells (Milner & Jackson, 1979). RNA synthesized in vitro after removal of the envelope of LNYV (Toriyama & Peters, 1980) and BNYV (Toriyama & Peters, 1981) is complementary to the viral RNA. Fluorescein-conjugated antibody studies show that antigens of PYDV (Chiu et al., 1970) and SYVV (Peters & Black, 1970) are at first confined to the nucleus of leafhopper and aphid cells in culture. Assembly occurs either preferentially at the inner nuclear membrane or at the endoplasmic reticulum in the cytoplasm.

Relationships within the Taxon

Although no subgroups of plant rhabdoviruses are officially recognised, two are now proposed, based on the cellular location of particle assembly, kinetics of transcriptase activity and protein composition of virus particles. The particles of viruses in subgroup I occur in the cytoplasm, contain protein M and possess transcriptase activity that is readily detectable in vitro. In these properties they resemble VSV. The particles of viruses in subgroup II accumulate in the perinuclear space, possess proteins M1 and M2, and have low in vitro transcriptase activity. They share these properties with rabies virus (Sokol, Stancek & Koprowski, 1971). No definite serological relationships between members of either subgroup have been established. The transcriptases of LNYV and BNYV are not interchangeable (Toriyama & Peters, 1981). BYSMV, NCMV, WCSMV and WRSV have the same vector species and particle dimensions. The first three viruses and WWMV have similar host ranges.

Affinities with Other Groups

Plant rhabdoviruses have many similarities to vertebrate-infecting rhabdoviruses. Indeed, further study may reveal that the affinity between subgroup I defined above and members of the vertebrate-infecting Vesiculovirus genus may be closer than that between subgroup I and subgroup II, which in turn may have its closest affinities with members of the vertebrate-infecting Lyssavirus genus.

No other well-characterized plant viruses have close affinities with plant rhabdoviruses. However, electron microscopy of thin sections of diseased orchids reveals bacilliform particles of two types. One type is undoubtedly typical of rhabdoviruses (Lawson & Ali, 1975; Peters, 1977). The other type is non-enveloped, c. 35 x 100 to 140 nm in size; these particles resemble the nucleocapsids of rhabdoviruses and form characteristic 'spoked-wheel' structures within the inner nuclear membrane. No information exists on the nature of their nucleic acid. Viruses producing these particles, including orchid fleck virus, which is the best studied (Descr. No. 183), and citrus leprosis virus (Kitajima et al., 1972), which has the same vector as CRV, may justify the formation of a new group.

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