Details of DPV and References
DPV NO: 244 July 1981
Species: | Acronym:
Plant rhabdovirus group
D. Peters Agricultural University, Department of Virology, Binnenhaven 11, 6709 PD Wageningen, The Netherlands
- Type Member
- Main Characteristics
- Geographical Distribution
- Transmission by Vectors
- Ecology and Control
- Relations with Cells and Tissues
- Properties of Particles
- Genome Properties
- Defective-Interfering RNA
- Notes on Tentative Members
- Affinities with Other Groups
Subgroup I: lettuce necrotic yellows virus (cytoplasm-associated)
Subgroup II: potato yellow dwarf virus (nucleus-associated)
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).
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
|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|
|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
|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||-||-||-|
|Chandrilla juncea||ee||58 x 135||nuc||-||-|
|Clover enation||ff||80 x 200||nuc||-||-|
|Gerbera sp.||hh||60/70 x 150/300||-||-||-|
|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||-||-||-|
|Melon variegation||pp||60 x 320||cyt||-||-|
|Pineapple chlorotic leaf streak||60/70 x 200/250||nuc||-||-|
|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||-||-||-|
|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.
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.
Transmission by 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 and Control
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 & OLoughlin, 1977). The reverse has been noticed for RTYV (Chen & Shikata, 1972). With LNYV (OLoughlin & 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).
Properties of Particles
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).
|M.Wt. of structural proteins (x 10-3)||Ref.|
* 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).
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).
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.
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.
References list for DPV: Plant rhabdovirus group (244)
- Amici, Faoro & Tornaghi, Riv. Patol. veg. 14: 85, 1978.
- Anon, Scientia sin. 22: 573, 1979.
- Ball & White, Proc. natn. Acad. Sci. U.S.A. 73: 442, 1976.
- Barckhaus & Weinert, Protoplasma 84: 101, 1975.
- Boakye & Randles, Aust. J. agric. Res. 25: 791, 1974.
- Brown, Bishop, Crick, Francki, Holland, Hull, Johnson, Martelli, Murphy, Obijeski, Peters, Pringle, Reichmann, Schneider, Shope, Simpson, Summers & Wagner, Intervirology 12: 1, 1979.
- Caner, July & Vicente, Summa Phytopath. 2: 264, 1976.
- Chagas, Phytopath. Z. 99: 301, 1980.
- Chang, Doi & Yora, Ann. Phytopath. Soc. Japan 42: 383, 1976.
- Chen & Shikata, Virology 47: 483, 1972.
- Chiu, Liu, MacLeod & Black, Virology 40: 387, 1970.
- Ciampor & Dokoupil, Acta Virol. 18: 355, 1974.
- Codaccioni & Cossard, C. r. hebd. Acad. Séanc. Paris 280: 1497, 1975.
- Conti, Ricerca scient. 39: 3, 1969.
- Conti & Appiano, J. gen. Virol. 21: 315, 1973.
- Duffus, Virology 24: 194, 1963.
- Eisbein, Arch. Phytopath. PflSchutz 12: 299, 1976.
- Emerson & Wagner, J. Virol. 10: 297, 1972.
- Francki & Randles, in Rhabdoviruses, p. 135, ed. D. H. L. Bishop, West Palm Beach: CRC press, 1980.
- Francki, Kitajima & Peters, in Handbook of Plant Virus Infections and Comparative Diagnosis, p. 455, ed. E. Kurstak, Amsterdam: Elsevier/North-Holland, 1981.
- Franco, Russo & Martelli, Phytopath. Medit. 18: 41, 1979.
- Garrett & O'Loughlin, Virology 76: 653, 1977.
- Gollifer, Jackson, Dabek, Plumb & May, PANS 23: 171, 1977.
- Greber, Aust. J. agric. Res. 30: 43, 1979.
- Greber & Gowanlock, Aust. J. biol. Sci. 32: 399, 1979.
- Hasan, Giannotti & Vago, Phytopathology 63: 791, 1973.
- Hills & Campbell, J. Ultrastruct. Res. 24: 134, 1968.
- Hitchborn, Hills & Hull, Virology 28: 768, 1966.
- Hsieh, Pl. Prot. Bull. F. A. O. 11: 159, 1969.
- Hsu, Virology 84: 9, 1978.
- Jackson & Christie, Virology 77: 344, 1977.
- Jackson, Milbrath & Jedlinski, in Virus and Virus-like Diseases of Maize and Sorghum in the United States, p. 54, ed. D. T. Gordon, J. K. Knoke & G. E. Scott, Wooster, Ohio: Southern Reg. Res. Publ., 1981.
- Jedlinski, Proc. Am. Phytopath Soc. 3: 19, 1976.
- Keene, Schubert & Lazzarini, Proc. natn. Acad. Sci. U.S.A. 74: 1353, 1977.
- Kitajima, Phytopath. Z. 82: 83, 1975.
- Kitajima & Costa, Virology 29: 523, 1966.
- Kitajima & Costa, Fitopat. Brasil. 4: 55, 1979.
- Kitajima, Lauritis & Swift, J. Ultrastruct. Res. 29: 141, 1969.
- Kitajima, Müller, Costa & Yuki, Virology 50: 254, 1972.
- Kitajima, Cupertino & Caetano, Fitopatologia 11: 16, 1976.
- Knipe, Rose & Lodish, J. Virol. 15: 1004, 1975.
- Knudson & MacLeod, Virology 47: 285, 1972.
- Kusunoki, Chang, Arai, Doi & Yora, Ann. Phytopath. Soc. Japan 43: 125, 1977.
- Lawson & Ali, J. Ultrastruct. Res. 53: 345, 1975.
- Leclant, Alliot & Signoret, Annls Phytopath. 5: 441, 1973.
- Lee, Virology 33: 84, 1967.
- Lee & Peters, Virology 48: 739, 1972.
- Lesemann, Phytopath. Z. 73: 83, 1972.
- Lundsgaard & Albrechtsen, Phytopath. Z. 87: 12, 1972.
- Maramorosch, Hirumi, Kimura, Bird & Vakili, Pl. Prot. Bull. F.A.O. 22: 32, 1974.
- Maramorosch, Govindu & Kondo, Pl. Dis. Reptr 61: 1029, 1977.
- Martelli & Castellano, Phytopath. medit. 9: 39, 1970.
- Martelli & Russo, in Insect and Plant Viruses: an Atlas, p. 181, ed. K. Maramorosch, New York: Academic Press, 1977.
- Milner & Jackson, Virology 97: 90, 1979.
- Murant & Roberts, Acta Hort. 95: 31, 1980:.
- Ohki, Doi & Yora, Ann. Phytopath. Soc. Japan 44: 202, 1978.
- OLoughlin & Chambers, Virology 33: 262, 1967.
- Peters, J. Ultrastruct. Res. 58: 166, 1977.
- Peters & Black, Virology 40: 847, 1970.
- Plese, Acta bot. croat. 38: 19, 1979.
- Plumb & James, Ann. appl. Biol. 80: 181, 1975.
- Polák, Králik & Limberk, Acta phytopath. Acad. Sci. hung. 12: 157, 1977.
- Proeseler, NachrBl. PflSchutz DDR 32: 254, 1978.
- Proeseler, in Vectors of Plant Pathogens, p. 97, ed. K. F. Harris & K. Maramorosch, New York: Academic Press, 1980.
- Rana & Franco, Phytopath. medit. 18: 48, 1979.
- Razvyaskina & Polyakova, Dokl. Akad. Nauk. SSSR 174: 1435, 1967.
- Rubio-Huertos, Phytopath. Z. 92: 294, 1978a.
- Rubio-Huertos, Phytopath. Z. 93: 1, 1978b.
- Rubio-Huertos & Bos, Neth. J. Pl. Path. 75: 329, 1969.
- Rubio Huertos & Peña-Iglesias, Pl. Dis. Reptr 57: 649, 1973.
- Russo, Martelli & Rana, Phytopath. Z. 83: 223, 1975.
- Russo, Castellano & Martelli, Phytopath. Z. 96: 122, 1979.
- Schmutterer, Z. PflKrankh. PflPath. PflSchutz 87: 145, 1980.
- Schultz, Harrap & Land, Ann. appl. Biol. 80: 251, 1975.
- Shaskolskaya, Zool. Zh. 41: 717, 1962.
- Signoret, Conti, Leclant, Alliott & Giannotti, Annls Phytopath. 9: 381, 1978.
- Sinha, Virology 44: 342, 1971.
- Sinha & Chiykowski, Virology 32: 402, 1967.
- Slykhuis & Sherwood, Can. J. Bot. 42: 1123, 1964.
- Sokol, Stancek & Koprowski, J. Virol. 7: 241, 1971.
- Su, in The Virus Diseases of the Rice Plant (Proc. Symp. int. Rice Res. Inst.), p.13, Baltimore: John Hopkins, 1969.
- Sylvester, Virology 38: 440, 1969.
- Sylvester & Richardson, Virology 37: 26, 1969.
- Sylvester & Richardson, Virology 42: 1023, 1970.
- Sylvester, Richardson & Frazier, Virology 59: 301, 1974.
- Tomlinson & Webb, Rept. natn. Veg. Res. Stn, 1973: 100, 1974.
- Tomlinson, Webb & Faithfull, Ann. appl. Biol. 71: 127, 1972.
- Toriyama, Ann. Phytopath. Soc. Japan 42: 563, 1976.
- Toriyama & Peters, J. gen. Virol. 50: 124, 1980.
- Toriyama & Peters, J. gen. Virol. 56: 59, 1981.
- Trefzger-Stevens & Lee, Virology 78: 144, 1977.
- Vega, Gracia, Rubio-Huertos & Feldman, Phytopath. Z. 85: 7, 1976.
- Vela & Rubio-Huertos, Phytopath. Z. 79: 343, 1974.
- Wagner, Emerson, Imblum & Kelley, in Negative Strand Viruses, Vol. 1,p. 1, ed. B. W. J. Mahy & R. D. Barry, London: Academic Press, 1975.
- Wolanski & Chambers, Virology 44: 582, 1971.
- Yamada & Shikata, J. Fac. Agric. Hokkaido Univ. 56: 91, 1969.
- Yamashita, Okamoto, Fujii, Doi & Yora, Ann. Phytopath. Soc. Japan 44: 61, 1978.
- Ziemiecki & Peters, J. gen. Virol. 32: 369, 1976.