294
July 1984		Family: Reoviridae
Genus:
Species:
Acronym:

Plant reovirus group

G. Boccardo
Istituto di Fitovirologia applicata del CNR, Via O. Vigliani 104, 10135 Torino, Italy

R. G. Milne
Istituto di Fitovirologia applicata del CNR, Via O. Vigliani 104, 10135 Torino, Italy

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 1 (phytoreoviruses): wound tumor virus
Subgroup 2 (fijiviruses): sugarcane Fiji disease virus
Subgroup 3: rice ragged stunt virus

Main Characteristics

Icosahedral double-shelled particles 65-75 nm in diameter, containing 10-12 segments of double-stranded RNA and at least six different polypeptides. Transmitted propagatively by phloem-feeding hemipterous insects (leafhoppers and planthoppers) but not mechanically except rarely by needle puncture. No seed transmission found. All members except rice dwarf virus are essentially confined to the phloem of infected plants, inducing hyperplasia of this tissue. Virus particles and characteristic viroplasms are confined to the cytoplasm. The plant reoviruses have recently been reviewed by Milne & Lovisolo (1977), Shikata (1977, 1981), Francki & Boccardo (1983) and Francki, Milne & Hatta (1984).

Members

Table 1 lists members of the group, their abbreviated names and some of their properties. All the plant reoviruses except RRSV fall naturally into two subgroups typified by WTV and FDV (Matthews, 1982). RRSV resembles subgroup 2 viruses in type of vector, host range, symptoms and number of genome segments, but the structure of the particle and the sizes of the genome segments are unlike those of other plant reoviruses, and seem to justify placing the virus in a separate category, subgroup 3.

Table 1. Members of the plant reovirus group and some of their properties

Virus No. of genome segments Main plant host Main vector Geographical
distribution 		Reference*
 
Subgroup 1 (phytoreoviruses)
Wound tumor (WTV) 12 Trifolium incarnatum Agalliopsis novella USA 1
Rice dwarf (RDV) 12 Oryza sativa Nephotettix cincticeps China, Japan, Korea 2
Rice gall dwarf (RGDV) 12 O. sativa N. nigropictus Malaysia, Thailand 3, 4, 5, 6, 7, 8
 
Subgroup 2 (fijviruses)
Sugarcane Fiji disease (FDV) 10 Saccharum officinarum Perkinsiella saccharicida Australia, Fiji, Madagascar, New Britain, New Guinea, New Hebrides, Samoa 9
Maize rough dwarf (MRDV)
(including cereal tillering disease (CTDV)
and mal de Rio Cuarto (MRCV))		 10 Zea mays Laodelphax striatellus Argentina, China†, central and southern Europe, Israel, Sweden 10, 11,12, 13
Rice black-streaked dwarf (RBSDV) 10 O. sativa L. striatellus China, Japan, Korea, 14, 15, 16
Pangola stunt (PaSV) 10 Digitaria decumbens Sogatella furcifera Brazil, Fiji, Guyana, Peru, Taiwan 17
Oat sterile dwarf (OSDV)
(including arrhenatherum blue dwarf (ABDV)
and lolium enation (LEV))		 10 Avena sativa Javesella pellucida Central and northern Europe 18, 19
 
Subgroup 3
Rice ragged stunt (RRSV) 10 O. sativa Nilaparvata lugens South-east Asia 20

* (1) Descr. 34; (2) Descr. 102; (3) Omura et al.,1980; (4) Ang & Omura, 1982; (5) Morikana et al., 1982; (6) Inoue & Omura, 1982; (7) Putta et al., 1982; (8) Omura et al., 1982; (9) Descr. 119; (10) Descr. 72; (11) Milne, Lindsten & Conti, 1975; (12) Milne et al., 1983; (13) Kung et al., 1981; (14) Descr. 135; (15) Lee, Hyung & Chung, 1977; (16) Reifman & Pinsker, 1976; (17) Descr. 175; (18) Descr. 217; (19) Luisoni et al., 1979; (20) Descr. 248.

†This virus, described as MRDV, may be nearer to RBSDV.

Geographical Distribution etc

The principal plant hosts, vectors and distributions of the viruses are shown in Table 1.

Subgroup 1. WTV, discovered in the leafhopper Agalliopsis novella and found, experimentally, to infect at least 20 dicotyledonous plant families, has never been detected in plants in nature or re-isolated from hoppers. Tumours grow at sites where infected plants have been wounded or where lateral roots grow out. RDV infects rice and at least 14 other species of Gramineae, causing chlorotic flecks and streaks, dwarfing and excess tillering. RDV is the only plant reovirus that does not provoke enlargement and division of infected cells. RGDV naturally infects rice and can be transmitted to several cereals and grasses but not maize or sorghum. It produces symptoms typical of subgroup 2 viruses (Omura et al., 1980; Ang & Omura, 1982; Putta et al., 1982).

Subgroup 2. Widespread, being reported from most tropical, subtropical and temperate regions except Africa and North America. All subgroup 2 viruses induce similar and characteristic symptoms. Infected plants are stunted, produce excess tillers and may not flower; they become abnormally dark green, except PaSV-infected plants, which may become reddish or chlorotic. Leaves may be distorted, ragged or 'bitten'; enations or galls develop on the backs of the veins of leaves, sheaths and stems.

Subgroup 3. RRSV is apparently confined to south-east and far-east Asia. Symptoms resemble those induced by subgroup 2 viruses. Only Oryza species are naturally infected, though several cereals are reported as experimental hosts (Hibino, 1979; Shikata et al., 1979; Descr. 248).

Association with Vectors

Transmitted propagatively by leafhoppers (Cicadellidae, Cicadoidea) (subgroup 1) and planthoppers (Delphacidae, Fulgoroidea) (subgroups 2 and 3). Minimum acquisition feeding time, latent (incubation) period and minimum inoculation feeding time are about 1-24 h, 10-20 days, and 1 h respectively. Usually less than half the hoppers having access to virus subsequently transmit, though a higher proportion may contain virus.

Subgroup 1. For reviews, see Reddy (1977), Black (1979), Maramorosch & Harris (1979), Chiykowski (1981), Shikata (1981) and Conti (1983, 1984). Early this century, Nephotettix cincticeps, the main vector of RDV, was the first insect shown to transmit a plant disease, and the first shown to pass a virus on to its progeny (Fukushi, 1969; Descr. 102). Multiplication of WTV in its vector has also been demonstrated (Descr. 34; see also Relations with Cells and Tissues). WTV has been grown in vitro in vector cell monolayers and in cells of non-vector leafhoppers (Black, 1979). RDV-infected leafhopper cell lines have also been established (Mitsuhashi & Nasu, 1967). Prolonged maintenance of WTV in hopper cell cultures causes selection of variants which have lost ability to reinfect plants when inoculated via living leafhoppers. It is not clear, however, whether these isolates were unable to multiply in the plants or had failed to enter the insects’ salivary glands and thus to be transmitted (Black, 1979). Propagation of WTV or RDV for long periods solely in plants leads to deletions within the genome and loss of vector transmissibility (Reddy & Black, 1974; Kimura, 1976).

Subgroup 1 viruses pass through the eggs of leafhoppers to a high proportion of progeny insects: 1.8-100% for WTV (Descr. 34), 60-85% for RDV (Descr. 102) and 87% for RGDV (Inoue & Omura, 1982). The effects of virus infection on the hoppers have not been thoroughly studied, but WTV-containing individuals apparently show no macroscopic evidence of disease (Descr. 34), and lifespan and fecundity appear normal (Maramorosch & Harris, 1979). In contrast, nymphs of Inazuma dorsalis infected with RDV through the egg tend to die prematurely (Descr. 102).

Subgroups 2 and 3. For reviews, see Harpaz (1972), Milne & Lovisolo (1977), Maramorosch & Harris (1979), Shikata (1981), Francki & Boccardo (1983) and Conti (1983, 1984). Evidence for the multiplication of these viruses in their vectors is based on transmission characteristics and electron microscopy of thin sections of viruliferous hoppers (see Relations with Cells and Tissues). These viruses are usually not transmitted, or are transmitted very infrequently through leafhopper eggs, though Chang (1977) suggested that FDV may be transmitted through up to 17% of vector eggs. Harpaz (1972) found that the longevity of hoppers carrying MRDV was little affected but, compared with uninfected hoppers, they laid 30-50% fewer eggs, of poorer viability. Hoppers carrying RRSV lay fewer eggs, though the longevity, both of males and of females, seems unaffected (Zhou et al., 1982).

Ecology

The ecology of WTV is unknown, that of the other group members has been reviewed by Harpaz (1972), Milne & Lovisolo (1977), Maramorosch & Harris (1979), Conti (1981, 1983, 1984) and Shikata (1981). Except in vegetatively propagated crops such as pangola grass or sugarcane, infection requires inoculation by viruliferous hoppers. High frequencies of egg transmission with subgroup 1 viruses may help to maintain virus levels in vector populations, but with viruses of subgroups 2 and 3 such transmission seems insignificant, except possibly with FDV (see previous section). In the humid tropics and subtropics, the crops, viruses and vectors are continuously present, and infection cycles are difficult to break. Breeding tolerant or resistant crops may be effective, although such resistance is likely to be broken within 5 or 6 years in any one variety (Swaminathan, 1982). In temperate countries, the viruses may overwinter in viruliferous hoppers in diapause, as with RDV in Japan (Kisimoto, 1969; Shikata, 1981) and MRDV in Italy (Conti, 1983, 1984). Neither of these viruses seems to overwinter in perennial weed hosts. In contrast, RBSDV in Japan overwinters in weed hosts to a greater extent than in diapausing nymphs (Shikata, 1981). In Scandinavia, both OSDV and the CTDV strain of MRDV overwinter in diapausing hoppers and in autumn-sown cereals and leys (Lindsten, 1974). In spring, hopper migrations often coincide with the presence of young crops just emerging and at their most susceptible stage. Thus, revision of autumn sowing practices, weed hygiene, insecticide treatment and careful timing of spring sowing can often reduce virus incidence to tolerable levels.

Relations with Cells and Tissues

With one exception, plant reoviruses are restricted to neoplastic tissues derived from the phloem (Milne & Lovisolo, 1977; Shikata, 1977; Omura et al., 1982; Franeki & Boccardo, 1983; Francki et al., 1985), though occasionally tracheids may also be involved (Appiano & Lovisolo, 1979; Hatta & Francki, 1981; Hatta, Boccardo & Francki, 1982). The exception is RDV, which does not cause hyperplasia, and invades mesophyll cells adjacent to the veins as well as vascular tissue (Shikata, 1977, 1981). WTV-induced tumours can continue growth for long periods (Descr. 34) whereas those induced by other group members cease growth after a short time (Hatta & Francki, 1981; Hatta et al., 1982), probably because there is no secondary meristematic system in the Gramineae.

The cytopathology of infected plants has been extensively studied by light and electron microscopy (see reviews by Shikata, 1977, 1981; Milne & Lovisolo, 1977; Francki & Boccardo, 1983; Francki et al., 1985). In thin sections, RRSV particles have a mean diameter of about 63 nm whereas other members of the group have particles about 70 nm in diameter. All particles have a more densely stained core about 45 nm in diameter, containing the RNA. They are found only in the cytoplasm, sometimes in crystalline arrays or within tubular structures.

Infected cells contain ‘viroplasms’ which are about the size of the nucleus, are not membrane-bounded, and, at least with viruses of subgroups 2 and 3, contain zones of differing appearance. The less strongly stained regions consist largely of kinked filaments (Dales, Gomatos & Hsu, 1965) with diameters of 7 nm in thin sections and 13 nm when freeze-etched and shadowed. In negative stain, the same structures are 8 nm wide but coiled tightly to give an apparent diameter of 13 nm. The more densely stained regions of the viroplasms contain filaments and also nascent inner viral shells, some containing RNA.

With the apparent exception of FDV-infected sugarcane and RRSV-infected rice, both insect and plant cells infected with viruses of the group contain tubules about 100 nm in diameter. These may contain virus particles and may be incompletely closed, forming scrolls. With MRDV, the tubules consist of protein apparently serologically unrelated to virus particle antigens. In transverse sections, the tubule walls appear three-layered. In negative stain they exhibit a square lattice repeating every 4 nm. MRDV and OSDV infections may provoke cell wall proliferation, and lysosomal activity has been detected in MRDV-infected cells. MRDV-induced enations contain less Ca and Si but more P, K and S than surrounding tissue.

In infected insect hosts, most tissues are invaded but tumours are not induced. Otherwise, the cytopathology is similar to that found in plants (Vidano, 1970; Shikata, 1977; Shikata & Kitagawa, 1977; Hibino, 1979; Hibino, Saleh & Roechan, 1979; Maramorosch & Harris, 1979).

Particle Properties

The particles contain segmented double-stranded RNA within isometric protein shells 45-50 nm in diameter, which are in turn enclosed in a second protein shell of diameter 65-70 nm. RRSV seems to be exceptional in having an incomplete outer shell. Sedimentation coefficients, s°20,w, are reported as 514 S (WTV), 510 S (RDV) and 400 S (MRDV subviral particles) (Shikata, 1981).

Subgroup 1. The particles are 65-70 nm in diameter in neutral phosphotungstate or in uranyl acetate negative stain, with obvious fine structure but no external spikes. The particles of WTV, RGDV and probably RDV possess, externally to the outer shell, a thin amorphous protein layer easily lost during purification (Reddy & MacLeod, 1976; Omura et al., 1982; Uyeda & Shikata, 1982). The inner shell shows no fine structure. The structure of the outer shell is uncertain; Kimura & Shikata (1968) and Black (Descr. 34) suggested a T=3 structure of 32 morphological subunits whereas Bils & Hall (1962) and Streissle & Granados (1968) favoured a T=9 structure of 92 morphological subunits. Uyeda & Shikata (1982) have plausibly proposed a model with 180 subunits surrounding 92 holes.

The protein coat of WTV contains seven polypeptide species of M. Wt 160-35 kd (I-VII). Peptides II and IV probably form the external amorphous layer, VI and VII the outer shell, and I, III and V the inner shell (Reddy & MacLeod, 1976). Results with RDV are similar (Nakata, Fukunaga & Suzuki, 1978). The inner shell of WTV contains an RNA-dependent RNA polymerase which transcribes all 12 segments (Reddy et al., 1977), and a RNA guanylyltransferase, a guanine-7-methyltransferase and a RNA 2'-O-methyltransferase which modify the 5' termini of the transcripts (Rhodes et al., 1977). Each transcript anneals specifically with one genome segment (Nuss & Peterson, 1980, 1981a). These enzymes are still found in WTV isolates propagated for extended periods in the absence of the vector (Nuss & Peterson, 1981b). An RNA polymerase has also been detected in the particles of RDV (Kodama & Suzuki, 1973) and RGDV (Yokoyama et al., 1984).

Subgroup 2. The intact particles of these viruses easily break down to form subviral particles. The intact particles are double-shelled icosahedra 65-70 nm in diameter, with a spike or knob (A spike) at each 5-fold vertex. The outer shell is about 8 nm thick, consisting probably of 92 morphological subunits of two types, B and C. The B subunits occur at the 5-fold vertices; each is a pentamer with a central hole, and is capped in the intact particle by an A spike. Where the A spike is missing, the viral RNA may protrude through the hole. B subunits are relatively resistant to removal, though the A spikes are labile. The C subunits, composing the rest of the outer shell, are easily stripped off by ageing or by treatment with chloroform to reveal the inner shell (the subviral particle) bearing the B subunits now standing out as B spikes. Each B spike rests on a base plate that forms part of the inner shell. The B spikes can be removed with 0.2 M salts, n-butanol or neutral PTA (Milne & Lovisolo, 1977; Shikata, 1981; Francki et al., 1985). The intact particles of subgroup 2 viruses are more labile than those of subgroup 1 and are disrupted in neutral PTA; only those of MRDV and FDV have been purified. The subviral particles are relatively stable and easier to prepare.

Six polypeptides (M. Wt 139-64 kd, I-VI) have been detected in the intact particles of MRDV; peptides I, II and III were found in the B-spiked subviral particles and I and II in the inner shell (Boccardo & Milne, 1975). B-spiked subviral particles of FDV contain three peptides, two of which may correspond with peptides I and II of MRDV, though the third seems much smaller than MRDV peptide III (van der Lubbe, Hatta & Francki, 1979). No enzyme activities have been detected in purified preparations of subgroup 2 viruses, but FDV-infected sugarcane extracts have shown some RNA-dependent RNA polymerase activity (Ikegami & Francki, 1976).

Subgroup 3. The particles resemble the B-spiked subviral particles of subgroup 2 viruses except that the B spikes are broader at the base. If a particle resembling the subgroup 2 intact particle exists, it must be rare or highly labile because no such particle has been demonstrated in negative-stain preparations even after fixation. In thin sections, most particles have a B-spiked morphology but some images from infected insect tissue may represent intact particles (Hibino et al., 1977; Milne, 1980; Descr. 248).

Genome Properties

The double-stranded RNA is in 12 segments (subgroup 1) or 10 segments (subgroups 2 and 3). Where the double-stranded RNA molecules of different viruses have been compared by coelectrophoresis, the relative M. Wt of the different numbered segments are similar within each subgroup, though the absolute values are only approximate.

Subgroup 1. The 12 segments range in size from about 3 to 0.3 Md, with a total size of about 16 Md. The segments of WTV and RDV are from 1.5 to 0.1 µm in length (Kleinschmidt et al., 1964; Fujii-Kawata, Miura & Fuke, 1970). The ribose-phosphate chains are 1.3 nm apart, with an orientation of the phosphate groups different from that in DNA (Tomita & Rich, 1964; Sato et al., 1966; Samejima et al., 1968).

Of the two RNA strands in each segment of the WTV genome one has 3'-terminal -UOH, the other -COH. The RNA polymerase within the inner shell transcribes the strands terminating in -UOH to form full-length mRNA molecules which become methylated at their 5' ends with the blocked structure 7mG(5')ppp(5')Amp. The RNA 2'-O-methyltransferase is also within the particle (Nuss & Peterson, 1981b; Francki & Boccardo, 1983). Each segment produces one mRNA which codes for one polypeptide that is not further processed (Nuss & Peterson, 1980). Of the 12 translation products, seven have been identified as particle proteins (Nuss & Peterson, 1981a). When WTV or RDV are propagated for long periods in plants or insect cell monolayers, genome deletions may occur. The RNA segments of 16 such WTV deletion mutants have been analysed (Reddy & Black, 1977).

Subgroup 2. The 10 segments range in size from about 2.6 to 1.0 Md, with a total size of about 17 Md. The products of the RNA polymerase present in FDV-infected sugarcane extracts anneal to FDV RNA but have not been further characterised (Ikegami & Francki, 1976).

Subgroup 3. The 10 segments of the RRSV genome range in size from about 2.5 to 0.5 Md, with a total size of about 16 Md (Boccardo et al., 1985; Omura et al., 1984).

Replication

Occurs in the cytoplasm. The viroplasms are the sites of virus synthesis, in both plant and insect cells. The RNA and the inner shell are assembled within the viroplasm, and the outer shell is probably acquired as the subviral particle emerges from the viroplasm into the cytoplasm proper (see Relations with Cells and Tissues).

The mode of replication of plant reoviruses is unknown. However, by analogy with the animal reoviruses (Joklik, 1974; Luria et al., 1978; Matthews, 1982), the dsRNA is probably totally conserved inside the inner shell during replication, the plus strand ssRNA synthesised upon this template escaping via the hollow B spikes.

Relationships within the Taxon

The viruses in subgroups 1 and 2 differ in the number of genome parts, particle structure, reactivity to various physical and chemical agents, and type of vector. RRSV does not fit well into either subgroup and is here assigned to a third subgroup which is nearer to subgroup 2 than subgroup 1. The serology of the group is complicated by the presence in some antisera of antibodies of low titre reacting non-specifically with dsRNA. The protein moieties of the particles are, however, good specific immunogens. No serological cross-reactions have been found between members in different subgroups.

Subgroup 1. WTV, RDV and RGDV are serologically unrelated to one another (Descr. 34; Descr. 102; Omura et al., 1980, 1982). The sizes of the various genome segments differ considerably between WTV, RDV and RGDV, and the host ranges and symptoms also distinguish the three viruses clearly.

Subgroup 2. Serology of the B-spiked subviral particles differentiates the subgroup into three unrelated clusters. These are (i), FDV; (ii), MRDV, PaSV and RBSDV, plus CTDV and MRCV, which are considered geographical races of MRDV; (iii), OSDV and serologically indistinguishable isolates previously described under the names ABDV and LEV (Table 1) (Luisoni et al., 1979; Shikata, 1981; Francki & Boccardo, 1983; Francki et al., 1985). Only low-titred antisera against the C subunits and the A spikes of the outer shell of fijiviruses were obtained by immunisation with unfixed or glutaraldehyde-fixed intact particles. However, good antisera to these components of MRDV were obtained by injecting rabbits with intact particles fixed in dithiobis(succinimidyl)propionate, and tests with these antisera confirm the relationships found earlier with antibodies directed against the B-spiked subviral particles (Boccardo et al., 1980; Boccardo & Milne, 1981). The electrophoretic patterns of the RNA species of the fijiviruses support the relationships detected by serology.

Some taxonomic points remain unsettled within the MRDV cluster. For historical and geographical reasons, RBSDV and PaSV have been considered distinct from MRDV but serologically their subviral particles are very similar, and the electrophoretic mobilities of their genome segments also differ minimally. The experimental host ranges of MRDV and RBSDV, where compared, are similar, though MRDV does not naturally infect rice whereas RBSDV naturally infects both rice and maize. These differences may partly result from the crop varieties used. The host range of PaSV has not been widely tested. The vectors of MRDV and RBSDV are the same; that of PaSV is different but again experimental comparisons are lacking. Although it is convenient to continue to consider RBSDV and PaSV as distinct viruses, their very close affinity to MRDV should be borne in mind. CTDV and MRCV, however, should be considered strains of MRDV.

Subgroup 3. RRSV differs significantly from the viruses in subgroups 1 and 2, in particle structure and size of genome segments. It is not serologically related to other viruses in the group.

Affinities with Other Groups

No affinities with other plant viruses. The group shares many features with reo-like viruses infecting vertebrates and invertebrates and has been placed with them in the same virus ‘family’, the Reoviridae (Matthews, 1982). Subgroup 1 viruses have particle structures rather similar to those of rotaviruses (Novo & Esparza, 1981; Palmer & Lane, 1982) and orbiviruses (Verwoerd, Huismans & Erasmus, 1979). The B-spiked subviral particles of subgroup 2 viruses (especially where the A spikes are retained) resemble the particles of insect cytoplasmic polyhedrosis viruses (Wood, 1973; Milne & Lovisolo, 1977; Payne & Harrap, 1977; Hatta & Francki, 1982).

Notes

Several plant diseases that resemble those caused by plant reoviruses (stunting, and swelling of leaf veins) are induced by hopper salivary toxins (Carter, 1973; Milne & Lovisolo, 1977). An example is the East African sugarcane gall or pseudo-Fiji disease (Antoine, 1959; Sheffield, 1968). Maize wallaby ear disease may also carry a reo-like virus that has been mistaken for the causal agent. This virus morphologically resembles plant reoviruses of subgroup 2 but does not replicate in plant tissues (Grylls, 1975; Boccardo et al., 1980; Ofori & Francki, 1983). Red clover rugose leaf curl disease may be a similar case (Grylls et al., 1974) though there is also evidence for the involvement of rickettsia-like organisms (Behncken & Gowanlock, 1976). Corn white leaf disease (Trujillo, Acosta & Pinero, 1974) may be caused by a toxin or a reo-like virus. Vein swellings induced by insect toxaemias appear to result from enlargement of parenchyma cells, as opposed to division of cells in the phloem (Antoine, 1959; Hatta et al., 1982).

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