185
September 1977
Family: Secoviridae
Genus: Nepovirus
Species:
Acronym:


Nepovirus group

B. D. Harrison
Scottish Horticultural Research Institute, Invergowrie, Dundee, Scotland

A. F. Murant
Scottish Horticultural Research Institute, Invergowrie, Dundee, Scotland

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

Tobacco ringspot virus

Main Characteristics

Three types of isometric particle c. 28 nm in diameter with angular outlines, sedimenting at c. 50, 90-120 and 120-130 S and containing respectively c. 0, 27-40 and 42-46% single-stranded RNA. Two RNA species, M. Wt c. 2.4 x 106 and 1.4-2.2 x 106, both necessary for infection. Each particle contains 60 molecules of a single coat polypeptide, M. Wt c. 55,000. Thermal inactivation point 55-70°C; longevity in sap a few days or weeks; concentration in sap 10-50 mg/l. Wide host range, causing ringspot and mottle symptoms, often with subsequent symptomless infection. Virus particles occur in cytoplasm, some in membraneous tubules. Many cells contain a vesiculated cytoplasmic inclusion body. Transmissible by inoculation of sap, by soil-inhabiting nematodes and to progeny through seed and pollen.

Members

Definitive and tentative members of the nepovirus group with some of their properties are:

Virus Description
No. or ref.
Main natural
vector(s)
Sedimentation
coefficients
(Svedbergs)
Approx.
RNA M.Wt
(x 10-6)*
        1 2
A. DEFINITIVE MEMBERS          
Tomato black ring (TBRV) sub-group ‡          
     TBRV, potato bouquet strain 38 L. attenuatus 55, 97,121 2.5 1.5
     TBRV, beet ringspot strain 38 L. elongatus
     Cocoa necrosis (CNV) 173 unknown 54, 101, 129 - -
     Grapevine chrome mosaic (GCMV) 103 unknown - , 92, 117 - -
     Myrobalan latent ringspot (MLRV) 160 unknown - , 105, 115 2.6 1.9
 
Artichoke Italian latent (AILV)
176 L. apulus 55, 96, 121 2.4 1.5
 
Mulberry ringspot (MRV)
142 L. martini 50, 96, 126 - -
 
Raspberry ringspot (RRV) sub-group
         
     RRV, type strain 6, 198 L. elongatus 50, 91, 125 2.4 1.4
     RRV, English strain 6, 198 L. macrosoma
 
Tobacco ringspot (TobRV) sub-group
         
     TobRV, type strain 17, 309 X. americanum 53, 91, 126 2.4 1.4
     TobRV, eucharis mottle strain 17, 309 unknown -, -, - 2.4 1.4
     Potato black ringspot (PBRV) (a), 206 unknown 49, 88, 117 2.5 1.5
 
Arabis mosaic (AMV) sub-group
         
     AMV, type strain 16 X. diversicaudatum 53, 93, 126 2.4 1.4
     Grapevine fanleaf (GFLV) 28 X. index 50, 86, 120 2.4 1.4
 
Tomato ringspot (TomRV)
18, 290 X. americanum 53, 119, 127 2.3 c.2.2
Peach rosette mosaic (PRMV) 150, 364 X. americanum 52, 115, 134 - -
Cherry leaf roll (CLRV) 80, 306 X. diversicaudatum,
X. coxi
-, 115, 128 2.4 2.1
 
B. TENTATIVE MEMBERS
Strawberry latent ringspot (SLRV) 126 X. diversicaudatum,
X. coxi
58, -, 126 2.6 1.6
Cherry rasp leaf (CRLV) 159 X. americanum 56, 96, 128 2.0 1.5
Tomato top necrosis (TTNV) (b) unknown 52, 102, 126 - -
Grapevine Bulgarian latent (GBLV) (c), 186 unknown 52, 120, 127 2.2 2.1

*From determinations made by electrophoresis in polyacrylamide gels under non-denaturing conditions
‡Sub-groups contain viruses that are serologically related
(a) Salazar, 1977
(b) Bancroft, 1968
(c) Martelli et al., 1977

Geographical Distribution etc

Individual nepoviruses tend to have a restricted distribution determined by that of the natural vector, but as a group they have been reported from most parts of the world. They have also been disseminated widely in infected seed and planting material.

Association with Vectors

Transmitted by free-living ectoparasitic, soil-inhabiting nematodes (species of Longidorus and Xiphinema, Table 1; Lamberti, Taylor & Seinhorst, 1975) which feed on plant roots. After acquiring virus, the nematodes retain ability to transmit for several weeks (Longidorus spp.) or months (Xiphinema spp.) but cease to transmit after moulting. The viruses do not multiply in their vectors and there is no transmission of virus through the egg. Virus particles are associated with specific sites in the anterior alimentary tract: the stylet lumen or guiding sheath (RRV, TBRV and AILV; Taylor & Robertson, 1969, 1973; Taylor, Robertson & Roca, 1976) or, by contrast, the cuticular lining of the oesophagus (AMV, GFLV, TobRV; Taylor & Robertson, 1970; McGuire, Kim & Douthit, 1970).

The specificity of association between nepoviruses and their vectors seems dependent on the properties of the particle protein (Harrison, 1964; Taylor & Murant, 1969; Harrison et al., 1974; Harrison & Murant, 1977).

Only one nepovirus, TobRV, has been reported also to spread aerially, and various arthropods including species of aphid, flea-beetle, grasshopper, thrips and spider mite are reported to transmit it (Desc. 17).

Ecology

Diseases caused by nepoviruses typically occur in patches in fields, reflecting the horizontal distribution of nematode vectors in the soil. The nematodes migrate slowly through soils and, unlike aerial vectors, can only carry viruses into crops from sources that are immediately adjacent. Dissemination of the viruses occurs in infected planting material and in infected seed and pollen of crop and weed hosts (Murant, 1970; Harrison, 1977). In some hosts the proportion of seeds infected often exceeds 50% (Lister & Murant, 1967).

Survival in seeds is also an important means of persistence of the viruses in fields, especially with RRV and TBRV (Murant & Taylor, 1965); soil from outbreaks of RRV and TBRV commonly contains many infected weed seeds (Murant & Lister, 1967).

Relations with Cells and Tissues

The nepoviruses invade all parts of infected plants, including the seed and pollen and apical meristems. Newly invaded tissue commonly shows a severe ‘shock’ reaction but in leaves produced subsequently the symptoms are less severe or absent; the plant is then said to have ‘recovered’, although the virus is still present. Perennial plants may show this sequence of symptoms each year. Many plants infected through seed are symptomless, i.e. in the ‘recovered’ condition (Lister & Murant, 1967; Hanada & Harrison, 1977).

Many nepoviruses (AMV, CLRV, GFLV, SLRV and RRV; Harrison et al., 1974) induce vesiculated membraneous inclusion bodies, containing ribosomes, to form in the cytoplasm of infected cells, often close to the nucleus. Particles of CLRV, SLRV (Walkey & Webb, 1968), TobRV (Crowley et al., 1969), TomRV (de Zoeten & Gaard, 1969), GFLV (Peña-Iglesias & Rubio-Huertos, 1971; Saric & Wrischer, 1975), MRV (Tsuchizaki, Hibino & Saito, 1971) and RRV (B. D. Harrison & I. M. Roberts, unpublished data) occur inside membraneous tubules, which may pass through cell wall projections developing from the plasmodesmata. With SLRV, the tubules are double-walled and also occur in the inclusion bodies. Particles of AMV occur in spherical aggregates in the cytoplasm (Gerola, Bassi & Betto, 1965).

Particle Properties

Definitive nepoviruses have coat polypeptides of c. 55,000 M. Wt, larger than those of other small isometric plant viruses. The protein shells are probably T= 1 icosahedral structures containing 60 of these molecules (Mayo, Murant & Harrison, 1971). In most nepoviruses, the protein subunits form stable ‘top’ components lacking RNA, suggesting that the particles are mainly stabilized by protein-protein bonds. In some nepoviruses, however, the ‘top’ component is absent or is easily destroyed during purification procedures, suggesting that the RNA, of these viruses at least, may play some part in stabilizing the particles.

Nepoviruses contain single-stranded RNA. All have two essential RNA molecules, RNA-1 with M. Wt c. 2.4 x 106, and RNA-2, ranging in M. Wt from 1.4 x 106 to 2.2 x 106 (Table 1). Particles containing RNA-1 (‘bottom’ component) have sedimentation coefficients of c. 120-130 S. Particles containing RNA-2 (‘middle’ component) sediment at c. 90-120 S depending on the RNA M. Wt (Table 1). Viruses with RNA-2 of M. Wt only 1.4 x 106 also produce a second type of bottom component particle containing two molecules of RNA-2 (Diener & Schneider, 1966; Mayo et al., 1973).

Top, middle and bottom components of AMV and SLRV differ somewhat in electrophoretic behaviour (Clark, 1976).

Genome Properties

RNA-1 and RNA-2 are both needed to produce infection (Harrison, Murant & Mayo, 1972a; Quacquarelli et al., 1976a; Randles et al., 1977). In TobRV little if any of the nucleotide sequence in one RNA species also occurs in the other (Rezaian & Francki, 1974). Pseudo-recombinant isolates (RRV, TBRV) can be produced by taking RNA-1 from one strain of a virus and RNA-2 from a different but closely serologically related strain. They are produced less readily when the parent nepoviruses are distantly serologically related and not at all when they are unrelated (Harrison, Murant & Mayo, 1972b; Randles et al., 1977). In RRV and/or TBRV, RNA-1 carries determinants for host range, seed transmissibility and kind of symptom, whereas RNA-2 carries determinants for other symptom reactions, serological specificity and nematode transmissibility; virulence depends on both RNA species (Harrison et al., 1974; Hanada & Harrison, 1977; Harrison & Murant, 1977).

Replication

Apparently cytoplasmic. Synthesis of TobRV and RRV particles is inhibited by cycloheximide, not by chloramphenicol, and presumably involves cytoplasmic ribosomes (Rezaian et al., 1976; B. D. Harrison, unpublished results). Virus particle antigen accumulates in the cytoplasmic inclusion body (RRV, TBRV); this may be a major site of synthesis or assembly of virus components (Barker & Harrison, 1977). Virus-induced RNA-dependent RNA polymerase (Peden, May & Symons, 1972) is produced by TobRV at the beginning of the most rapid phase of virus nucleoprotein synthesis, when short double-stranded RNA molecules of unknown function also appear (Rezaian & Francki, 1973).

Satellites

Reported in TobRV, TBRV (beet ringspot and potato bouquet strains) and MLRV. Each satellite RNA replicates only in cells infected with its own ‘helper’ virus and is produced only when the inoculum contains it; satellite RNA molecules become packaged in shells of helper virus protein. In TobRV, the satellite RNA is of M. Wt c. 0.9 x 105 its presence in cultures affects symptom type, its synthesis predominates over that of the ‘helper’ virus RNA species, and nucleoprotein particles are produced, each containing 12-25 satellite RNA molecules (Schneider, 1971; Schneider, Hull & Markham, 1972). In TBRV and MLRV, the satellite RNA is of M. Wt c. 5 x 105, does not affect symptoms and is produced in relatively small amounts (Murant et al., 1973; Delbos et al., 1976).

Relationships within the Taxon

Sub-groups based on serological relationships are indicated in Table 1. Martelli (1975) and Quacquarelli et al. (1976b) assigned the viruses to clusters on the basis of the M. Wt of their RNA-2, as follows. (i) M. Wt 1.4-1.5 x 106, some bottom component particles containing two molecules: the RRV, TobRV and AMV sub-groups. (ii) M. Wt 1.5-1.6 x 106, one molecule per particle: TBRV, CNV, GCMV and AILV. (iii) M. Wt> 1.6 x 106, one molecule per particle: TomRV, PRMV, CLRV. Finally, the nepovirus group can be divided into two parts according to the genus of nematode vector (Table 1); this division would split the above cluster (i).

Notes on Tentative Members

SLRV produces no M component and the particles contain two polypeptide species (M. Wt 29,000 and 44,000) but the virus resembles nepoviruses in nematode and seed transmissibility, wide host range, particle stability and genome size.

CRLV has particles containing two polypeptide species (M. Wt 24,000 and 22,500) but the virus resembles nepoviruses in many other properties.

TTNV superficially resembles nepoviruses but its vector, coat polypeptide M. Wt and RNA M. Wt are not known.

GBLV has a single coat polypeptide and two RNA species of M. Wt resembling those of nepoviruses but is not known to be transmitted by nematode vectors or through seed.

Affinities with Other Groups

The viruses with closest affinities to the nepoviruses are broad bean wilt virus (BBWV) and the comoviruses. BBWV (Taylor & Stubbs, 1972) differs from nepoviruses in being transmitted by aphids, not by nematodes or through seed, and in having two coat polypeptides of M. Wt 26,000 and 42,000. Comoviruses are transmitted by beetles and probably not by nematodes. They also differ from nepoviruses in having narrower host ranges, not causing ringspot symptoms, occurring in greater concentration in sap and each having coat polypeptides of M. Wt c. 25,000 and 44,000.

References

  1. Bancroft, Phytopathology 58: 1360, 1968.
  2. Barker & Harrison, J. gen. Virol. 35: 125, 1977.
  3. Clark, J. gen. Virol. 32: 331, 1976.
  4. Crowley, Davison, Francki & Owusu, Virology 39: 322, 1969.
  5. Delbos, Dunez, Barrau & Fisac, Annls Microbiol. (Inst. Pasteur) 127A: 101, 1976.
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  7. Diener & Schneider, Virology 29: 100, 1966.
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