B. D. Harrison
Scottish Horticultural Research Institute, Invergowrie, Dundee, Scotland
A. F. Murant
Scottish Horticultural Research Institute, Invergowrie, Dundee, Scotland
Tobacco ringspot virus
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
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
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.
Definitive and tentative members of the nepovirus group with some of
their properties are:
No. or ref.
|A. DEFINITIVE MEMBERS
|Tomato black ring (TBRV) sub-group
| TBRV, potato bouquet strain
| TBRV, beet ringspot strain
| Cocoa necrosis (CNV)
||54, 101, 129
| Grapevine chrome mosaic (GCMV)
||- , 92, 117
| Myrobalan latent ringspot (MLRV)
||- , 105, 115
Artichoke Italian latent (AILV)
||55, 96, 121
Mulberry ringspot (MRV)
||50, 96, 126
Raspberry ringspot (RRV) sub-group
| RRV, type strain
||50, 91, 125
| RRV, English strain
Tobacco ringspot (TobRV) sub-group
| TobRV, type strain
||53, 91, 126
| TobRV, eucharis mottle strain
||-, -, -
| Potato black ringspot (PBRV)
||49, 88, 117
Arabis mosaic (AMV) sub-group
| AMV, type strain
||53, 93, 126
| Grapevine fanleaf (GFLV)
||50, 86, 120
Tomato ringspot (TomRV)
||53, 119, 127
|Peach rosette mosaic (PRMV)
||52, 115, 134
|Cherry leaf roll (CLRV)
|-, 115, 128
B. TENTATIVE MEMBERS
|Strawberry latent ringspot (SLRV)
|58, -, 126
|Cherry rasp leaf (CRLV)
||56, 96, 128
|Tomato top necrosis (TTNV)
||52, 102, 126
|Grapevine Bulgarian latent (GBLV)
||52, 120, 127
*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
Association with Vectors
Transmitted by free-living ectoparasitic, soil-inhabiting nematodes (species
and Xiphinema, Table 1
; Lamberti, Taylor &
) which feed on plant roots. After acquiring virus, the nematodes
retain ability to transmit for several weeks (Longidorus
spp.) or months
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
; Taylor, Robertson & Roca, 1976
) or, by
contrast, the cuticular lining of the oesophagus (AMV, GFLV, TobRV; Taylor &
; 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).
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 &
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 &
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),
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).
Definitive nepoviruses have coat polypeptides of c.
55,000 M. Wt,
larger than those of other small isometric plant viruses. The protein shells are
= 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).
RNA-1 and RNA-2 are both needed to produce infection (Harrison, Murant &
; 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
). 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.,
; Hanada & Harrison, 1977
; Harrison & Murant, 1977
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
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
et al., 1976
Relationships within the Taxon
Sub-groups based on serological relationships are indicated in
Quacquarelli et al. (1976b
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
(BBWV) and the comoviruses
(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.
- Bancroft, Phytopathology 58: 1360, 1968.
- Barker & Harrison, J. gen. Virol. 35: 125, 1977.
- Clark, J. gen. Virol. 32: 331, 1976.
- Crowley, Davison, Francki & Owusu, Virology 39: 322, 1969.
- Delbos, Dunez, Barrau & Fisac, Annls Microbiol. (Inst. Pasteur) 127A: 101, 1976.
- De Zoeten & Gaard, J. Cell. Biol. 40: 814, 1969.
- Diener & Schneider, Virology 29: 100, 1966.
- Gerola, Bassi & Betto, Caryologia 18: 353, 1965.
- Hanada & Harrison, Ann. appl. Biol. 85: 79, 1977.
- Harrison, Virology 22: 544, 1964.
- Harrison, A. Rev. Phytopath. 15: 331, 1977.
- Harrison & Murant, Ann. appl. Biol. 86: 209, 1977.
- Harrison, Murant & Mayo, J. gen. Virol. 16: 339, 1972a.
- Harrison, Murant & Mayo, J. gen. Virol. 17: 137, 1972b.
- Harrison, Murant, Mayo & Roberts, J. gen. Virol. 22: 233, 1974.
- Lamberti, Taylor & Seinhorst (eds.), Nematode Vectors of Plant Viruses, London & New York: Plenum, 460 pp., 1975.
- Lister & Murant, Ann. appl. Biol. 59: 49, 1967.
- McGuire, Kim & Douthit, Virology 42: 212, 1970.
- Martelli, in Nematode Vectors of Plant Viruses, p. 223, ed. Lamberti, Taylor & Seinhorst, London & New York: Plenum, 1975.
- Martelli, Gallitelli, Abracheva, Savino & Quacquarelli, Ann. appl. Biol. 85: 51, 1977.
- Mayo, Murant & Harrison, J. gen. Virol. 12: 175, 1971.
- Mayo, Harrison, Murant & Barker, J. gen. Virol. 19: 155, 1973.
- Murant, Outlook on Agriculture 6: 114, 1970.
- Murant & Lister, Ann. appl. Biol. 59: 63, 1967.
- Murant & Taylor, Ann. appl. Biol. 55: 227, 1965.
- Murant, Mayo, Harrison & Goold, J. gen. Virol. 19: 275, 1973.
- Peden, May & Symons, Virology 47: 498, 1972.
- Peña-Iglesias & Rubio-Huertos, Microbiol. Española 24: 183, 1971.
- Quacquarelli, Gallitelli, Savino & Martelli, J. gen. Virol. 32: 349, 1976a.
- Quacquarelli, Gallitelli, Savino, Piazzola & Martelli, Abstr. Proc. 6th Conf. Internatl. Counc. Grapevine Viruses Cordova 1976: 10, 1976b.
- Randles, Harrison, Murant & Mayo, J. gen. Virol. 36: 187, 1977.
- Rezaian & Francki, Virology 56: 238, 1973.
- Rezaian & Francki, Virology 59: 275, 1974.
- Rezaian, Francki, Chu & Hatta, Virology 74: 481, 1976.
- Salazar, Ph.D. Thesis, Univ. of Dundee, 1977.
- Saric & Wrischer, Phytopath. Z. 84: 97, 1975.
- Schneider, Virology 45: 108, 1971.
- Schneider, Hull & Markham, Virology 47: 320, 1972.
- Taylor & Murant, Ann. appl. Biol. 64: 43, 1969.
- Taylor & Robertson, Ann. appl. Biol. 64: 233, 1969.
- Taylor & Robertson, Ann. appl. Biol. 66: 375, 1970.
- Taylor & Robertson, Rep. Scott. hort. Res. Inst., 1972: 77, 1973.
- Taylor, Robertson & Roca, Nematol. Mediterranea 4: 23, 1976.
- Taylor & Stubbs, CMI/AAB Descriptions of Plant Viruses 81, 4pp., 1972.
- Tsuchizaki, Hibino & Saito, Ann. phytopath. Soc. Japan 37: 266, 1971.
- Walkey & Webb, J. gen. Virol. 3: 311, 1968.