Tomato black ring virus
A. F. Murant
Scottish Horticultural Research Institute, Invergowrie, Dundee, Scotland
- Described by Smith (1946).
- Selected synonyms
- Buschbohnenringflecken-Virus = bean ringspot virus (Rev. appl. Mycol.
35: 411; 42: 457)
- Lettuce ringspot virus (Rev. appl. Mycol. 39: 142)
- Kartoffelbukett-Virus = potato bouquet virus (Rev. appl. Mycol.
32: 274; 37: 463)
- (For names of other more serologically distinctive isolates see also under
- A RNA-containing virus which has isometric particles about 30 nm in diameter
and occurs in Europe. It is readily sap-transmissible, has a wide host range,
infects the seed of many host plants, and is transmitted in soils by nematodes (Longidorus spp.).
In addition to black ring of tomato, the various strains of this virus cause
ringspot diseases of bean, sugar beet, lettuce, raspberry and strawberry, yellow
vein of celery, bouquet and pseudo-aucuba of potato, shoot-stunting of peach,
one type of mosaic of Robinia pseudoacacia
and unnamed diseases of leek and
onion. It occurs in many other plants, including cabbage, grapevine, lucerne and
Not reported outside Europe.
Host Range and Symptomatology
Host range is wide: infects naturally many species of wild and cultivated
monocotyledonous and dicotyledonous plants. An isolate from Robinia
infected 76 species in 29 dicotyledonous families after mechanical
inoculation (Schmelzer, 1963
It is reported to infect the roots of the gymnosperm,
. Nearly all commonly used herbaceous test plants are
- Diagnostic species
- Chenopodium amaranticolor and C. quinoa. Chlorotic or necrotic
local lesions (Fig.1); systemic necrosis or chlorotic mottle (Fig.2).
- Nicotiana rustica and N. tabacum cvs. White Burley or Xanthi-nc
(tobacco). Local chlorotic or necrotic spots or rings (Fig.3); systemic spots,
rings and line patterns with variable amounts of necrosis (Fig.4). Leaves produced
later appear normal but contain virus.
- Phaseolus vulgaris cv. The Prince (French bean). In winter in the U.K.,
dark brown local lesions c. 2 mm in diameter (Fig.5), in summer chlorotic
lesions or none; systemic chlorotic mottle with variable amounts of necrosis and
- Petunia hybrida. Chlorotic local lesions sometimes with brown necrotic
margins; systemic veinal chlorosis or necrosis. Leaves produced subsequently are
symptomless but contain virus.
- Propagation species
- Nicotiana rustica is a suitable plant for maintaining cultures; N. clevelandii and
Petunia hybrida are good sources of virus for purification.
- Assay species
- Chenopodium amaranticolor is the most reliable local-lesion host. C.
quinoa, Cucumis sativus (cucumber) and Brassica rapa (turnip) are
convenient bait plants in nematode transmission experiments.
The best known strains are:
Tomato black ring strain (Smith, 1946). The type strain.
Lettuce ringspot strain (Smith & Short, 1959).
Potato bouquet strain of Köhler, Rev. appl. Mycol. 32: 274
Potato pseudo -aucuba strain of Köhler, Rev. appl. Mycol. 35:
481 (Bercks, 1962).
Beet ringspot strain (Harrison, 1957).
Celery yellow vein strain (Hollings, 1965).
These strains probably cannot be reliably distinguished by symptoms on host
plants but differ in their serological and vector relationships.
Transmission by Vectors
Vectors are free-living soil-inhabiting nematodes of the genus Longidorus
Strains serologically similar to the type strain are transmitted most efficiently
by L. attenuatus
, those more closely related to the beet ringspot strain by
(Harrison, Mowat & Taylor, 1961
; Harrison, 1964
& Murant, 1969
). Larvae and adults of L. elongatus
both transmit, but
the adult does not pass the virus to its progeny, nor is the virus retained when
the nematode moults. L. elongatus
kept in fallow soil retains infectivity
up to about 9 weeks. Virus-like particles seem adsorbed to the stylet guiding
sheath of L. elongatus
which have fed on plants infected with tomato black
ring virus (Taylor & Robertson, 1969
Transmission through Seed
Reported in at least twenty-four spp. in fifteen botanical families. In many
hosts more than 10%, and in some 100%, of progeny seedlings are infected. Many
plants infected through the seed show no symptoms. Virus was transmitted to seed
of raspberry and strawberry from either male or female parent, but plants
pollinated with virus-carrying pollen did not become infected (Lister &
). Besides aiding dissemination of the virus, infection of the seed
seems to provide an important means of survival of the virus in soils (Murant
& Lister, 1967
Transmission by Dodder
Nine species of Cuscuta
failed to transmit the potato bouquet strain
Strongly immunogenic in rabbits; antisera with titres of 1/500 are easily
obtained. Precipitin tests in tubes, droplets or 1% agar gel give satisfactory
results. The virus gives one line of precipitate in gel-diffusion tests. The
celery yellow vein strain is unusual in eliciting no antibodies in rabbits
unless virus treated with 0.2% formaldehyde is used as immunogen (Hollings &
There is much antigenic variation between strains. Most antisera place the
strains into two groups; one contains the type, lettuce ringspot and potato bouquet
strains; the other contains the beet ringspot and potato pseudo-aucuba strains
; Bercks, 1962
); the celery yellow vein strain seems intermediate
Plant-protection may not be complete, even between strains that are closely
serologically related, and is frequently only partial or non-reciprocal in
tests between distantly related strains.
Tomato black ring virus shares many properties with other nepoviruses (arabis
mosaic, grapevine fanleaf, raspberry ringspot, strawberry latent ringspot, tobacco
ringspot and tomato ringspot) but is unrelated to them serologically.
Stability in Sap
In tobacco sap, the virus usually loses infectivity after 10 min at 60-65°C
storage at room temperature for 2-3 weeks, or dilution to
. The lesion number decreases with dilution by
more than the dilution factor (Harrison, 1957
A modification of Steeres butanol/chloroform method is useful (Harrison
& Nixon, 1960
Properties of Particles
The particles are all the same size but sediment as three components (Fig.6
empty protein shells (T) and two kinds of nucleoprotein with different amounts
of RNA (M and B).
Sedimentation coefficients (s20,w) at infinite
dilution (svedbergs): 55(T), 97(M), 121(B).
Other physical properties not
Isometric, about 30 nm in diameter with a 5- or 6-sided angular outline
(Harrison & Nixon, 1960
). Electron micrographs show particles some completely,
some partially and some not penetrated by negative stain (Fig.7
particles possibly correspond to the T, M and B components. Detailed structure
of the particle not known.
RNA about 28% (M) and 38% (B) of the particle weight (estimated from the
Relations with Cells and Tissues
Plants infected with tomato black ring virus are patchily distributed in crops
because of the slow migration of the soil-inhabiting vectors, Longidorus
spp. Some strains tend to occur in soils together with strains of raspberry
because they share the vector, L. elongatus
. These two
viruses are serologically unrelated; they can be distinguished from each other
by their reactions in Chenopodium amaranticolor
. In general, however, these
and other unrelated viruses of the nepovirus
group cannot be reliably identified
by host range or symptomatology; serological tests are essential.
- Bercks, Phytopath. Z. 46: 97, 1962.
- Harrison, Ann. appl. Biol. 45: 462, 1957.
- Harrison, J. gen. Microbiol. 18: 450, 1958.
- Harrison, Virology 22: 544, 1964.
- Harrison, Mowat & Taylor, Virology 14: 480, 1961.
- Harrison & Nixon, Virology 12: 104, 1960.
- Hollings, Ann. appl. Biol. 55: 459, 1965.
- Hollings & Stone, Nature, Lond. 194: 607, 1962.
- Lister & Murant, Ann. appl. Biol. 59: 49, 1967.
- Murant & Lister, Ann. appl. Biol. 59: 63, 1967.
- Schmelzer, Phytopath. Z. 28: 1, 1956.
- Smith, Parasitology 37: 126, 1946.
- Smith & Short, Pl. Path. 8: 54, 1959.
- Taylor & Murant, Ann. appl. Biol. 64: 43, 1969.
- Taylor & Robertson, Ann. appl. Biol. 64: 233, 1969.
- Schmelzer, Phytopath. Z. 46: 235, 1963.
Local lesions in Chenopodium amaranticolor.
Systemic necrosis in C. quinoa.
Local necrotic rings and spots in Nicotiana tabacum, cv. White
Systemic symptoms in N. tabacum cv. Xanthi-nc.
Local lesions in Phaseolus vulgaris cv. The Prince.
Schlieren diagram of a sedimentation analysis of a partially purified
preparation, showing three virus components (T, M and B). The other components
were probably derived from the N. clevelandii host tissue.
Virus particles from a purified preparation showing some particles
completely, some partially and some not penetrated by phosphotungstate. Bar
represents 50 nm.