- Selected synonyms
- Tobacco ringspot virus no. 1 (Rev. appl. Mycol. 15:
- Annulus tabaci (Rev. appl. Mycol. 28: 514)
- Nicotiana virus 12 (Rev. appl. Mycol. 36:
- A virus with isometric particles about 28 nm in diameter sedimenting
as three components and with a bipartite RNA genome. The virus is readily
transmissible by sap inoculation and has a wide host range, including both
and herbaceous plants. It is transmitted by the nematode Xiphinema
americanum and other closely related Xiphinema spp. Reports of
natural spread are largely confined to North America but the virus has been
disseminated to many countries in infected planting material. A satellite
RNA is associated with some virus cultures.
Main DiseasesThe virus occurs in nature in both annual and perennial crops. It causes
serious disease problems in those regions of North America where the nematode
vectors also occur. If the virus is disseminated in seed or planting stock to
areas where Xiphinema spp. are absent, or present in low numbers, the
disease problem is usually negligible. Of the many diseases caused by the virus,
bud blight of soybean is the most severe and causes the greatest losses. The
most obvious symptom is curving of the terminal bud, with other buds on the
infected plant later becoming brown and brittle. Brown streaks may develop on
the stems and petioles of larger leaves, pods are underdeveloped and aborted,
and those that set before infection may develop dark blotches (Sinclair &
Shurtleff, 1975). The virus is widespread in the tobacco-growing areas of North
America, causing ring and line patterns on the foliage, dwarfing of the plant,
and small leaves of poor quality (Lucas, 1975). The virus occurs in the major
blueberry-growing region of the USA, causing blueberry necrotic ringspot
disease, in which susceptible cultivars are stunted, unproductive, show
extensive twig dieback, and necrotic or chlorotic spots, rings or line patterns
on the foliage (Converse & Ramsdell, 1982; Lister et al., 1963). The
virus causes a ringspot disease of cucurbits in Texas (McLean & Meyer, 1961)
and Wisconsin (Sinclair & Walker, 1956). Infected plants are stunted and
show a leaf mottle accompanied by leaf malformation and reduced fruit set. Other
plants that have been found naturally infected with the virus include American
spearmint (Stone et al., 1962), blackberry (Rush & Gooding, 1970),
cherry (Fig.1; Stace-Smith & Hansen, 1974), apple (Lana et al., 1983),
grapevine (Gilmer et al., 1970), pelargonium (Kemp, 1967), ash (Hibben &
Bozarth, 1972), dogwood (Waterworth & Povish, 1972), anemone (Hollings,
1965), gladiolus (Bridgmon & Walker, 1952) and elderberry (Wilkinson, 1952).
Geographical DistributionThe virus is endemic in central and eastern North America, extending from
southern Ontario in Canada to the Rio Grande Valley in Texas. Although the virus
has been isolated from cherry (Stace-Smith & Hansen, 1974) and blueberry
(Converse & Ramsdell, 1982) in western North America, the apparent absence
there of field spread suggests that infected plants were introduced as nursery
stock. Similarly, the virus has been isolated from various plant species in
other parts of the world, including gladiolus in Japan (Fukumoto et al.,
1982) and Australia (Randles & Francki, 1965), iris in the Netherlands
(Asjes, 1979), petunia (Rani et al., 1969), capsicum (Bidari &
Reddy, 1983), eggplant (Sastry & Nayudu, 1976) and soybean (Gupta, 1978) in
India, papaya in Nigeria (Lana, 1980), soybean (Murav'eva, 1976) and lupin
(Kowalska, 1971) in the USSR, tobacco in Yugoslavia (Mickovski, 1969) and
cucurbits in Iran (Ebrahim-Nesbat, 1974). As the natural vectors of the virus
occur in various parts of the world, limited natural spread may be associated
with some of the recorded occurrences outside the USA and Canada.
Host Range and SymptomatologyExperimental host range is wide; species in more than 17 dicotyledonous and
monocotyledonous families are susceptible (Price, 1940). In nature, the virus
occurs both in woody and in herbaceous plants. The virus is transmitted by
inoculation with sap, readily to herbaceous hosts but with difficulty to woody
- Diagnostic species
- Chenopodium amaranticolor and C. quinoa. Necrotic local
lesions; usually no systemic infection.
Cucumis sativus (cucumber). Chlorotic or necrotic local lesions;
systemic mottling and dwarfing with apical distortion (Fig.2).
- Nicotiana tabacum (tobacco) (Fig.3) and N. clevelandii (Fig.
4). Necrotic local lesions that frequently develop into rings or ringspots;
systemically infected leaves may show ring or line patterns. Leaves produced
later are symptomless but contain virus.
- Phaseolus vulgaris (French bean). Necrotic spots on inoculated
leaves; systemically infected leaves may show spots and rings and the growing
tip becomes necrotic.
- Lycopersicon esculentum (tomato). Difficult to infect by sap
inoculation; plants that are infected develop small necrotic spots on inoculated
leaves, systemic vein necrosis and epinasty.
- Vigna unguiculata ssp. sinensis (cowpea). Necrotic primary
lesions, systemic necrosis, apical necrosis and wilt. Cowpea cultivars may be
used to distinguish strains. Local lesions may be greatly decreased in size or
show other modifications when satellite RNA is present in the inoculum
(Schneider, 1971; Schneider et al., 1972b).
- Propagation species
- Nicotiana spp. are suitable for maintaining cultures; N.
clevelandii or cucumber are good sources of virus for purification.
- Assay species
- Nicotiana tabacum, N. clevelandii, Chenopodium amaranticolor and
Vigna unguiculata are useful for local lesion assays. Cucumber is a
useful source and bait plant for nematode transmission experiments (Fulton,
StrainsTwo viruses originating in Peru, eucharis mottle (Kahn et al., 1962)
and potato black ringspot (Salazar & Harrison, 1977) (= Andean potato calico
virus of Fribourg (1977)) are serologically related to tobacco ringspot virus.
However, the relationship is sufficiently distant for these viruses to be
considered separate entities (Gooding, 1970; Salazar & Harrison, 1978). Many
variants of tobacco ringspot virus have been reported, based primarily on
differences in symptomatology (Valleau, 1932; Hollings, 1965; Sauer, 1966; Tu,
1981). There are also many natural antigenic variants: Gooding (1970) identified
four serologically distinct isolates from tobacco and one from watermelon. No
correlation was found between a variant and its geographical origin or the type
of tobacco from which it was isolated.
Transmission by VectorsMost vector studies have been done with nematode populations identified as
Xiphinema americanum. However, X. americanum sensu lato is
now considered to be a complex of many species
(Lamberti & Bleve-Zacheo, 1979) and clarification of the vector
potential of the component species is required.
X. coxi has been reported to be a vector (van Hoof, 1971) but the
evidence supporting this claim is considered to be
inadequate (Trudgill et al., 1983).
The virus is acquired by X. americanum within 24 h. It is
transmitted by adult and larval stages. Single nematodes may infect a plant but
the frequency of infection increases with the number of nematodes (McGuire,
1964). Viruliferous nematodes could still transmit after storage at 10°C
for 49 weeks (Bergeson et al., 1964). The nematodes transmitted the virus
to 25 of 38 species tested, with 100% transmission occurring when the nematodes
were given 3 weeks access to the infected source and 10 viruliferous nematodes
were placed on each test plant (Douthit & McGuire, 1978). Virus-like
particles were found in the lumen of the oesophagus of viruliferous nematodes
(McGuire et al., 1970).
Transmission by X. americanum to soybean is inefficient (Bergeson
et al., 1964; McGuire & Douthit, 1978), suggesting that other
vectors may be involved. A possible important vector is Thrips tabaci, of
which nymphs but not adults are capable of acquiring and transmitting the virus
(Messieha, 1969). Other possible vectors are spider mites of the genus Tetranychus
(Thomas, 1969), grasshoppers of the genus Melanoplus (Dunleavy,
1957) and the tobacco flea beetle, Epitrix hirtipennis (Schuster, 1963).
There are also reports of aphid species serving as vectors (Semal, 1958; Komuro
& Iwaki, 1968; Rani et al., 1969).
Transmission through SeedSeed-transmission has been reported in at least 12 species of crop and weed
hosts, the frequency of transmission ranging from 3% in Cucumis melo to
100% in Glycine max (Mandahar, 1981; Murant, 1983). Probably some
seed-transmission occurs in most hosts. The virus is associated with the
embryonic tissue of the seed but not with the seed coat. The age of the plant at
the time of infection is the most important factor in determining the extent of
seed-transmission (Athow & Bancroft, 1959; Owusu et al., 1968).
Cross-pollination experiments with soybean suggest that infection of
megagametophytes is the principal factor contributing to seed-transmission (Yang
& Hamilton, 1974).
SerologyThe virus is a good immunogen. Rabbits given a series of intravenous or
intramuscular injections yield antiserum samples with titres up to 1/2048. A
single precipitin band is formed in gel-diffusion tests. Serologically
distinguishable strains have been identified in gel-diffusion tests (Gooding,
1970; Gergerich et al., 1983). The ELISA technique is applicable for
detecting the virus in soybean (Lister, 1978;
Moore et al., 1982) and
pelargonium (Romaine et al., 1981;
Newhart et al., 1982).
RelationshipsThe virus is the type member of the nepovirus group. Based on the occurrence
of the smaller nucleic acid species in some particles of the bottom component as
well as in those of the middle component, the virus is in a cluster of
nepoviruses that contains arabis mosaic, eucharis mottle, grapevine fanleaf,
potato black ringspot (= Andean potato calico virus) and raspberry ringspot
viruses (Harrison & Murant, 1977). The virus is not related serologically to
arabis mosaic, grapevine fanleaf or raspberry ringspot viruses but it is related
to eucharis mottle and potato black ringspot viruses. In fact, these two
viruses, both originating in Peru, have been considered as strains of tobacco
ringspot virus (Kahn et al., 1962; Fribourg, 1977). However, the
serological relationships are not close and this criterion together with
behaviour in plant-protection tests and inability to form pseudo-recombinants
suggests that they should be considered separate viruses (Salazar &
In plant-protection tests, plants infected with one isolate usually do not
develop additional symptoms after challenge inoculation with a second isolate
(Price, 1936). An exception to this was obtained in plant-protection tests
involving an isolate from Jersey highbush blueberry, where tobacco plants
initially inoculated with a tobacco isolate or a different blueberry isolate did
not protect against the Jersey isolate when challenge-inoculated (Ramsdell,
Stability in SapIn petunia, tobacco or French bean sap the virus loses infectivity after 10
min at 60-65°C, storage at room temperature for 1-2 weeks, or dilution to
10-3 to 10-4. Lyophilized sap was infective after storage
for more than 10 years in
sealed ampoules (Hollings & Stone, 1970) or more than 17 years in leaf
tissue dehydrated over calcium chloride and stored at c. 1°C
(McKinney et al., 1965).
PurificationThe virus particles are relatively stable and many purification procedures
are satisfactory. Squash, cucumber, petunia, cowpea, French bean, tobacco and
N. clevelandii have been used as sources for purification (Steere,
1956; Stace-Smith et al., 1965; Ladipo & de Zoeten, 1972; Murant
et al., 1981). Virus yield depends on the isolate, propagation host, time
of year and purification procedure, but yields of 50-100 mg/kg tissue are not
A purification procedure devised by Steere (1956) involved the addition of
butanol and chloroform to the extracted sap at the rate of 1:1:1. This procedure
has the disadvantage of using large quantities of organic solvents. A
modification that is equally satisfactory involves the addition of
a final concentration of 8.5% (Tomlinson et al., 1959). After
clarification of leaf extracts by either of these methods, the virus may be
concentrated by differential centrifugation.
Properties of ParticlesThe particles are all the same size but sediment as three components in
sucrose density gradients (Fig.5). The top component (T) consists of empty
protein shells; the middle (M) and bottom (B) components are nucleoproteins
containing different amounts of RNA. The B component particles are of two types
containing either 1 molecule of RNA-1 or 2 molecules of RNA-2. Isolates
containing the satellite RNA produce 11 to 14 additional types of particle
containing different numbers of satellite RNA molecules.
Sedimentation coefficients (s20,w) in svedbergs:
53 (T), 91(M) and 126 (B) (Schneider & Diener, 1966; Fig.6). Sedimentation
particles containing the satellite RNA range from 91 to 126 S (Schneider
Particle weight (daltons; assuming 60 subunits of M. Wt 57,000): 3.4 x
(T), 4.7 x 106 (M), 6.1 x 106 (B) (Mayo et al.,
Diffusion coefficient (D20 x 10-7 cm2
sec-1): 1.59 (Stace-Smith et al.,
Isoelectric point: pH 4.7 (Stanley, 1939).
Electrophoretic mobility: 11.3 x 10-5 cm2
volt-1 sec-1 in 0.05 M phosphate, pH 7.0 (Steere, 1956).
Absorption coefficient (A0.1%,1 cm) at 260 nm: about 10.0 (B) (R.
Stace-Smith, unpublished data).
A260/A280: 0.72 (T), 1.38 (M), 1.57 (B)
(R. Stace-Smith, unpublished
Buoyant density (g/cm3): 1.423 (M); bottom component has two
populations averaging 1.507 (B1) and 1.518 (B2)
(Schneider et al., 1972a). Buoyant densities of particles
containing the satellite RNA range from 1.408 to 1.529 in increments of
0.009 (Schneider et al., 1972a).
Particle StructureParticles are c. 28 nm in diameter, with angular outlines, and have
60 structural subunits (Mayo et al., 1971). Electron micrographs show
some particles completely, some partially and some not penetrated by
phosphotungstate (Fig.7). Particles penetrated by negative stain do not
necessarily represent particles devoid of RNA; the proportion of particles
penetrated increases with increasing pH of the stain but the staining time has
no effect on penetration (Davison & Francki, 1969).
Particle CompositionNucleic acid: RNA, single-stranded. The genome comprises two
essential RNA molecules, RNA-1 and RNA-2 (Harrison et al., 1972), with
M. Wt of 2.73 x 106 and 1.34 x 106 respectively, estimated
by electrophoresis of
glyoxylated RNA in 0.75% agarose gels (Murant et al., 1981). The
sedimentation coefficient of RNA-1 is c. 32 S and that of RNA-2
c. 24 S. For unfractionated RNA, the percentage nucleotide
composition is G:A:C:U = 24.7:23.1:22.4:29.8 (Stace-Smith et al.,
Protein: Coat protein can be isolated by disrupting virus in 1.0 M
HCl at room temperature for 24 h (Stace-Smith et al., 1965) or by
heating for 2 h at 55-60°C in 0.1 M phosphate buffer, pH 8.0 (Chu &
Francki, 1979). The protein subunit has a M. Wt of approximately 57,000 (Mayo
et al., 1971) although there is evidence to suggest that each subunit is
a stable tetramer of a smaller protein with a M. Wt of c. 13,000 (Chu &
Genome PropertiesEach RNA species contains polyadenylate, apparently at the 3' end (Mayo et
al., 1979a) and a protein of M. Wt c. 4000 attached covalently,
probably at the 5' end (Mayo et al., 1979b). This genome-linked
protein is apparently needed for infectivity because infectivity is abolished by
incubation with Pronase or proteinase K (Harrison & Barker, 1978; Mayo et
al., 1982) but it is not necessary for viral RNA translation in vitro
in a wheat germ system (Chu et al., 1981). In this system and in the
rabbit reticulocyte lysate system, RNA-1 is translated into proteins of M. Wt
25,000 and 205,000, one or both of which is processed to produce proteins of M.
Wt 195,000 and 135,000; RNA-2 is translated into protein predominantly of M. Wt
116,000 which is processed in reticulocyte lysates by a protein induced by RNA-1
into products of M. Wt 53,000, 40,000 and 23,000. The 53,000 M. Wt product is
precipitated by antiserum to tobacco ringspot virus and is presumably the virus
coat protein (Forster & Morris-Krsinich, 1985).
SatellitesSmall satellite ssRNA molecules which depend upon the genomic RNA molecules
of the virus for coat protein and for replication functions have been detected
in the particles of some isolates of the virus (Schneider, 1971; Schneider et
al., 1972a,1972b; Rezaian, 1980). The most abundant molecule (RNA-S)
has a M. Wt of approximately 120,000 (Sogo et al., 1974) but at least 10
covalent multimeric forms of this molecule were detected in particle
preparations by electrophoretic analysis (Kiefer et al., 1982). Neither
polyadenylate sequences nor covalently linked protein were detected in RNA-S or
its more slowly migrating forms, and the biological activity of RNA-S was not
protease-sensitive (Kiefer et al., 1982). In addition, plants infected
with the virus and RNA-S yielded a multicomponent population of RNA molecules
having some of the properties of dsRNA (Schneider & Thompson, 1977).
Electron microscopy of such material revealed linear molecules of various
lengths but also circular molecules and racket-like structures (Sogo &
Schneider, 1982). When denatured, this partially double-stranded RNA fraction
gives a series of up to 12 electrophoretic components that contain both RNA-S
sequences and sequences that hybridize with RNA-S; they represent an oligomeric
series of (+) and (-) stranded satellite RNA sequences (Kiefer et al., 1982).
Linthorst & Kaper (1984) found circular single-stranded monomeric and
dimeric forms of the satellite in infected tissue but detected only linear (+)
stranded monomers and dimers in RNA from purified virus particles. The evidence
suggests that RNA-S molecules replicate via a rolling circular mechanism
analogous to that proposed for viroid replication (Kiefer et al., 1982;
Linthorst & Kaper, 1984).
Relations with Cells and TissuesThe virus particles are morphologically similar to ribosomes and individual
particles are consequently difficult to identify in thin sections of infected
tissue. However, they can be recognized when they associate in characteristic
ways, e.g. within tubules, in crystalline arrays or in unstructured aggregates.
Files of particles, enclosed in tubules and frequently associated with
plasmodesmata, were detected in the root tips of infected French bean (Crowley
et al., 1969), in the meristematic cells of tobacco (Roberts et al.,
1970; Walkey & Webb, 1970), and in the cell walls of infected soybean
seed (Yang & Hamilton, 1974). Particle aggregates were not detected in
root-tip or leaf cells of infected French bean, cucumber or cowpea (Crowley
et al., 1969) but they were observed in soybean in the bundle sheath
(Halk & McGuire, 1973), and in the intine of the pollen wall, the wall
and the cytoplasm of the generative cell, the integuments, nucellus, embryo
sac wall and megagametophytic cells (Yang & Hamilton, 1974).
NotesTobacco ringspot virus may be confused with several other nepoviruses when
identification is based on the symptom response in a range of herbaceous
indicator plants. Of the various nepoviruses, tomato ringspot is the one most
likely to be confused with tobacco ringspot because these two viruses commonly
infect the same species and occur in the same geographical region. McLean (1962)
reported that 11 of 43 species that were tested showed differential reactions to
the two viruses. Despite the possibility of distinguishing these viruses on the
basis of host reactions, serological tests are essential for positive
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Symptoms in naturally infected sweet cherry.
Local and systemic symptoms in Cucumis sativus.
Lesions in inoculated Nicotiana tabacum leaf.
Local and systemic symptoms in Nicotiana clevelandii.
Sucrose density gradient profile of a purified preparation
showing top (T), middle (M) and bottom (B) components. Gradient was centrifuged
in a Beckman SW41 rotor at 4°C, 38 000 rev/min for 90 min.
Analytical ultracentrifugation photograph taken with schlieren optics
showing relative proportion of (left to right) T, M and B components.
Virus particles from a purified preparation stained with 2% uranyl
acetate. Bar represents 100 nm.