Rice stripe virus
Laboratory of Plant Pathology, Faculty of Agriculture, University of Tokyo, Bunkyo-ku, Tokyo 113, Japan
Disease described by
Kuribayashi (1931a). Virus characterized by
S. Toriyama (1982a,
A virus with filamentous particles, of undetermined length but only c.
8 nm wide. The particles sediment as three components and contain four RNA
species and a single type of protein. Non-structural protein material is
produced abundantly in infected cells. Mechanical inoculation is difficult.
The virus is transmitted by Laodelphax striatellus and three other
planthopper species in a persistent manner; it is transmitted through the egg
to about 90% of progeny insects. It infects many species of Gramineae but is
not known to infect plants in other families. It occurs in rice-growing areas
of Asia and the USSR, and causes significant reduction in rice yield.
In rice the virus causes chlorotic stripes, chlorosis, moderate stunting
and loss of vigour (Fig.1
); in severe infections the leaves develop brown to
grey necrotic streaks and die. Diseased plants produce few or no panicles; those
produced carry whitish to brown discoloured malformed spikelets (Fig.3
infection of rice causes significant loss of yield
(Yasuo, Ishii & Yamaguchi, 1965
late infection also reduces yield by retarding ear emergence and ripening
(Yasuo et al., 1965
). In maize and wheat the
virus causes chlorotic stripes, chlorosis and stunting.
The disease was first recognized in the early 1900s in central Japan, where
severe damage was caused to rice crops. Since the 1950s the extension of early
planting favoured the occurrence of the disease in Japan
(Yasuo et al., 1965
) and Korea
). In Japan c
. 200,000 ha of rice
is affected each year. Damage in rice has also been reported in China
) and the USSR
(Reifman, Pinsker & Krylova, 1978
Host Range and Symptomatology
The virus occurs naturally in rice, maize, wheat, oat, foxtail millet and
wild grasses such as Cynodon dactylon, Digitaria adscendens, D. violascens,
and Setaria viridis.
The virus is reported to
infect 37 species of the family Gramineae but no species in other families. The
main type of symptom induced is chlorotic striping
Yamada & Yamamoto, 1956
The virus is readily transmitted to test plants by the planthopper,
but is difficult to transmit mechanically.
Okuyama & Asuyama (1959)
obtained infection in 6% of plants that were injected with crude extracts
made from diseased plants with 0.01 M cysteine-HCl, and
infection in 0.9% of plants that were injected with extracts of viruliferous
Oryza sativa (rice). Seedlings of most Japanese paddy varieties are highly
susceptible to infection (See Notes). Chlorotic stripes, mostly with light
yellowish broken streaks (Fig.1), develop on systemically infected leaves 10
to 25 days after inoculation by planthoppers (L. striatellus).
Characteristically, limp chlorotic leaves emerge without unfolding, elongate,
droop and wilt (Fig.2). Yellowing and moderate stunting also occur.
Triticum aestivum (wheat) and Zea mays (maize) (cv. Golden Cross
Bantam). Symptoms in these species are similar to those in O. sativa.
Wheat plants may produce whitish, rolled, fine leaves that quickly droop.
Rice, wheat and maize are used to maintain cultures and as a source of virus for
purification. Young rice seedlings are readily killed, and so care must be taken
to use the appropriate growth stage and varieties, e.g. third leaf stage of rice
cv. Norin No. 8 or Kinmaze. When maize seedlings are used, wheat, barley or
rice plants must also be planted, or the planthoppers will die within 2-3 days.
Young rice and wheat seedlings are suitable for assaying transmission by insect
An isolate that causes mild symptoms on rice
(Ishii & Ono, 1966
) and two
variants that differ in symptoms induced in wheat and in insect transmissibility
are reported but there are no detailed studies of these isolates.
Transmission by Vectors
The most active vector in the field is the small brown planthopper, Laodelphax striatellus
); three other
planthopper species, Unkanodes sapporona
), U. albifascia
) and Terthron albovittatum
) also transmit.
The proportion of active transmitters of L. striatellus
is about 20%
Although the shortest acquisition feeding period is 15 min,
best transmission is obtained with planthoppers that acquire the virus by
feeding for 1 day. The incubation period of the virus in L. striatellus
ranges from 5 to 21 days but incubation is complete within 5 to 10 days for most
individuals. Minimum inoculation feeding time is 3 min: about half or more of
the infective planthoppers infect rice seedlings after feeding for 1 h
(Yamada & Yamamoto, 1955
Ability of the insects to transmit the
virus decreases markedly with age. Females of L. striatellus
efficient transmitters than males
). The virus passes through
a high percentage of eggs to progeny, about 90% in L. striatellus
Yamada & Yamamoto, 1954
was selected and bred for high or low ability
to acquire and transmit the virus (50-60% and less than 10% of the insects
transmitting, respectively), and this was correlated with the frequency of
transmission of the virus through the eggs
). Evidence of virus
multiplication in L. striatellus
has been obtained by repeated passage
through the eggs for 6 years through 40 generations
), by serial
transfer of the virus from insect to insect by injection
(Okuyama, Yora & Asuyama, 1968
and by detection of virus particle antigen in various organs
of viruliferous insects with the fluorescent antibody staining technique
(Kitani, Kiso & Yamamoto, 1968
Transmission through Seed
None found in rice (Kuribayashi, 1931b
The virus is a good immunogen. Rabbit antisera with titres of 1/512 to
1/1024 in precipitin tests are readily obtained. In agar gel diffusion tests,
it is necessary to disrupt virus particles in purified preparations or crude
sap of infected tissues by treatment with 0.5% SDS. The haemagglutination
test was used to detect the virus particle antigen at high dilutions in vectors or plants
(Saito & Iwata, 1964
Yasuo & Yanagita, 1963
Sonku & Sakurai, 1973b
The virus is serologically related to
maize stripe virus
(Gingery, Nault & Bradfute, 1981
but not to rice hoja blanca virus
(Yasuo, Yanagita & Yamaguchi, 1961
The particle structure of these three viruses is similar
(S. Toriyama, 1982b
In recent work (H. Hibino, personal communication) a
filamentous virus purified from rice with grassy stunt disease was found to be
distantly serologically related to rice stripe virus.
Stability in Sap
Assayed by observing transmission by injected insects. Dilution end-point:
in extracts from viruliferous insects and
in sap from diseased leaves. Thermal inactivation
point (5 min): 50-55°C. Longevity: 4 days in extracts of viruliferous
insects kept at 4°C, 8-12 months in viruliferous insects and diseased
rice plants kept at -20°C, and 1-2 months in purified preparations kept
at -20°C (Kiso, Yamamoto & Kitani, 1974
(S. Toriyama, 1982a
Grind infected leaves in 0.1 M
containing 10 mM DIECA, and adjust to pH 7.2 with
solid ascorbic acid. After clarification by treatment with 20% chloroform,
collect the virus by centrifugation for 2 h at 123,000 g
precipitation from 8% polyethylene glycol. Resuspend the virus in 0.01 M
phosphate buffer, pH 7.5, and purify by repeated low and high speed centrifugation.
Host plant impurities can be precipitated by adding solid ammonium sulphate to
30% saturation. The preparation can be further purified by centrifugation in
10-40% linear sucrose density gradients. The infective component (nB) aggregates
readily and sediments to the bottom of sucrose gradient tubes; it may be
necessary to resuspend the pellet and repeat the density gradient centrifugation.
The yield of virus is 20-30 mg per 100 g fresh leaves. Addition of
, EDTA or bentonite to the buffer did not
improve preservation of the virus particles (S. Toriyama, unpublished data).
Properties of Particles
The virus particles sediment as three main components: middle (M), bottom
(B) and nB component (Fig.5
(S. Toriyama, 1982a
). A top component
also occurs but consists of degraded particles
(S. Toriyama, 1982a
Sedimentation coefficients (s20,w) determined on a
preparation with A260= 10: 72 S (M)
65 S (M), 80 S (B) and 98 S (nB) (S. Toriyama, unpublished data).
A260/A280: 1.49, determined on an unfractionated
preparation (Koganezawa, Doi & Yora, 1975).
Absorbance at 260 nm (1 mg/ml, 1 cm light path): 4.4, determined on an
unfractionated preparation; not corrected for light-scattering (S. Toriyama, unpublished data).
Buoyant density in caesium chloride: 1.282 g/cm3 (all components)
(S. Toriyama, unpublished data)
Isoelectric point: particles precipitate at around pH 4.5 (S. Toriyama, unpublished data).
The virus was formerly thought to have spherical particles
(Koganezawa et al., 1975
) but it is now known that the particles are
filamentous, and only c.
8 nm wide (Fig.8
(S. Toriyama, 1982b
In negatively stained dip preparations, the virus is mostly observed as apparently
branched structures. The length of particles of M component (including length of branches) was 400 nm
(Koganezawa et al., 1975
). The branched appearance is
caused by supercoiling: completely unfolded particles possess a helical structure
3 nm wide which in turn form secondary coils about 8 nm wide
(S. Toriyama, 1982b
Particle CompositionNucleic acid:
RNA, single-stranded. Four species, of M. Wt
) 1.9, 1.4, 1.0 and 0.9
(S. Toriyama, 1982a
two smallest RNA species occur in M component (which is a mixture of two
components), the 1.4 x 106
M. Wt RNA occurs in B component and the
1.9 x 106
M. Wt RNA in nB component (Fig.4
). Only the nB component
particles are infective. The RNA constitutes about 12% of the particle weight,
as judged by the A260
value of purified preparations.
The three RNA species from M and B components are linear molecules about 0.7-1.0
µm long (S. Toriyama, 1982a
Protein: One species, of M. Wt 3.2 x 104
S. Toriyama, 1982b).
Amino acid composition: asp 25 residues; thr 28;
ser 21; glu 22; pro 5; gly 21; ala 23; cys ?; val 14; met 8; ileu 14; leu 24;
tyr 9; phe 8; lys 27; his 5; arg 7; trp ? (S. Toriyama, unpublished data).
Other components: No significant amounts of lipid or polyamine are
found in purified preparations (S. Toriyama, unpublished data).
Relations with Cells and Tissues
Large inclusions, shaped like rings, rods or figures of eight, are present in infected cells
Hirai et al., 1964
Reifman et al., 1978
The inclusions usually contain many granules, but some have no granules
and resemble crystalline inclusions. The inclusions probably consist of the
non-structural protein which is serologically unrelated to the coat protein and
is produced abundantly in infected cells of plants with severe symptoms but less
so or not at all in infected cells of tolerant or resistant varieties. The
isoelectric point is pH 5.4. Purified non-structural protein forms needle crystals
at pH 4-5. Its sedimentation coefficient (s20,w
) is 3
(Kiso & Yamamoto, 1973
One polypeptide species, of M. Wt 2 x 104
was reported by
Amino acid composition: asp 19 residues; thr 11;
ser 11; glu 18; pro 12; gly 8; ala 4; cys ?; val 5; met 4; ileu 6: leu 20;
tyr 6; phe 8; lys 13; his 7; arg 4; trp ? (S. Toriyama, unpublished data; see
also Kiso & Yamamoto, 1973
In sections of infected plant cells
(Koganezawa, 1977), recognition of
individual filamentous virus particles is difficult but granular regions,
sometimes enclosed by membranes, can be observed in the cytoplasm. These regions
are possibly formed from virus aggregates. Virus particle antigen was detected
in phloem tissue and mesophyll of infected wheat leaves by fluorescent antibody
staining (Kiso et al., 1974).
The virus moves downwards in the phloem
at a rate of 25-30 cm/h at 30°C and multiplies when young tissues are
reached (Sonku & Sakurai, 1973a,
Rice stripe is readily distinguished from other viruses infecting rice,
wheat and maize by its characteristic symptoms and its transmissibility by
The resistance of rice (Oryza sativa)
virus has been extensively studied. Most Japanese paddy varieties are highly
susceptible but Japanese upland varieties and indica-
type rice varieties
are resistant and/or tolerant. Inheritance of resistance appears to be governed
by multiple alleles with various levels of resistance: gene St2
Japanese upland varieties and gene St2i
varieties. A gene St1
at another locus as well as St2
essential for resistance in Japanese upland varieties. Resistant Japanese paddy
varieties (Chugoku No. 31 and Mineyutaka) have been bred
(Yamaguchi, Yasuo & Ishii, 1965
Sakurai & Ezuka, 1964
Washio et al., 1967
K. Toriyama, 1969
K. Toriyama et al., 1966
- Amano, J. Pl. Prot., Tokyo 24: 774, 1937.
- Chen, Chekiang agric. Sci. 3: 123, 1964.
- Gingery, Nault & Bradfute, Virology 112: 99, 1981.
- Hirai, Suzuki, Kimura, Nakazawa & Kashiwagi, Phytopathology 54: 367, 1964.
- Hirao, Jap. J. appl. Ent. Zool. 12: 137, 1968.
- Iida, in The Virus Diseases of the Rice Plant, p. 3, Baltimore: Johns Hopkins, 1969.
- Ishii & Ono, Ann. phytopath. Soc. Japan 32: 83, 1966.
- Kawai, Ann. phytopath. Soc. Japan 9: 97, 1939.
- Kisimoto, Proc. Conf. on Relationships between Arthropods and Plant-Pathogenic Viruses (mimeo), Tokyo, p. 73, 1965.
- Kisimoto, Virology 32: 144, 1967.
- Kiso & Yamamoto, Rev. Pl. Prot. Res. 6: 75, 1973.
- Kiso, Yamamoto & Kitani, Bull. Shikoku agric. Exp. Stn 27: 1, 1974.
- Kitani, Kiso & Yamamoto, Bull. Shikoku agric. Exp. Stn 18: 117, 1968.
- Koganezawa, Symp. Virus Dis. trop. Crops, Trop. Agric. Res. Ser. No.10, p. 151, Trop. Agr. Res. Cent. Japan, 1977.
- Koganezawa, Doi & Yora, Ann. phytopath. Soc. Japan 41: 148, 1975.
- Kuribayashi, Bull. Nagano agric. Exp. Stn 2: 45, 1931a.
- Kuribayashi, J. Pl. Prot., Tokyo 18: 565, 636, 1931b.
- Lee, in The Virus Diseases of the Rice Plant, p. 67, Baltimore: Johns Hopkins, 1969.
- Lee, Taiwan Agric. 11: 95, 1975.
- Okuyama, Doct. Thesis, Univ. Tokyo, 155 pp., 1959.
- Okuyama & Asuyama, Ann. phytopath. Soc. Japan 24: 35, 1959.
- Okuyama, Yora & Asuyama, Ann. phytopath. Soc. Japan 34: 255, 1968.
- Reifman, Pinsker & Krylova, Arch. Phytopath. PflSchutz. 14: 273, 1978.
- Saito, Rev. Pl. Prot. Res. 10: 83, 1977.
- Saito & Iwata, Virology 22: 426, 1964.
- Sakurai, in The Virus Diseases of the Rice Plant, p. 275, Baltimore: Johns Hopkins, 1969.
- Sakurai & Ezuka, Bull. Chugokunatn. agric. exp. Stn A 10: 51, 1964.
- Shinkai, Ann. phytopath. Soc. Japan 18: 169, 1954.
- Shinkai, Ann. phytopath. Soc. Japan 20: 100, 1955.
- Shinkai, Bull. natn. Inst. agric. Sci. Tokyo C 14: 1, 1962.
- Shinkai, Ann. phytopath. Soc. Japan 32: 317, 1966.
- Shinkai, Ann. phytopath. Soc. Japan 36: 375, 1970.
- Sonku, Bull. Chugoku natn. agric. exp. Stn E 8: 1, 1973.
- Sonku & Sakurai, Ann. phytopath. Soc. Japan 39: 53, 1973a.
- Sonku & Sakurai, Ann. phytopath. Soc. Japan 39: 109, 1973b.
- Sugiyama, Ann. phytopath. Soc Japan 32: 83, 1966.
- K. Toriyama, in The Virus Diseases of the Rice Plant, p. 313, Baltimore: Johns Hopkins, 1969.
- K. Toriyama, Rev. Pl. Prot. Res. 5: 22, 1972.
- K. Toriyama, Sakurai, Washio & Ezuka, Bull. Chugoku natn. agric. exp. Stn A 13: 41, 1966.
- K. Toriyama, Washio, Sakurai, Ezuka, Shinoda, Sakamoto, Yamamoto, Morinaka & Sekizawa, Bull. Chugoku natn. agric. exp. Stn A 21: 1, 1972.
- S. Toriyama, Ann. phytopath. Soc. Japan 48: 482, 1982a.
- S. Toriyama, J. gen. Virol. 61: 187, 1982b.
- Washio, Ezuka, Sakurai & K. Toriyama, Jap. J. Breed. 17: 91, 1967.
- Washio, K. Toriyama, Ezuka & Sakurai, Jap. J. Breed. 18: 96, 1968a.
- Washio, K. Toriyama, Ezuka & Sakurai, Jap. J. Breed. 18: 167, 1968b.
- Yamada & Yamamoto, Ann. phytopath. Soc. Japan 18: 169, 1954.
- Yamada & Yamamoto, Spec. Bull. Okoyama pref. Agric. Exp. Stn 52: 93, 1955.
- Yamada & Yamamoto, Spec. Bull. Okayama pref Agric. Exp. Stn 55: 33, 1956.
- Yamaguchi, Yasuo & Ishii, J. cent. agric. Exp. Stn 8: 109, 1965.
- Yasuo, in The Virus Diseases of the Rice Plant, p. 167, Baltimore: Johns Hopkins, 1969.
- Yasuo & Yanagita, Ann. phytopath. Soc. Japan 28: 84, 1963.
- Yasuo, Yanagita & Yamaguchi, Ann. phytopath. Soc. Japan 26: 68, 1961.
- Yasuo, Ishii & Yamaguchi, J. cent. agric. Exp. Stn 8: 17, 1965.
Chlorotic stripe symptoms on infected leaves of rice (Oryza sativa)
compared with a healthy leaf (extreme left).
Drooping and wilting symptoms in young seedlings of O. sativa
(cv. Norin No. 8).
Malformed and immature ears, and chlorotic stripes on flag-leaves,
of rice plants infected at a late growth stage.
Ribonucleic acid species on polyacrylamide gels: (left),
three RNA segments from M + B components; (right), four RNA segments
in a preparation from nB component, all except the uppermost being caused by
contamination with M + B components.
Bands formed by rice stripe virus after sedimentation in a sucrose
gradient column: middle component (M), bottom component (B) and nB component (nB).
Partially and completely unfolded virus particles. Bar represents 100 nm.
Completely unfolded particles c. 3 nm wide. Note that they
still retain a coiled appearance. Bar represents 100 nm.
Filamentous particles, c. 8 nm wide, seen in purified nB
component. Bar represents 100 nm.