Agricultural Research Organization, Volcani Center, Bet Dagan, Israel
A. F. Murant
Scottish Crop Research Institute, Invergowrie, Dundee, Scotland
Beet yellows virus
Closteroviruses have very flexuous filamentous particles c.
1 nm in diameter but fall into three subgroups with particle lengths of c.
1250-1450 and 1650-2000 nm and sedimentation coefficients of c.
96, 110 and 140 S.
The particles contain a single molecule of ssRNA which, depending on the
subgroup, has M. Wt (x 10-6
) of c.
2.5, 4.7 and 6.5 and constitutes
about 5% of the particle weight. There is a single species of coat protein of M. Wt
) 23.5-25 which is arranged as a helix (pitch 3.7 nm) enclosing the
genome. The coat proteins of several members have a low content of aromatic amino acids
which may explain the unusually high
ratios given by
particle preparations. Thermal inactivation points (10 min) are 40-55°C, longevity
in sap 12-48 h, dilution end-points usually 1/500-1/10,000 and concentration in sap
0.3-40 mg/100 g tissue.
Most closteroviruses are transmitted by aphids in a semi-persistent manner; the mode
of transmission of some members is unknown. Cytopathological effects are mostly confined
to cells of the phloem which contain characteristic aggregates of virus particles and
accumulations of vesicles. Members of this group have restricted or only moderately wide
host ranges, but some cause economically important diseases.
Table 1 lists the definitive and several tentative members of the group together
with some of their properties.
Table 1 Definitive and tentative members of the closterovirus group
|Virus and abbreviation
||Description No. or Ref.
||Modal length (nm)
||Family of major host
|Apple chlorotic leaf spot
| Grapevine stem pitting-associated (=grapevine leaf roll?)*
||Conti et al. (1980)
Namba et al. (1979)
|Beet yellow stunt
|Carnation necrotic fleck
||Inouye & Mitsuhata (1971)
|Carrot yellow leaf*
||Yarnashita et al. (1976)
||Ohki et al. (1976)
||Schmidt et al. (1963)
||Bern & Murant (1979a)
|Lilac chlorotic leaf spot*
|Wheat yellow leaf
* Tentative assignment to this group-virus needs further characterization.
Geographical Distribution etc
ACLSV, BYV, CTV and CNFV occur throughout the geographical ranges of their respective
hosts. Most other closteroviruses have restricted distributions. Host ranges vary
considerably: BYV infects 120 species in 15 families, whereas almost all other members
have restricted host ranges consisting of a few species within the principal host plant
family and few if any in non-related species (reviewed in
Bar-Joseph, Garnsey & Gonsalves, 1979
Lister & Bar-Joseph, 1981
Association with Vectors
Most closteroviruses are transmitted by aphids in the semi-persistent manner, but
the modes of transmission of ACLSV, FNV, GSAV and LCLV are unknown. Transmission of HLV
is dependent on a helper virus
(Bem & Murant, 1978
unpublished data) which is not yet identified. The minimum acquisition access times
for BYV, CNFV and CTV were 15-30 min but a longer acquisition period (24 h) resulted
in much higher frequencies of transmission
(Ohki et al., 1977
Inouye & Mitsuhata, 1973
Costa & Grant, 1951
Raccah, Loebenstein & Bar-Joseph, 1976
BYV was retained by aphids for up to 3 days but the frequency of transmission fell by 50% in 8 h
The minimum inoculation access time for
BYV was 15 min with maximum frequencies of transmission after 1 to 6 h. BYV was
transmitted experimentally by 23 aphid species, CTV by seven, BYSV, HLV and HV6 by
three, and BdYV, CNFV, CYLV, CYV and WYLV were each transmitted by a single aphid species (see
Bar-Joseph et al., 1979
, for a recent review). Differential
transmission of CTV strains by A. gossypii
(Bar-Joseph & Loebenstein, 1973
is considered the main cause of the great differences in rate of virus spread at
different times in different citrus-growing areas.
Closteroviruses are not seed-borne, and do not spread by contact. Long distance
spread by vectors is uncommon and the highest incidence of disease occurs in areas
adjacent to the virus source
(Heathcote & Cockbain, 1966
). The world-wide
dissemination of ACLSV, CNFV and CTV, and the transfer of BYV to the USA have occurred
mainly through distribution of infected planting material. The severe losses caused to
the citrus industry by CTV in South America are considered a classic case of a
The compulsory use of CTV-free propagation material and the introduction of
coordinated eradication programmes has prevented spread of CTV in California and in
several Mediterranean citrus areas
(Rosenberg et al., 1978). A weather factor
formula (Watson et al., 1975)
has been used to forecast aphid movement so that
BYV epidemics can be prevented by aphicide application.
Relations with Cells and Tissues
Closterovirus particles are confined mainly to phloem tissue where they induce
swelling and disintegration of chloroplasts and mitochondria, and accumulation of
osmiophilic globules in the mitochondria and of phytoferritin in the chloroplasts.
In addition to these non-specific reactions, closteroviruses of sub-groups B and C
(Table 1) induce characteristic types of inclusion and the accumulation of
(Esau & Hoefert, 1971a
Plaskitt & Bar-Joseph, 1978
Some inclusions are cross-banded and consist of virus aggregates
having a periodicity arising from an orderly arrangement of particles in stacked layers.
Sections of the aggregates reveal three distinctive patterns: (1) cross-sections of
hexagonal arrays with a centre-to-centre distance of 109 Å (measured only for CNFV;
Bar-Joseph, Josephs & Cohen, 1977
(2) regions of nearly parallel virus particles;
(3) regions in which no orderly arrangement is evident. Tilting of the specimen shows
that these patterns represent different orientations of the same arrangement of particles.
The characteristic vesicles are more or less rounded in outline, 80-120 nm in diameter,
and contain a fine network of fibrils.
Esau & Hoefert (1971a
) suggested that
vesicles originated de novo
as sites of synthesis of virus RNA.
Table 1 summarizes some properties of individual closteroviruses. The closteroviruses
have very flexuous filamentous particles of width c.
12.0 ± 1 nm and
with obvious cross-banding of pitch c.
3.4-3.8 nm. There are three morphological
subgroups, A, B and C, with particle modal lengths of approximately 730, 1250-1450 and
1650-2000 nm respectively (Table 1). These length differences are reflected in the
genome sizes, which are 2.5 x 106
for ACLSV and HLV
(Bar-Joseph, Hull & Lane, 1974
Murant et al., 1981
), 4.2 x 106
(Bar-Joseph & Hull, 1974
Carpenter, Kassanis & White, 1977
) and 6.5 x 106
(Gumpf, Bar-Joseph & Dodds, 1981
Thus closterovirus particles have similar ratios
of RNA mass to modal length, and there are probably four nucleotides for each protein subunit
(Bar-Joseph & Hull, 1974
Length differences within subgroups could be real
but might also reflect differences in calibrating techniques or in the type of stain,
which has been shown to affect BYV, CNFV and HLV modal lengths. Particles of ACLSV,
BYV, CNFV, CTV and HLV contain a single species of protein of 2.35-2.5 x 104
daltons. Protein subunits of ACLSV, BYV, CNFV and HLV lack tryptophan
(Short et al., 1977
Carpenter et al., 1977
Bem & Murant, 1979c
) which may
explain why their
ratios are anomalously high (1.4-1.8).
Particles of ACLSV, BYV, CTV and HLV are disrupted by CsCl but stable in
in which their buoyant densities are 1.24-1.27 g/cm3
(Bar-Joseph & Hull, 1974
Flores et al., 1975
Gonsalves, Purcifull & Garnsey, 1978
Bem & Murant, 1979c
Relationships within the Taxon
Information on relationships within the group is limited. Definite antigenic
relationships have been established between BYV and CNFV
(Short et al., 1977
judged by their gross composition there are c.
50 amino acid replacements
between these two viruses. Antisera to ACLSV, BYV, BYSV, CNFV, CTV; LCLV and WYLV did
not cross-react with HLV, and antiserum to HLV did not react with ACLSV
(Bem & Murant, 1979a
Antisera to CTV did not cross-react in ELISA with CNFV and WYLV
(M. Bar-Joseph & T. Inouye, unpublished data). Cross protection tests between
ACLSV and HLV (Bem & Murant, 1979a
gave no indication of strain relationships.
The morphology of the flexuous particles and some of the cytopathological features
associated with infection suggest that viruses associated with the alligator weed stunting disease
(Hill & Zettler, 1973) and dendrobium vein necrosis
should be grouped as closteroviruses. Cucumber yellows virus, which is transmitted
by the whitefly Trialeurodes vaporariorum, has filamentous particles c. 1000 x 12 nm
(Yamashita et al., 1979) resembling those of closteroviruses, and
also induces similar cytopathological features, including vesicular structures. However
further in formation on biochemical properties is needed to establish whether it should
be placed in this group. Several viruses included in the group lack some group
characteristics: ACLSV, FNV, GSAV and LCLV are not known to be aphid-transmitted, and
ACLSV and LCLV do not have the typical cytopathological effects.
Affinities with Other Groups
No well-characterized viruses have close affinities with closteroviruses. Two
viruses previously included in this group because of superficial similarities in particle
morphology, apple stem grooving virus
(Desc. 31) and
potato virus T
(Desc. 187), and
possibly also the citrus stunt-tatter leaf virus, are in fact quite distinct and should
be placed in a new group of elongated plant viruses.
- Bar-Joseph & Hull, Virology 62: 552, 1974.
- Bar-Joseph & Loebenstein, Phytopathology 63: 716, 1973.
- Bar-Joseph, Hull & Lane, Virology 62: 563, 1974.
- Bar-Joseph, Josephs & Cohen, Virology 81: 144, 1977.
- Bar-Joseph, Garnsey & Gonsalves, Adv. Virus. Res. 25: 93, 1979.
- Bem & Murant, Rep. Scott. hort. Res. Inst., 1977: 100, 1978.
- Bem & Murant, Ann. appl. Biol. 92: 237, 1979a.
- Bem & Murant, Ann. appl. Biol. 92: 243, 1979b.
- Bem & Murant, J. gen. Virol. 44: 817, 1979c.
- Carpenter, Kassanis & White, Virology 77: 101, 1977.
- Conti, Milne, Luisoni & Boccardo, Phytopathology 70: 394, 1980.
- Costa & Grant, Phytopathology 41: 105, 1951.
- Esau & Hoefert, Protoplasma 72: 255, 1971a.
- Esau & Hoefert, Protoplasma 72: 459, 1971b.
- Esau & Hoefert, Protoplasma 73: 51, 1971c.
- Flores, Garro, Conejero & Cunat, Revta Agroquim. Tecnol. Aliment. 15: 93, 1975.
- Gonsalves, Purcifull & Garnsey, Phytopathology 68: 553, 1978.
- Gumpf, Bar-Joseph & Dodds, Phytopathotogy 71: 878, 1981.
- Heathcote & Cockbain, Ann. appl. Biol. 57: 321, 1966.
- Hill & Zettler, Phytopathology 63: 443, 1973.
- Inouye & Mitsuhata, Nogaku Kenkyu 54: 1, 1971.
- Inouye & Mitsuhata, Ber. Ohara Inst. landw. Biol. 15: 195, 1973.
- Lesemann, Phytopath. Z. 89: 330, 1977.
- Lister & Bar-Joseph, in Handbook of Plant Virus Infections and Comparative Diagnosis, p. 809, ed. E. Kurstak, Amsterdam: Elsevier/North-Holland, 943 pp., 1981.
- Murant, Rep. Scott. hort. Res. Inst., 1979: 103, 1980.
- Murant, Rep. Scott. hort. Res. Inst., 1980: 102, 1981.
- Murant, Taylor, Duncan & Raschké, J. gen. Virol. 53: 321, 1981.
- Namba, Yamashita, Doi, Yora, Terai & Yano, Ann. phytopath. Soc. Japan 45: 497, 1979.
- Ohki, Doi & Yora, Ann. phytopath. Soc. Japan 42: 313, 1976.
- Ohki, Yamashita, Arai, Doi & Yora, Ann. phytopath. Soc. Japan 43: 46, 1977.
- Plaskitt & Bar-Joseph, Micron 9: 109, 1978.
- Raccah, Loebenstein & Bar-Joseph, Phytopathology 66: 1102, 1976.
- Rosenberg, McEachern, Blanc, Robinson & Foote, in The Citrus Industry, Vol.IV, Crop Protection, p. 233, ed. W. Reuther, E. C. Calavan & G. E. Carman, Berkeley: Univ. Calif. Press, 362 pp., 1978.
- Schmidt, Richter, Hertzch & Klinkowski, Phytopathotogy 47: 66, 1963.
- Short, Hull, Bar-Joseph & Rees, Virology 77: 408, 1977.
- Sylvester, J. econ. Entomol. 49: 789, 1956.
- Watson, Proc. R. Soc., B. 133: 200, 1946.
- Watson, Heathcote, Lauckner & Sowray, Ann. appl. Biol. 81: 181, 1975.
- Yamashita, Ohki, Doi & Yora, Ann. phytopath. Soc. Japan 42: 382, 1976.
- Yamashita, Doi, Yora & Yoshino, Ann. phytopath. Soc. Japan 45: 484, 1979.
- Esau & Hoefert, J. Ultrastruct. Res. 75: 326, 1981.