July 1982
Family: Closteroviridae
Genus: Closterovirus

Closterovirus group

M. Bar-Joseph
Agricultural Research Organization, Volcani Center, Bet Dagan, Israel

A. F. Murant
Scottish Crop Research Institute, Invergowrie, Dundee, Scotland


Type Member
Main Characteristics
Geographical Distribution etc
Association with Vectors
Relations with Cells and Tissues
Particle Properties
Genome Properties
Defective-Interfering RNA
Relationships within the Taxon
Notes on Tentative Members
Affinities with Other Groups

Type Member

Beet yellows virus

Main Characteristics

Closteroviruses have very flexuous filamentous particles c. 12 ± 1 nm in diameter but fall into three subgroups with particle lengths of c. 730, 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 (x 10-3) 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 A260/A280 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 Cryptogram
Subgroup A
Apple chlorotic leaf spot (ACLSV) 30 720 Rosaceae R/1:2.5/5:E/E:S/*
Grapevine stem pitting-associated (=grapevine leaf roll?)* (GSAV) Conti et al. (1980)
Namba et al. (1979)
800 Vitaceae R/1:2.5/*:E/E:S/*
Heracleum latent (HLV) 228 730 Umbelliferae R/1:2.5/5:E/E:S/Ve/Ap
Subgroup B
Beet yellows (BYV) 13 1250-1450 Chenopodiaceae R/1:4.2/5:E/E:S/Ve/Ap
Beet yellow stunt (BYSV) 207 1400 Chenopodiaceae */*:*/*:E/E:S/Ve/Ap
Carnation necrotic fleck (CNFV) 136 1250-1450 Caryophyllaceae R/1:4.0/5:E/E:S/Ve/Ap
Subgroup C
Burdock yellows* (BdYV) Inouye & Mitsuhata (1971) 1600 Compositae */*:*/*:E/E:S/Ve/Ap
Carrot yellow leaf* (CYLV) Yarnashita et al. (1976) 1600 Umbelliferae */*:*/*:E/E:S/Ve/Ap
Citrus tristeza (CTV) 33 2000 Rutaceae R/1:6.5/5:E/E:S/Ve/Ap
Clover yellows* (CYV) Ohki et al. (1976) 1700 Leguminosae */*:*/*:E/E:S/Ve/Ap
Festuca necrosis* (FNV) Schmidt et al. (1963) 1700 Gramineae */*:*/*:E/E:S/*
Heracleum 6* (HV6) Bern & Murant (1979a) 1400 Umbelliferae */*:*/*:E/E:S/Ve/Ap
Lilac chlorotic leaf spot* (LCLV) 202 1500-1600 Oleaceae */*:*/*:E/E:S/*
Wheat yellow leaf (WYLV) 157 1700 Gramineae */*:*/*:E/E:S/Ve/Ap

* 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; Murant, 1980; 1981 and 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 (Watson, 1946; Sylvester, 1956). 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 ‘man-assisted’ epidemic.

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 characteristic vesicles (Esau & Hoefert, 1971a, 1971b, 1971c, 1981; 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.

Particle Properties

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 for BYV (Bar-Joseph & Hull, 1974; Carpenter, Kassanis & White, 1977) and 6.5 x 106 for CTV (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 A260/A280 ratios are anomalously high (1.4-1.8). Particles of ACLSV, BYV, CTV and HLV are disrupted by CsCl but stable in Cs2SO4 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 (Lesemann, 1977) 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.


  1. Bar-Joseph & Hull, Virology 62: 552, 1974.
  2. Bar-Joseph & Loebenstein, Phytopathology 63: 716, 1973.
  3. Bar-Joseph, Hull & Lane, Virology 62: 563, 1974.
  4. Bar-Joseph, Josephs & Cohen, Virology 81: 144, 1977.
  5. Bar-Joseph, Garnsey & Gonsalves, Adv. Virus. Res. 25: 93, 1979.
  6. Bem & Murant, Rep. Scott. hort. Res. Inst., 1977: 100, 1978.
  7. Bem & Murant, Ann. appl. Biol. 92: 237, 1979a.
  8. Bem & Murant, Ann. appl. Biol. 92: 243, 1979b.
  9. Bem & Murant, J. gen. Virol. 44: 817, 1979c.
  10. Carpenter, Kassanis & White, Virology 77: 101, 1977.
  11. Conti, Milne, Luisoni & Boccardo, Phytopathology 70: 394, 1980.
  12. Costa & Grant, Phytopathology 41: 105, 1951.
  13. Esau & Hoefert, Protoplasma 72: 255, 1971a.
  14. Esau & Hoefert, Protoplasma 72: 459, 1971b.
  15. Esau & Hoefert, Protoplasma 73: 51, 1971c.
  16. Flores, Garro, Conejero & Cunat, Revta Agroquim. Tecnol. Aliment. 15: 93, 1975.
  17. Gonsalves, Purcifull & Garnsey, Phytopathology 68: 553, 1978.
  18. Gumpf, Bar-Joseph & Dodds, Phytopathotogy 71: 878, 1981.
  19. Heathcote & Cockbain, Ann. appl. Biol. 57: 321, 1966.
  20. Hill & Zettler, Phytopathology 63: 443, 1973.
  21. Inouye & Mitsuhata, Nogaku Kenkyu 54: 1, 1971.
  22. Inouye & Mitsuhata, Ber. Ohara Inst. landw. Biol. 15: 195, 1973.
  23. Lesemann, Phytopath. Z. 89: 330, 1977.
  24. Lister & Bar-Joseph, in Handbook of Plant Virus Infections and Comparative Diagnosis, p. 809, ed. E. Kurstak, Amsterdam: Elsevier/North-Holland, 943 pp., 1981.
  25. Murant, Rep. Scott. hort. Res. Inst., 1979: 103, 1980.
  26. Murant, Rep. Scott. hort. Res. Inst., 1980: 102, 1981.
  27. Murant, Taylor, Duncan & Raschké, J. gen. Virol. 53: 321, 1981.
  28. Namba, Yamashita, Doi, Yora, Terai & Yano, Ann. phytopath. Soc. Japan 45: 497, 1979.
  29. Ohki, Doi & Yora, Ann. phytopath. Soc. Japan 42: 313, 1976.
  30. Ohki, Yamashita, Arai, Doi & Yora, Ann. phytopath. Soc. Japan 43: 46, 1977.
  31. Plaskitt & Bar-Joseph, Micron 9: 109, 1978.
  32. Raccah, Loebenstein & Bar-Joseph, Phytopathology 66: 1102, 1976.
  33. 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.
  34. Schmidt, Richter, Hertzch & Klinkowski, Phytopathotogy 47: 66, 1963.
  35. Short, Hull, Bar-Joseph & Rees, Virology 77: 408, 1977.
  36. Sylvester, J. econ. Entomol. 49: 789, 1956.
  37. Watson, Proc. R. Soc., B. 133: 200, 1946.
  38. Watson, Heathcote, Lauckner & Sowray, Ann. appl. Biol. 81: 181, 1975.
  39. Yamashita, Ohki, Doi & Yora, Ann. phytopath. Soc. Japan 42: 382, 1976.
  40. Yamashita, Doi, Yora & Yoshino, Ann. phytopath. Soc. Japan 45: 484, 1979.
  41. Esau & Hoefert, J. Ultrastruct. Res. 75: 326, 1981.