184
September 1977
Family: Virgaviridae
Genus: Tobamovirus
Species:
Acronym:


Tobamovirus group

A. J. Gibbs
Research School of Biological Sciences, Australian National University, Canberra, Australia

Contents

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

Type Member

Tobacco mosaic virus

Main Characteristics

Particles of most tobamoviruses are straight tubes about 300 x 18 nm, sedimenting at around 190 S. Each particle is constructed of c. 2000 protein subunits of a single protein species (M. Wt c. 1.8 x 104) arranged as a helix (pitch c. 2.3 nm) enclosing the genome, which is a single molecule of single-stranded RNA (M. Wt c. 2.0 x 106) and constitutes c. 5% of the particle weight. Tobamoviruses with particles of this type have thermal inactivation points c. 90°C, survive in sap for many years, and occur in sap at concentrations up to 10 g/l. Most have wide host ranges among angiosperms, and cause mottles and mosaics. They may be transmitted by inoculation with sap, or by contact with infected plants or contaminated soil, and are sometimes carried on seed, but no efficient and specific vectors are known. Tobamovirus particles are found in the cytoplasm and sometimes in the chloroplasts of cells of all tissues (except perhaps embryos) where they may form elongated (paracrystalline) or plate-shaped (crystalline) inclusions; together with various cell constituents, they may form amorphous inclusions.

Other tobamoviruses and tobamo-like viruses with particles of similar morphology have less stable particles of two or more modal lengths. These viruses have more limited host ranges, and some are transmitted efficiently by root-infecting plasmodiophoromycete fungi in which they persist for long periods.

Members

Table 1 lists the definitive and tentative members of the group together with some of their properties.

Table 1 Definitive and tentative members of the tobamovirus group

    Description
No. or ref.
Particle
length(s)
(nm)
RNA M.Wt
(x 10-6)
Coat
protein
M.Wt
(x 10-4)
Amino
acid
residues/
subunit
 Stability* Natural vector
 
A. DEFINITIVE MEMBERS
Tobacco mosaic virus (TMV)   151 300 2.05 1.75 158 + + + unknown
Cucumber green mottle mosaic virus (CGMMV)   154 300 - 1.71 160 + + + unknown
Cucumber virus 4 (CV4)   154 300 - 1.70 158 + + + unknown
Frangipani virus (FV)   196 (a) c. 300 - - - + + + unknown
Odontoglossum ringspot virus (ORSV)   155 300 - 1.76 157 + + + unknown
Ribgrass mosaic virus (HRV)   152 300 c. 2.0 1.75 156 + + + unknown
Sammons' opuntia virus (SOV)   (b) 300 c. 2.0 c. 1.75 - + + + unknown
Sunn-hemp mosaic virus (SHMV)   153 300; 40 2.0; 0.3 1.81 161 + + + unknown
U2 - tobacco mosaic virus (T2MV)   351 (c) 300 2.0 1.75 158 + + + unknown
Tomato mosaic virus (ToMV)   156 300 c. 2.0 1.76 158 + + + unknown
 
B. TENTATIVE MEMBERS
Beet necrotic yellow vein virus (BNYVV)   144 (d) 390; 265; c.100 2.3; 1.8; 0.7 2.1 197 ++ Polymyxa betae
Chara corallina virus (CCV)   (e) 532 3.6 1.75 c. 170 + unknown
Nicotiana velutina mosaic virus (NVMV)   189 (f) 100-175; c.290 - 2.14 - + unknown
Peanut clump virus (PCV)   235 (g) 245; 190 - - - + unknown
Potato mop-top virus (PMTV)   138 250-300; 100-150 - 1.98 - + + Spongospora subterranea
Soil-borne wheat mosaic virus (SBWMV)   77 300;
110-160
2.0; 1.0 - - + Polymyxa graminis

(a) Francki, Zaitlin & Grivell, 1971, (b) Sammons & Chessin, 1961, (c) Siegel & Wildman, 1954, (d) Putz, 1977, (e) Skotnicki et al., 1976b, (f) Randles et al., 1976, (g) Thouvenel et al., 1976

*Stability: T.I.P. L.I.V.
+ + + > 85° decades
++ 70° -85° days
+ < 70° hours

Geographical Distribution etc

The definitive tobamoviruses are widespread and found in all parts of the world where their crop and weed hosts grow. Most of the tentative tobamoviruses have a more restricted distribution, which, for those with soil-borne fungus vectors, reflects the distribution of the vector.

Association with Vectors

No natural specific vectors are known for the definitive tobamoviruses; some have been transmitted experimentally by insects, probably on contaminated feet or mouthparts. Three of the tentative tobamoviruses are specifically transmitted by three different, but related, plasmodiophoromycete fungi; infection occurs when virus-carrying zoospores enter plant roots. These fungi acquire the virus while parasitizing virus-infected roots, and their zoospores apparently carry the viruses internally; zoospores that are merely exposed to surface contamination by virus suspensions fail to transmit. Virus can be carried in the air-dry resting spores of the fungi for several years (Desc. 77, 138 & 144), but it is not known whether the viruses replicate in the fungi.

Ecology

The definitive tobamoviruses are most widespread in crop and weed plants that are frequently handled by man or machines, because they are very infectious and readily spread by contact between infected and healthy plants. They are probably disseminated over greater distances in infected planting material and seed. Little is known about their ecology in nature.

The fungus-transmitted tobamoviruses often occur in patches in crops, reflecting the distribution of the vector; there is no evidence of spread by contact. These viruses cause obvious symptoms in the aerial parts of infected plants in cool weather.

PCV is soil-borne and probably has a fungus vector (Thouvenel et al., 1976). The well developed propensity of NVMV for seed transmission may be an adaptation to its host’s semi-arid environment (Randles et al., 1976).

Relations with Cells and Tissues

The tobamoviruses probably invade all parts of infected plants, some even the pollen and embryos. Plants show symptoms of similar severity whether recently infected or infected for a long time; there is no ‘recovery’. In contrast with many other viruses, mature leaves of plants are more susceptible than young leaves to TMV infection.

Tobamovirus particles are found mainly in the cytoplasm, but also in cell organelles. The particles often aggregate to form inclusions. Most commonly these are crystalline plates, often hexagonal, with the particles aligned perpendicularly to the plane of the plate; sometimes they are long paracrystalline fibres of aligned particles. Cell constituents may also aggregate with or without virus particles to form amoeboid inclusions or X-bodies.

Probably the uncoated genome RNA of TMV can spread from cell to cell through plasmodesmata; intact particles can spread through the phloem but whether they can also spread through plasmodesmata is unknown (Gibbs, 1976). The pattern of systemic invasion of test plants by PMTV suggests that it may only spread through plasmodesmata (Desc. 138).

Virus-like particles have been seen in Polymyxa betae zoospores carrying BNYVV (Desc. 144).

Particle Properties

Particles of definitive tobamoviruses contain a single species of protein, of 1.70-1.80 x 104 daltons (156-161 amino acid residues). The structure of TMV protein is known in detail (Champness et al., 1976). Each TMV particle contains c. 2130 protein subunits closely packed by hydrophobic bonds into a rigid tube 300 nm long with internal and external diameters of 4 nm and 18 nm. The tube is helically constructed with 16 1/3 subunits/turn and a right-handed basic pitch of 2.3 nm (Finch, 1972). The single-stranded genome RNA (2 x 106 M. Wt) is tightly bound into the basic helix of the particle at a radius of c. 4 nm and with three nucleotides associated with each protein sub-unit (Stubbs et al., 1977). The end of the particle containing the 3' end of the genome is convex in outline, the other end concave (Wilson et al., 1976).

The particles may be disassembled and reassembled into infective particles or stacked discs of protein subunits (Durham et al., 1971); the double disc of protein seems an important intermediate in assembly, which starts at a specific site on the genome near, but not at, the 3' terminus (Butler et al., 1977).

Preparations of definitive tobamoviruses contain some particles less than 300 nm long. These particles contain viral messenger RNAs, notably the coat protein messenger, which in SHMV preparations is in 40 nm long particles (Higgins et al., 1976; Beachy & Zaitlin, 1977).

Most of the tentative tobamoviruses have particles of more than one modal length, but it is not known whether these viruses have a divided genome. The particles have a morphology that closely resembles that of the definitive tobamoviruses, but their basic pitch is greater (2.5-2.9 nm) perhaps because their proteins are larger (up to 2.1 x 104 M. Wt), and they are much less stable.

Genome Properties

The definitive tobamoviruses each have a genome consisting of a single molecule of single-stranded RNA of M. Wt c. 2.0 x 106 and, except for CV4, having molar base ratios within 2% of G 25.2: A 29.2:C 18.9:U 26.8; the genome of CV4 consistently differs in having A 26.0 and U 29.2.

TMV genome RNA terminates at the 5' end in a guanosine residue and the 5' position of this residue is linked by a triphosphate group to the 5' position of 7-methyl-guanosine; this structure, which is found in most eukaryote mRNAs, is required for infectivity (Ohno et al., 1976). The 3' end of the TMV genome has the sequence Cp Cp Cp A-OH; it will accept and bind histidine in the presence of amino acyl-tRNA ligase (Litvak et al., 1973). The ‘origin’ for particle reassembly is c. 925 nucleotides, and the start of the coat protein gene c. 750 nucleotides, from the 3' end of the genome (Zimmern & Wilson, 1976; Hunter et al., 1976).

Replication

The site of TMV genome replication is uncertain. Some experiments suggest that the nucleus and, especially, the nucleolus are involved, perhaps, in the early stages of transcription (Smith & Schlegel, 1965; Machida & Kiho, 1970); others suggest that cytoplasmic membranes are involved (Ralph et al., 1971; Zaitlin et al., 1973; Nilsson-Tillgren et al., 1974). The coat protein is probably not translated directly from the genome RNA, but from a specific mRNA (c. 0.3 x 106 M. Wt); this and other viral mRNAs may be assembled into particles shorter than 300 nm (Skotnicki et al., 1976a; Beachy & Zaitlin, 1977). The coat protein mRNA is probably translated on cytoplasmic ribosomes (Zaitlin et al., 1968).

Relationships within the Taxon

The definitive tobamoviruses are most conveniently and usefully grouped by the amino acid composition of their coat proteins.

Table 2. Number of amino acid residues per subunit of coat protein*

No. of
isolates
in cluster
TMV† CGMMV CV4 FV ORSV HRV SOV SHMV T2MV ToMV BNYVV CCV
19 2 7 1 3 2 1 1 7 32 1 1
                         
ala 14,13-15 21 20,19 14 11 18,17 12 12 18,17 11,12 19 14
arg 11,10-12 8 10,9 11 10 10,11 8 12 8 9,8-10 10 8
asp 18,17-19 20,21 17,18-20 17 20 17,16 12 18 22 18,17-19 24 25
cys 1 0 0 1 1 1 1 0 1 1,0 0 N.D.
glu 16,15-18 10 10 16 15 22,21 12 16 16 19,18-21 14 15
gly 6,5-8 9 5,6 9 7 4,3 5 4 4,5 6,7 14 12
his 0,1 1 0 1 0 1 0 1 0 0 2 1
ile 8,9 7 6-7 11 8,9 8,7 7 10 8 7,6-8 5 6
leu 12,12-14 18 12-14 13 14 11,12 12 15 11 13,12-14 19 12
lys 2,3 4 4,3-5 4 1 2 4 1 1 2 12 10
met 0,1 0 0 0 3 3,4 1 0 2 1 7 3
phe 8,9 9 11 7 7 6,5 6 6 8 8,7-10 6 14
pro 8,9 6 9,8-10 4 9 8,9 6 8 10 8,9 10 9
ser 16,13-17 24 21-24 14 12 13,16 9 18 10 15,13-16 18 15
thr 16,14-17 10 12,10-11 13 21 13 11 19 19 16,14-17 15 14
trp 3 2 1 5 3 2,3 N.D. 1 2 3 4 N.D.
tyr 4,5 4 4 5 6,5 7 5 8 6 5,4-6 4 4
val 14,13-15 7 14,12 13 9,10 10 9 12 12 15,14-18 14 8
                         
Total
Residues
in protein
158 160,161 c. 158 158 157,158 156,158 N.D. 161 158 158 197 N.D.

* The most common number; other numbers, if found, are given in italics
N.D. Not determined
† Viruses are arranged in the same order as in Table 1

The computed relationships of these groups are shown in Fig.1, and the relatedness of individual viruses within and between groups correlates well with their serological specificity (Fig.2), coat protein primary structure, cross-protection behaviour, and the host from which they were first isolated (Gibbs & Harrison, 1976). Fig.1 and Fig.2 show that the three clusters of tobamoviruses from solanaceous plants (TMV, ToMV and T2MV) are closely related to, but distinct from, one another. They are close to ORSV and more distantly related to SHMV and HRV. The other definitive tobamoviruses are even more distantly related to one another, with the cucurbit tobamoviruses most distant both from the other viruses and from each other.

Notes on Tentative Members

Of the tentative members, CCV seems closest to the definitive members. Its particles have one modal length, and are of a similar composition and structure to those of the definitive tobamoviruses, and they are distantly serologically related to particles of TMV and ORSV (Gibbs et al., 1975; Skotnicki et al., 1976b).

BNYVV, PMTV, SBWMV, and probably also PCV and NVMV are closely related to one another both in the properties of their particles, and also by their pathology, ecology and vector relations. They probably form a coherent subgroup of the tobamoviruses; indeed the particles of PMTV and SBWMV are serologically related (Randles et al., 1976). Particles of PMTV and SBWMV also are distantly serologically related to TMV particles (Kassanis et al., 1972; Powell, 1976).

Affinities with Other Groups

No well-characterized viruses have close affinities with the tobamoviruses. Some have superficially similar particles (e.g. the tobraviruses), but these differ greatly in particle composition and structure, and in biology and ecology.

References

  1. Beachy & Zaitlin, Virology 81: 168, 1977.
  2. Butler, Finch & Zimmern, Nature, Lond. 265: 217, 1977.
  3. Champness, Bloomer, Bricogne, Butler & Klug, Nature, Lond. 259: 20, 1976.
  4. Chessin, Zaitlin & Solberg, Phytopathology 57: 542, 1967.
  5. Durham, Finch & Klug, Nature New Biol. 229: 37, 1971.
  6. Finch, J. molec. Biol. 66: 291, 1972.
  7. Francki, Zaitlin & Grivell, Aust. J. Biol. Sci. 24: 815, 1971.
  8. Gibbs, in Intercellular communication in plants: studies on plasmodesmata, p.149, ed. B. E. S. Gunning & A. W. Robards, Springer-Verlag, 1976.
  9. Gibbs & Harrison, Plant virology; the principles, London: Arnold, 292 pp., 1976.
  10. Gibbs, Skotnicki, Gardiner, Walker & Hollings, Virology 64: 571, 1975.
  11. Gower, Biometrika 53: 325, 1966.
  12. Gower, The Statistician 17: 13, 1967.
  13. Hariharasubramanian, Smith & Zaitlin, Virology 55: 202, 1973.
  14. Higgins, Goodwin & Whitfeld, Virology 71: 486, 1976.
  15. Hunter, Hunt, Knowland & Zimmern, Nature, Lond. 260: 759, 1976.
  16. Kado, van Regenmortel & Knight, Virology 34: 17, 1968.
  17. Kassanis, Woods & White, J. gen. Virol. 14: 123, 1972.
  18. Kurachi, Funatsu, Funatsu & Hidaka, Agr. Biol. Chem. 36: 1109, 1972.
  19. Lance & Williams, Aust. Comput. J. 1: 15, 1967a.
  20. Lance & Williams, Comput. J. 9: 373, 1967b.
  21. Linnasalmi & Toiviainen, Annls Agric. Fenn. Phytopath. 13: 79, 1974.
  22. Litvak, Tarrago, Tarrago-Litvak & Allende, Nature New Biol. 241: 88, 1973.
  23. Machido & Kiho, Jap. J. Microbiol. 14: 144, 1970.
  24. Mosch, Huttinga & Rast, Neth. J. Pl. Path. 79: 104, 1973.
  25. Nilsson-Tillgren, Kielland-Brandt & Bekke, Molec. gen. Genetics 128: 157, 1974.
  26. Nozu, Tochihara, Komuro & Okada, Virology 45: 577, 1971.
  27. Ohno, Okada, Shimotohno, Miura, Shinshi, Miwa & Sugimura, FEBS Lett. 67: 209, 1976.
  28. Powell, Virology 71: 453, 1976.
  29. Putz, J. gen. Virol. 35: 397, 1977.
  30. Ralph, Bullivant & Wojcik, Virology 43: 713, 1971.
  31. Randles, Harrison & Roberts, Ann. appl. Biol. 84: 193, 1976.
  32. Rombauts & Fraenkel-Conrat, Biochem. 7: 3334, 1968.
  33. Sammons & Chessin, Nature, Lond. 191: 517, 1961.
  34. Siegel & Wildman, Phytopathology 44: 277, 1954.
  35. Skotnicki, Gibbs & Shaw, Intervirology 7: 256, 1976a.
  36. Skotnicki, Gibbs & Wrigley, Virology 75: 457, 1976b.
  37. Smith & Schlegel, Virology 26: 180, 1965.
  38. Stubbs, Warren & Holmes, Nature, Lond. 267: 216, 1977.
  39. Thouvenel, Dollet & Fauquet, Ann. appl. Biol. 84: 311, 1976.
  40. Tsugita, J. molec. Biol. 5: 293, 1962.
  41. Tung & Knight, Virology 48: 574, 1972.
  42. van Regenmortel, Virology 31: 467, 1967.
  43. van Regenmortel, Virology 64: 415, 1975.
  44. Wang & Knight, Virology 31: 101, 1967.
  45. Wilson, Perham, Finch & Butler, FEBS Lett. 64: 285, 1976.
  46. Zaitlin, Duda & Petti, Virology 53: 300, 1973.
  47. Zaitlin, Spencer & Whitfeld, in Biochemical regulation in diseased plants or injury, p.91, ed. T. Hirai, Z. Hidaka & I. Uritani, Tokyo: Phytopath. Soc. of Japan, 1968.
  48. Zimmern & Wilson, FEBS Lett. 71: 294, 1976.


Figure 1

Diagram illustrating a principal co-ordinates analysis (Gower, 1966; 1967) of the definitive tobamoviruses computed from the amino acid compositions of their coat proteins. Analyses for 75 isolates were classified (MULTCLAS program using Euclidean metric; Lance & Williams, 1967a, b) and fell into 10 clusters or individuals. The mean compositions of these clusters or individuals were then used to compute similarity measures whose principal co-ordinates were calculated. The cluster called TMV contained 19 isolates (type, 01, 03, 04, 05, 06, 0M, M, J14D1, YA, GA, Mosch 6 & 19, Mutant 470 & 483, PM1D, PM21B, PM4A, PM4C), the CGMMV cluster 2 isolates (CGMMV, CV3 Jap), the CV4 cluster 7 isolates (4 of CV4, CV3 Berk, CV4 Czech, CV4 Berk), the ORSV cluster 3 isolates (ORSV, 02, 07), the HRV cluster 2 isolates (HRV, Lychnis), the T2MV cluster 7 isolates (U2, G-TAMV, HNO2 262 & 328, P0249, NBSI 206 & 223), and the ToMV cluster 32 isolates (Y-TAMV, dahlemense, NBSI331, Mosch 1-5, 7-10 & 12-18, VC6O, VC61, AC9, HD, SJ, VEN, Aus-11, Dut-1, YLGP, K-1, PTA, PTV, SAF). The sources of data were Chessin et al., 1967; Desc. 153; Francki et al., 1971; Hariharasubramanian et al., 1973; Kado et al., 1968; Kurachi et al., 1972; Linnasalmi & Toiviainen, 1974; S. J. Morris, pers. comm.; Mosch et al., 1973; Nozu et al., 1971; Rombauts & Fraenkel-Conrat, 1968; Tsugita, 1962; Tung & Knight, 1972; van Regenmortel, 1967; and Wang & Knight, 1967.

The relative positions of the ‘individuals’ in the third dimension of the ordination are indicated by their sizes. The first dimension contains 32% of the ‘comparative information’ of the ordination, the second contains 21% and the third 20%; altogether 73%.

Figure 2

Diagram illustrating an ordination of the serological differentiation indices (SDI’s) in Table 2 of van Regenmortel (1975); the SDI between HRV and CGMMV was taken as 6.5 (M. H. V. van Regenmortel, pers. comm.). The first dimension contains 43% of the ‘information’ in the ordination, the second 28% and the third 18%; altogether 89%.