Alfalfa mosaic virus
E. M. J. Jaspars
Department of Biochemistry, State University, Leiden, Netherlands
Institute for Phytopathological Research, Wageningen, Netherlands
Described by Weimer (1931,
Bancroft & Kaesberg (1958,
- Lucerne mosaic virus (Rev. appl. Mycol. 24: 513)
- Alfalfa virus 1 and 2 (Rev. appl. Mycol. 13: 488)
- Marmor medicaginis (Rev. appl. Mycol. 28: 514)
A virus with bacilliform particles of different lengths, the largest usually
c. 60 nm, in
which four species of single-stranded RNA of messenger polarity are separately packaged. The three
largest RNA species comprise the genome; the fourth is a sub-genomic messenger for the coat protein.
The three genome RNA species and either the fourth RNA or the coat protein are needed for infectivity.
The virus is readily sap-transmissible, is seed-transmissible in some hosts and is transmitted in the
non-persistent manner by aphids to a very wide range of host plants. Common in most countries.
Causes various mosaics, mottles and malformations in lucerne (alfalfa; Medicago sativa
but is often symptomless in this host, especially during summer, and is most prevalent in
old crops. Causes calico and tuber necrosis in potato, various symptoms in tobacco and garden lupin,
mosaic in Malva parviflora
and Viburnum opulus,
yellow fleck in Caryopteris incana,
white mottle in Philadelphus
sp. and is one of the causes of mosaic in red and white clover,
celery, celeriac and lettuce, of yellow mosaic in bean (Phaseolus vulgaris
), cowpea (Vigna
), mung bean (V. radiata
) and chilli pepper (Capsicum annuum
of necrosis and stunting in pea (Pisum sativum
), of severe necrosis in tomato, and of wilting
in chickpea (Cicer arietinum
). It occurs naturally in many wild and cultivated species. In
lucerne and clovers, crop yield is often reduced and predisposition to drought and winter injury
Host Range and Symptomatology
Occurs naturally and often symptomlessly in many herbaceous and some woody hosts (150 species in
Schmelzer, Schmidt & Beczner, 1973
It is transmissible to over 430 species of 51
Crill, Hagedorn & Hanson, 1970
Schmelzer et al., 1973
Sap transmission is easy between most hosts, but may be difficult between some e.g.
from lucerne to Phaseolus
beans during summer. Symptoms depend greatly on virus strain,
host variety and stage of growth, and environmental conditions. Infection may be latent or masked
and recovery often occurs. In many species mottle or mosaic is bright yellow (calico); local and
systemic necrosis may also occur.
- Chenopodium amaranticolor and C. quinoa. Chlorotic or necrotic local lesions; the
characteristic systemic chlorotic and necrotic flecking distinguishes
alfalfa mosaic virus from cucumber mosaic virus.
- Nicotiana tabacum (tobacco). Necrotic or chlorotic local lesions
(Fig.4). Some strains
give no local reaction. Systemic symptoms usually are mild mottle, bright chlorotic vein banding,
(Fig.5) and, rarely, deformation
(Fig.6). Plants commonly recover
Enations are induced by some strains.
- Ocimum basilicum (basil). Systemic yellow mosaic.
- Phaseolus vulgaris (French bean). Many strains of the virus give necrotic local lesions
sometimes coalescing, which appear in 3 to 5 days in most cultivars; other strains produce
chlorotic local lesions or none at all but give systemic mild mottle, vein necrosis and leaf distortion.
- Pisum sativum (pea). In most cultivars local lesions and/or wilting of inoculated leaves
with stem necrosis and plant death.
- Vicia faba (broad bean). Most strains give black necrotic local lesions, sometimes
followed by a mild mottle, but more often by stem necrosis and plant death.
- Vigna unguiculata (cowpea). The commonest strains produce necrotic local lesions and do
not infect systemically; others do not induce local lesions but produce various systemic symptoms.
- Nicotiana tabacum and N. glutinosa are suitable for maintaining cultures. N.
tabacum cultivars, especially those hypersensitive to
tobacco mosaic virus (e.g.
Samsun NN), are good sources of virus for purification. It should be noted that virus
concentration in tobacco soon reaches a high peak but rapidly declines thereafter to a very
low level, and this loss of virus coincides with recovery from symptoms
(Ross, 1941). Peak virus
concentration and the time needed to reach it are influenced by inoculum dose
- Phaseolus vulgaris and Vigna unguiculata are good assay hosts for strains that
produce local lesions in these plants. Chenopodium amaranticolor and C. quinoa
are also suitable.
Numerous strains or variants with minor differences have been described. Distinction is
mainly by differential reaction on one or two selected hosts (notably Phaseolus vulgaris
and Vigna unguiculata
) and by differences in such properties as particle aggregation
forms in tobacco cytoplasm, pollen and seed transmission and physico-chemical properties. Most
molecular biological research has been done with strain AMV-S originating from lucerne
(Gibbs & Tinsley, 1961
strain AMV 425 isolated from clover
(Hagedorn & Hanson, 1963
alfalfa yellow spot mosaic strain of
and strains AMV 15/64 and VRU of
Symptomatologically different strains do not necessarily differ in amino
acid composition and serological behaviour
(Tremaine & Stace-Smith, 1969
). A grouping of
strains on the basis of the chemical properties of the coat proteins has been proposed by
Transmission by Vectors
Transmitted in the non-persistent manner by at least 14 aphid species
(Crill et al., 1970
There is no latent period in the aphid and frequency of transmission is increased
by starving the aphids before acquisition of virus
). Myzus persicae
acquire the virus from purified preparations through Parafilm membranes
Transmission through Seed
Presumably common in lucerne
Hemmati & McLean, 1977
); reported up
10% in commercial seed
(Beczner & Manninger, 1975
Hemmati & McLean, 1977
and up to c.
50% in seeds from individual infected plants (55%:
Zschau & Janke, 1962
Beczner & Manninger, 1975
with rates of transmission depending on virus strain and lucerne cultivar or clone
Beczner & Manninger, 1975
). More seed infection
occurs through pollen than through ovules
Hemmati & McLean, 1977
Frequency of transmission in lucerne seed is not decreased by storage
transmission of 1-5% occurs in chilli pepper
) and of 23% in Nicandra physalodes
(Gallo & Ciampor, 1977
Transmission by Dodder
Occurs in at least five Cuscuta
Moderately immunogenic, giving antibody titres of 1/1024
(Bancroft et al., 1960
The variously sized intact particles of the virus are serologically indistinguishable. The yellow
spot mosaic and 425 strains differ sufficiently from each other for spurs to form in agar gel
(Van Vloten-Doting, Kruseman & Jaspars, 1968
). In the ring interface
precipitin test, strains differing widely in pathogenicity and geographical origin behaved as
though closely related
(Bancroft et al., 1960
No serological relationship to any other virus has been found. The tripartite genome and the
presence of the coat protein messenger RNA in the particles (see Particle Composition) suggest a
phylogenetic relationship with the bromo-
cucumoviruses, which have isometric particles all
of one size, and with ilarviruses
tobacco streak virus
citrus leaf rugose virus
have isometric particles of several sizes. The coat proteins of alfalfa mosaic virus and some
ilarviruses are needed for infectivity and can reciprocally activate each others genomes
(Van Vloten-Doting & Jaspars, 1977
Indeed, some workers
(Lister & Saksena, 1976
Gonsalves & Fulton, 1977
have suggested that alfalfa mosaic virus should be included in the ilarvirus
group. The bacilliform particles of alfalfa mosaic virus have some resemblance to those of a
of a mycoplasma virus
(Gourlay, Bruce & Garwes, 1971
cacao swollen shoot
(Brunt, Kenten & Nixon, 1964
mottle leaf viruses
(Kenten & Legg, 1967
), and of
rubus yellow net virus
(Jones & Roberts, 1976
Bacilliform particles have also been observed in preparations of some ilarviruses
(Halk & Fulton, 1978
Stability in Sap
The thermal inactivation point is usually between 60 and 65°C, but may range between 50
and 70°C, the dilution end-point is mostly between 10-3
is sometimes higher, and the longevity in vitro
is usually 1 to 4 days but sometimes
considerably longer. Infectivity in sap seems to be best retained at pH 7.0 to 7.5 and phosphate
buffers (0.01 to 0.1 M) are used for leaf extraction. Particles are degraded in phosphotungstate
stains for electron microscopy except at pH 3 to 4
(Milne & Masenga, 1978
Modifications of Steeres butanol/chloroform method are mostly used
(Van Vloten-Doting & Jaspars, 1972
and yield up to 1.5 g virus per kg leaf tissue. Some preparations contain ribosomal
material. Alternatively, the virus may be precipitated directly from the sap with polyethylene
glycol, M.Wt 20,000, in 0.2 M NaCl
The virus components are separated by differential precipitation in 0.03 M MgSO4, and
by centrifugation in sucrose gradients
(Van Vloten-Doting & Jaspars, 1972), or by differential
solubilization of a polyethylene glycol precipitate
(Clark, 1968). Biological activity of purified
components often decreases rapidly, but can be stabilized by ethylenediamine-tetraacetate (0.001 M).
Infective preparations of the RNA are best prepared by phenol extraction of the virus in 0.01 M
phosphate buffer containing 1% sodium dodecyl sulphate or 2% sodium pyrophosphate. Infectivity of
unfractionated RNA, assayed on Phaseolus vulgaris, is about 1% of that of intact virus.
A convenient way to isolate the protein is to dissociate the virus in 0.5 M MgCl2; the
RNA precipitates, and the supernatant fluid, after dialysis against 0.05 M acetate buffer,
pH 5.5, contains the protein in dimer form
(Kruseman et al., 1971).
Properties of Particles
Analytical ultracentrifugation of purified preparations reveals up to six components
(Bancroft & Kaesberg, 1960
consisting of bacilliform particles of different lengths
(Gibbs, Nixon & Woods, 1963
The three larger, obviously bacilliform, components
) are essential
for infection and, in order of decreasing size, are named bottom (B), middle (M), and top b
(Tb). The two or three spheroidal accessory top components (Ta, To, and Tz) are not infective,
singly or together, and cannot replace the function of any of the three larger components of the
(Van Vloten-Doting, Dingjan-Versteegh & Jaspars, 1970
by a mixture of the functional components of two virus strains give pseudo-recombinant strains
with properties of both parents. The relative amounts of the components depend on the virus strain
and on the growing conditions.
Sedimentation coefficients (svedbergs) at infinite dilution: 94 (B), 82 (M), 73 (Tb), 66 (Ta), c.
60 (To) and c. 53 (Tz).
Molecular weights: 6.9 x 106 (B), 5.2 x 106 (M), 4.3 x 106 (Tb),
3.8 x 106 (Ta).
Electrophoretic mobility: -6.6 x 10-5 cm2 sec-1 volt-1 at
pH 7 and 0.1 ionic strength. The virus migrates as a single component, but in sieving media such as
3% polyacrylamide gel it is resolved into at least 17 components. The RNA contributes to the surface
(Bol & Veldstra, 1969).
The virus is precipitated below pH 6. Above pH 4, precipitates
retain infectivity for at least a few hours at 4°C.
A260/A280: 1.7-1.8 (B, M, Tb, Ta and probably also the other components).
Absorbance at 260 nm (1 mg/ml, 1 cm light path): 5.1 (B), 4.8 (M and Tb), 4.7 (Ta).
Partial specific volume: 0.703 (B, Ta and probably also the other components).
Buoyant density in Cs2SO4 (fixation with formaldehyde is unnecessary): mean
for all components 1.278 g/cm3. Density of the components increases slightly with
increasing size (Hull, 1976).
The virus nucleoprotein particles are mainly stabilized by protein-RNA interactions. They are
sensitive to low concentrations of sodium dodecyl sulphate
(Kaper, 1973), to pancreatic ribonuclease
(Pirone, 1962) and trypsin
(Bol, Kraal & Brederode, 1974). In the presence of ribonuclease the
particles lose RNA fragments and ultimately degrade to smaller structures
(Bol & Veldstra, 1969).
Particles undergo a reversible unfolding at slightly alkaline pH. Free RNA is capable of removing
coat protein subunits from intact nucleoprotein particles
(Verhagen et al., 1976). At high
ionic strength (e.g. 1.5 M NaCl, pH 5.5) a partially reversible dissociation occurs
(Bol & Kruseman, 1969).
Nucleoprotein particles have been partially reconstituted from isolated
RNA and protein by
Lebeurier, Wurtz & Hirth (1969) and
The cylindrical part of the bacilliform particles consists of a hexagonal lattice net (angle
of prominent lattice vector with particle axis: 0°; lattice spacing: 4.4 nm). At each end the
6-fold axes of the cylindrical net are probably converted into 5-fold ones giving rise to
icosahedral caps. The coat protein subunits are grouped in dimers at the 2-fold positions of the
so that there are 18 subunits per spacing. The components represent a
series of particles with 60 + (n
being 10 (B), 7 (M), 5 (Tb) and 4 (Ta), respectively
(Heijtink, Houwing & Jaspars, 1977
The smaller components To and Tz may have lower n
values, but most of these particles have an irregular spheroidal shape. Even in Ta the
irregular particles predominate
(Heijtink & Jaspars, 1976
values are probably
represented by minor components observed upon electrophoresis in polyacrylamide gels
(Bol & Lak-Kaashoek, 1974
The lengths (nm) of the purified components (mounted in potassium
phosphotungstate after fixation with formaldehyde) are 56 (B), 43 (M), 35 (Tb) and 30 (bacilliform
Ta). Particles considerably longer than B are abundant in preparations of strain VRU. In crude
preparations of strain 15/64, particles over 1 µm in length have been observed. The diameter
of all particles is about 16 nm. With uranyl acetate as negative stain, fixation is unnecessary.
Particle CompositionNucleic acid:
Four species of single-stranded RNA designated RNA 1 to 4, in order of
decreasing M. Wt. These are separately packaged in components B (RNA 1), M (RNA 2), Tb (RNA 3)
and Ta (2 copies of RNA 4). Minor RNA species of M. Wt intermediate between RNA species 3 and 4
(X-RNA species) or smaller than RNA 4 (Z-RNA species) are found. They are packaged in minor
components and in some of the Tb and Ta particles. Particles longer than B do not contain RNA
species longer than RNA 1, but have combinations of the above RNA species. M. Wt of RNA-anions:
1.04 x 106
, 3250 nucleotides (RNA 1); 0.73 x 106
, 2250 nucleotides (RNA 2).
0.62 x 106
, 1950 nucleotides (RNA 3); and 283 x 103
, 882 nucleotides (RNA 4).
The RNA species represent 16.3% (RNA 1),
15.5% (RNA 2 and RNA 3) and 15.2 to 15.6% (RNA 4) of the weight of the corresponding components.
Sedimentation coefficients (svedbergs) at infinite dilution (solvent: 0. 01 M sodium phosphate,
0.15 M NaCl, pH 7): 25.8 (RNA 1) and 12.7 (RNA 4). Partial specific volumes (Na salts): 0.459
(RNA 1) and 0.470 (RNA 4). Absorbance at 260 nm (1 mg anion/ml, 1 cm light path, 20°C, 0.01
M sodium phosphate, pH 7): 26.3 (RNA 1) and 25.8 (RNA 4)
(Heijtink et al., 1977
percentages of nucleotides: G22.9; A26.8; C20.4; U29.8 for RNA 1
(Rauws, Jaspars & Veldstra, 1964
and G23.9; A24.4; C24.0; U27.7 for RNA 4 (from sequence).
Protein: All components have the same coat protein, which consists of 220 amino acids
in strain 425 (M. Wt 24,280). The amino acid sequence is known for strains 425
(Van Beynum et al., 1977), S
(Collot et al., 1977) and VRU
(Castel et al., 1979). VRU and S
proteins have 219 and 217 amino acids, respectively. The N-terminus is acetylated serine. The
sequence of the 39 N-terminal amino acids is identical in the three strains. Amino acid compositions
of the coat proteins of several strains were compared by
Kraal (1975) and protein polymerization
behaviour was studied by
Driedonks, Krijgsman & Mellema (1977,
1978). Absorbance of protein
preparations at 280 nm (1 mg/ml, 1 cm light path, 20°C, 0.05 M sodium acetate, pH 5.5,
corrected for light-scattering): 0.70.
All the RNA species are capped by m7
but have no poly(A) tails. No amino acid charging is possible at the 3' ends. RNA species
1, 2 and 3 comprise the complete genome. They share at least 80% sequence homology in the last
150 3'-terminal nucleotides
(Pinck & Pinck, 1979
Koper-Zwarthoff et al., 1979
Gunn & Symons, 1980
RNA species 1 and 2 are possibly monocistronic, coding for proteins of M.
100,000 and c.
80,000 respectively. RNA 3 is dicistronic, coding for a
protein of M. Wt c.
35,000 and for the coat protein
(Mohier et al., 1975
Van Vloten-Doting et al., 1977
RNA 4 is homologous with the 3' half of RNA 3
(Gould & Symons, 1978
Little, if any, coat protein is produced by translation of RNA 3 in vitro
or in vivo,
but RNA 4 is an efficient subgenomic coat protein messenger with a leader
sequence of 40 nucleotides (cap and initiation triplet included)
(Koper-Zwarthoff et al., 1977
The complete nucleotide sequence is known for RNA 4 of strain 425
(Brederode, Koper-Zwarthoff & Bol, 1980
The leader sequence of RNA 4 has
been found to be identical in seven strains (assuming that the cap is the same in all cases),
except for position 27 where G, U or A may occur
(Swinkels & Bol, 1980
The ratio RNA 3/RNA 4 in virus preparations is determined by RNA 3. Symptom markers are carried
by RNA 2 and RNA 3
(Dingjan-Versteegh, Van Vloten-Doting & Jaspars, 1972;
Hartmann et al., 1976).
Mutations affecting the relation between growth and temperature were found to be
carried by all three genome RNA species
(Franck & Hirth, 1976;
Van Vloten-Doting et al., 1980).
Complementation studies with temperature-sensitive mutants suggest that RNA 1 and RNA
2 each possess more than one gene function. The three genome RNA species and either the coat
protein or RNA 4 are needed for infectivity
(Bol, Van Vloten-Doting & Jaspars, 1971).
Preparations of double-stranded RNA which contain molecules that correspond to each of the
genome RNA species have been isolated from infected plants
(Mohier, Pinck & Hirth, 1974;
Bol et al., 1975).
Relations with Cells and Tissues
Transient, amorphous, granular inclusion bodies have been seen by light microscopy in tobacco
Electron microscopy has revealed virus particles within the cytoplasm
of a number of plants, either non-aggregated or in whorls and rafts containing particles packed
side by side
(Hull, Hills & Plaskitt, 1969
De Zoeten & Gaard, 1969
Gerola, Bassi & Betto, 1969
similar rafts occur in the vacuoles of tobacco cells
(Hull et al., 1969
Particles have also been found in cytoplasmic invaginations in the chloroplasts
(Hull, Hills & Plaskitt, 1970
Dingjan-Versteegh, Verkuil & Jaspars, 1974
but not in any organelle, although
chloroplasts of basil showed ultrastructural changes
(Favali & Conti, 1970
Tobacco and cowpea
protoplasts can be infected
(Motoyoshi, Hull & Flack, 1975
Alblas & Bol, 1978
for cowpea protoplasts must have the same composition as that for intact plants (i.e.
genome plus either coat protein or RNA 4). Preparations of membrane-bound and solubilized RNA
polymerase have been obtained from infected tobacco, but it is uncertain whether virus-coded
proteins are involved
(Linthorst, Bol & Jaspars, 1980
In host range, symptoms, vector relations, nature of the genome and in many other properties
alfalfa mosaic virus resembles
cucumber mosaic virus
. The latter, however, has spherical particles,
is independent of coat protein for infection, produces local lesions in Phaseolus vulgaris
only in winter, and most strains do not infect Chenopodium amaranticolor
or C. quinoa
systemically; moreover not all strains of alfalfa mosaic virus infect cucumber.
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Lucerne (alfalfa) with yellow mosaic (above) and vein mosaic (below).
(Courtesy L. Beczner, Budapest.)
Capsicum annuum with mosaic (courtesy L. Beczner).
Phaseolus vulgaris cv. Bataaf, with local lesions of strain 425.
(Photo IPO, Wageningen.)
Lesions of strain 425 in inoculated leaf of Nicotiana tabacum cv. White Burley.
(Photo IPO, Wageningen.)
Systemic symptoms of strain 425 and recovery in N. tabacum cv. White Burley.
(Photo IPO, Wageningen.)
Systemic symptoms of the yellow spot mosaic strain in N. tabacum cv. White Burley.
(Photo Dept. Biochem, State Univ., Leiden.)
Electron micrograph of purified virus preparation, fixed with formaldehyde and mounted
in phosphotungstate. B, bottom component; M, middle component; Tb, top component b. Spheroidal
particles are top components Ta, To or Tz. Bar represents 100 nm. (Courtesy M. Verhoyen and S.
Influence of concentration of inoculum on multiplication of alfalfa mosaic virus in
Nicotiana rustica. (After Verhoyen, 1966)