Barley yellow mosaic virus
M. J. Adams
Plant Pathology Department, IACR-Rothamsted, Harpenden, Herts., AL5 2JQ, UK
Described by Ikata & Kawai (1940)
A virus with slightly flexuous filamentous particles with a diameter of c. 13 nm
and two modal lengths, c. 275 and 550 nm, containing two species of ssRNA.
It is transmitted by the plasmodiophorid fungus Polymyxa graminis and is
sap-transmissible with difficulty. The only host known is barley.
Pinwheel inclusions are formed in the cytoplasm of infected cells.
Barley yellow mosaic virus is one of two agents (the other is barley mild mosaic virus)
that causes yellow mosaic disease of barley. The disease is soil-borne because the viruses
are transmitted by the plasmodiophorid fungus Polymyxa graminis
which has resting spores
that survive in soil. The viruses occur, either separately or together, in autumn-sown barley
and cause similar symptoms. In the field, yellow patches appear in winter or early spring
Leaves of infected plants have elongated, pale green or yellow flecks, typically on the
youngest (unfurling) leaves
and infected leaves may be curled, giving the plants a spiky appearance. Sometimes the leaves
show complete yellowing with necrotic patches and the plants are stunted. Affected plants have
fewer tillers, yield less grain and grain size may be irregular. The severity of symptoms depends
on the cultivar of barley and the environmental conditions but symptoms become less obvious as
the stem elongates towards flowering and upper leaves are often free of symptoms. Patches may
remain visible as areas of stunted growth even when symptoms have apparently disappeared but
plants sometimes appear to recover from infection. Yield losses are difficult to estimate but
values of 40-80% loss in 2-rowed barley in Japan and up to 50% in Europe have been recorded
Proeseler et al., 1988
They depend upon the barley cultivar and winter weather conditions, being greatest on crops
sown early in the autumn and when the autumn is mild but the winter is especially cold
(Kusaba et al., 1971
Widespread in Japan
(Kashiwazaki et al., 1989
), Eastern China
(Chen et al., 1996
and various western European countries, including Belgium
(Froidmont et al., 1993
(Hill & Walpole, 1989
(Hariri et al., 1990
Signoret & Huth, 1993
Proeseler et al., 1991
) and Italy
It has also been reported from Greece
(Katis et al., 1997
), and the Ukraine
(Fantakhun et al., 1987
Omel'chenko et al., 1996
Host Range and Symptomatology
The only host known is Hordeum vulgare
Transmitted through infested soil, and (with difficulty) by inoculation of sap.
The species of plants tested but not infected include Triticum aestivum
(oat), Oryza sativa
(rice), Chenopodium amaranticolor
and Nicotiana tabacum
(tobacco). Hordeum spontaneum
and H. agriocrithon
were susceptible when planted in infested soil
Reports of successful mechanical inoculation of the virus to other species of Hordeum
and to a few other species of the Poaceae
refer to what was then described as a strain of barley yellow mosaic virus but which is
now recognised as barley mild mosaic virus.
Barley (Hordeum vulgare). The virus is transmissible to barley, though not readily,
by inoculation with plant sap and keeping test plants below about 18°C. Optimal results
with Japanese isolates were obtained by inoculating all leaves of seedlings at the 4-5 leaf
stage and growing the plants at 10°C for one week after inoculation
(Inouye et al., 1990).
Increased infectivity was observed when inoculum was made by grinding diseased leaves in
10-3 M KCN, Na-DIECA, or Na-azide
(Takanashi et al., 1967),
(Takahashi et al., 1968),
or 10-4 M p-nitrophenol
(Kusaba et al., 1971).
With European isolates, highly infectious inoculum was found necessary and plants were kept
after inoculation at 10°C (day): 8°C (night)
Barley (Hordeum vulgare).
No local lesion host is known. Where mechanical inoculation is successful, the virus may
be assayed by finding the percentage of Hordeum vulgare plants infected using
different concentrations of inoculum.
Reports from Europe during the period 1980-1990 refer to a strain that is readily
transmissible by mechanical inoculation (BaYMV-M or BaYMV-Streatley). These isolates are
now recognised as a different virus, barley mild mosaic virus
(Huth & Adams, 1990
Six different strains (in three groups) have been identified in Japan based on the response
of differential cultivars: I-1, I-2, I-3, II-1, II-2 and III
(Kashiwazaki et al., 1989).
In Europe, two strains are recognised on the basis of the response of cultivars carrying
the ym4 resistance gene. These cultivars are immune to the common strain but susceptible
to a resistance-breaking strain that is usually named BaYMV-2 and which is becoming
Hariri et al., 1990;
Several strains probably occur in China but these are less well defined
(Chen et al., 1996).
No differences in serological or other properties have been demonstrated between any of
these strains and they are distinguished only by cultivar response.
Transmission by Vectors
Transmitted by the plasmodiophorid fungus Polymyxa graminis
(Kusaba et al., 1971
which is an obligate root parasite. The virus is acquired when the plasmodia of the fungus
are growing inside the barley root cells and it is transmitted within the zoospores
) or resting spores
) that it produces. The virus survives within the resting spores
and infectivity has been retained in air-dried soil for 5-10 years
Transmission through Seed
Not found (Yasu & Yoshino, 1964
The virus is only moderately immunogenic. Serum from a rabbit injected intravenously,
then intramuscularly, with partially purified virus reacted with the virus to a titre of 1/1280
in complement fixation tests
(Usugi & Saito, 1970
ISEM and ELISA are useful for routine diagnosis
Monoclonal antibodies have been prepared
(Hariri et al., 1996a
The different strains of BaYMV have been characterised only by cultivar response and cannot
be distinguished by serological tests. Nucleotide sequencing suggests that the two European strains
are extremely similar
(Shi et al., 1995
and it has not so far proved possible to develop a test to distinguish them.
BaYMV resembles the other members of the genus Bymovirus in transmission by
Polymyxa graminis, in particle morphology and in inducing pinwheel-type inclusions and
characteristic membranous network structures in the cytoplasm of infected plant cells. There is a
close serological relationship to both wheat yellow mosaic and wheat spindle streak mosaic viruses
(Usugi et al., 1989)
but no detectable relationship to the other viruses, including barley mild mosaic virus. The percentages
of amino acids in the coat protein identical to those of the other bymoviruses that have been sequenced
are: 74-76% (WSSMV), 68% (WYMV), 33-34% (BaMMV) and 34% (RNMV)
(Badge et al., 1997;
Namba et al., 1998).
Stability in Sap
The dilution end-point is less than 10-2
(Kusaba et al., 1971
Yasu & Yoshino, 1964
The thermal inactivation point and longevity in vitro
are not known.
Infectivity of dried leaf tissue is retained for two years at 5-10°C
There are several published protocols developed from the procedure of
Usugi & Saito (1970)
The protocol currently in use at IACR-Rothamsted is:
Homogenise 100 g leaf pieces (fresh or powdered in liquid N2 and stored at -70°C)
in 400 ml cold buffer A (0.1M Tri-potassium citrate; 0.01M EDTA di-sodium salt; pH adjusted to 7.0
with KOH if necessary) + 25 ml/l Triton X-100 + 1mM phenylmethylsulfonylfluoride (PMSF; added from
a 50mM stock solution in isopropanol immediately before use) and strain through muslin.
Centrifuge at 15-20,000 g for 15 min at 4°C and retain supernatant.
Centrifuge through a 30% (w/w) sucrose cushion at 98,000 g for 2 hours at 4°C.
Resuspend pellet in cold buffer A + 1mM PMSF. Allow to resuspend for about 1 hour at 4°C then centrifuge
at c. 2,500 g for 10 min at 4°C and retain supernatant.
Dilute with buffer A + 1mM PMSF and repeat centrifugation through sucrose cushion, resuspend and low
speed spin as before. Mix with CsCl (5.15 ml preparation + 2.85 ml stock 60% (w/w) CsCl solution for
each 10 ml tube), centrifuge at 84,000 g overnight (16-17 hours) at 4°C and collect the
light-scattering virus band using a bent needle and syringe. Dilute 10-20 fold in buffer A and collect
by centrifugation at 67,500 g for 4 hours at 4°C.
Properties of Particles
Buoyant density in CsCl: 1.321 to 1.349 g/cm3
Particle weights 2.8 x 106 (RNA1) and 1.4 x 106 daltons (RNA2)
A260/A280: 1.14 (not corrected for light-scattering).
) of barley yellow mosaic virus are slightly flexuous
filaments 13 nm in diameter and having two modal lengths of 275 and 550 nm; both lengths are found in
leaf dips and in partially purified virus preparations
Particle CompositionNucleic acid
: Single-stranded linear RNA in two segments (RNA1, 7630-7645 nucleotides;
RNA2, 3585 nucleotides) comprising about 5 % of particle weight.
Protein: A single coat protein species consisting of 297 amino acids. The mol. wt was
estimated as 33-35 kDa by SDS-polyacrylamide gel electrophoresis, which is slightly larger than that
(32.4 kDa) calculated from the sequence. The coat protein undergoes partial proteolysis during
purification of virus particles
(Ehlers & Paul, 1986;
Kashiwazaki et al., 1989).
Bipartite, positive-sense ssRNA with poly(A) at the 3' terminus and probably with a genome-linked
protein (VPg) at the 5' terminus. There is no extensive nucleotide sequence homology between RNA1 and
RNA2 except for the 5' non-coding regions
(Kashiwazaki et al., 1991
Complete nucleotide sequences have been determined for the genomes of Japanese
D01092, RNA2) German
D01099, RNA2) and Chinese
AJ132269, RNA2) isolates. Nucleotide sequences have also been reported for the 3'-terminus
(including the coat protein gene) of RNA1 of a UK isolate
(Z24677) and for the coat protein coding region of three UK
(X95695-X95697) and 10 Chinese isolates
(AJ224619-AJ224628). Partial sequences for a region at the 5'-end of the P2 region of RNA2 have
been reported for one German BaYMV-2 isolate
(X69836), 3 UK isolates
(X95698-X95700) and 10 Chinese isolates
The organisation of the genome is shown in Fig.7.
RNA1 consists of 7632-7643 nucleotides, excluding the 3' poly(A), and encodes a single large
polyprotein of 2410-2412 amino acids (271 kDa). Its organisation resembles the 3'-terminal three
quarters of the monopartite genome of potyviruses
(Kashiwazaki et al., 1990;
Peerenboom et al., 1992)
with the coat protein at the C-terminus and at least five, and probably seven, putative
non-structural proteins which have been identified by sequence alignments and motif comparisons
(Table 1). The NIa-Pro probably acts as a proteinase to catalyse cleavage of the polyprotein at the
QX or EX dipeptides indicated in
Fig.7, to give rise to the functional proteins.
Table 1. Protein products of RNA1 of barley yellow mosaic virus
|7K||7|| ||Unknown: analogous to Potyvirus 6K1|
|CI||74||Cylindrical inclusion protein||NTP-binding motif (helicase)|
|14K||14|| ||Unknown: analogous to Potyvirus 6K2|
|NIa-VPg||22||Nuclear inclusion protein||Genome-linked protein|
|NIa-Pro||25||Nuclear inclusion protein||Serine-like protease |
|NIb||60||Nuclear inclusion protein||RNA-dependent RNA polymerase|
|CP||32||Coat protein||Capsid protein|
RNA2 consists of 3585 nucleotides, excluding the 3' poly(A), and encodes a single polyprotein
of 890 amino acids (98.2 kDa) which contains two putative functional proteins
(Davidson et al., 1991;
Kashiwazaki et al., 1991).
P1 (28 kDa) contains a protease domain that corresponds to the helper component proteinase of
potyviruses, and probably cleaves the 98K polyprotein at a GS dipeptide. By analogy with barley mild
mosaic virus, P2 (70 kDa) is probably involved in fungus transmission. Both proteins have been shown to
be associated with inclusion bodies in infected leaf cells
(Schenk et al., 1993).
Japanese and German isolates display 94-95% nucleotide homology. Examination of European
resistance-breaking BaYMV-2 isolates has shown that these are extremely similar to the common isolate:
the crucial difference has yet to be identified but does not occur in the coat protein coding region
(Shi et al., 1995;
Relations with Cells and Tissues
X-bodies can be found in cells of epidermal strips of infected leaves
In ultrathin sections, inclusion bodies of pinwheel-type
), densely packed membranes
), and crystal-like bodies
) can be observed in the cytoplasm
(Saito et al., 1966
Hibino et al., 1981
Schenk et al., 1993
Ecology and Control
Because of its transmission by Polymyxa graminis
, barley yellow mosaic virus is soil-borne.
It survives within the fungus resting spores, which remain within root debris after the crop is
harvested and can persist in soil for many years. No weed hosts of the virus are known and although
some isolates of the fungus may be able to infect other cereals or grass weeds, it is generally
assumed that other hosts play little or no role in the epidemiology of the disease
There is a potential role for spring barley as a symptomless host, but this has never been
demonstrated in the field.
Barley roots become infected in the autumn soon after sowing. The optimum temperature is 13-16ºC
and little infection occurs below about 10ºC
(Kusaba et al., 1971).
The virus remains in the roots until the spring when it seems that re-growth of plants, damaged by
earlier cold weather, causes the plants to mobilise root reserves, thus reversing the normal
downward phloem movement. This translocates virus particles from the roots to the growing leaves
where further virus multiplication results in the typical systemic mosaic symptoms
(Schenk et al., 1995).
The lack of symptoms on leaves produced later in the season may be related to the speed of their growth
or to the higher temperatures that are unfavourable to the virus
(Inouye et al., 1990).
The absence of symptoms on spring-sown barley is probably due to the speed of crop development and
the lack of stimulus to reverse the phloem movement.
Although general soil sterilisation may control the disease
(Saito et al., 1964;
Kusaba et al., 1971)
it is practically difficult and economically unjustified. Other chemical treatments have not
given consistent benefits
(Proeseler and Kastirr, 1988).
The incidence and severity of the disease can be decreased by delaying sowing in the autumn
(Watanabe et al., 1989)
probably because this results in less root infection by the fungus vector before the onset of winter.
The value of delayed sowing as a practical control measure varies between seasons
(Adams et al., unpublished) probably depending upon the autumn weather conditions.
Although the disease is more severe where barley is grown continuously than where it is grown in
a rotation system (one year in three or four)
(Faccini et al., 1995;
Rubies-Autonell et al., 1995),
crop rotation is not widely practised as a control measure.
The principal means of control is the use of resistant varieties, which are available in Europe
and East Asia. These varieties are susceptible to the fungus vector but are immune to the virus.
Several resistance genes have been identified but some of these can be overcome by certain
strains (pathotypes) of the virus or by barley mild mosaic virus. In Europe, the only widely used gene
has been ym4, derived from the Yugoslav landrace Ragusa. It confers resistance to the
common European strain but not to BaYMV-2
(Graner & Bauer, 1993).
It also confers resistance to some, but not all, Chinese strains
(Chen et al., 1996).
In Japan, a wider range of resistance genes have been deployed
(Kashiwazaki et al., 1989;
Iida et al., 1992;
Konishi et al., 1997)
and some of these are now being used by European breeders.
The mosaic viruses are readily distinguished from most other viruses that affect barley by the
mosaic flecking on the youngest leaves. Of those with elongated particles,
soil-borne wheat mosaic virus
and barley stripe mosaic virus
do not usually cause the flecking symptoms, have straight
rod-shaped particles and can be distinguished by serological tests. They also cause local lesions
on inoculated leaves of Chenopodium amaranticolor
or C. quinoa
, which BaYMV does not.
Barley mild mosaic virus
causes identical symptoms to barley yellow mosaic
virus and dual infections can also occur, especially in Europe. The two viruses can only be distinguished
by serological tests (e.g. ELISA). Related, but distinct, mosaic viruses occur on other cereal
crops, causing similar symptoms on oats
(oat mosaic virus
) and wheat
(wheat yellow mosaic and
wheat spindle streak mosaic
viruses) in particular.
Although the wheat bymoviruses have a close serological relationship to BaYMV, the viruses are confined
to their respective cereal hosts.
Publications apparently describing work with BaYMV from Europe in the period 1980-1990 often used
virus isolates that are now recognised as barley mild mosaic virus and this can cause confusion.
In particular, the strain described from Germany as transmissible by mechanical inoculation (BaYMV-M)
and from the UK as the Streatley strain are now recognised as barley mild mosaic virus
(Huth & Adams, 1990).
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Yellow patches in winter barley cv. Panda caused by barley yellow mosaic virus.
Mosaic leaf symptoms on barley (cv. Igri) caused by barley yellow mosaic virus.
Light micrograph of barley root stained with methylene blue, showing plasmodium of
Zoospore suspension of Polymyxa graminis. Main picture shows a light micrograph; inset shows a scanning electron micrograph of a single zoospore. Zoospores are about 4µm in diameter. F = flagellum.
Resting spore clusters of Polymyxa graminis: Main picture shows a light
micrograph of a heavily infected barley root (not stained);
inset shows a scanning electron micrograph of a single cluster.
Individual spores are about 6µm in diameter.
Electron micrograph of particles of barley yellow mosaic virus. Bar represents 100 nm.
Diagram showing the genome organisation of barley yellow mosaic virus.
X-bodies in epidermal cells of barley. N = nucleus; X = X-body.
Electron micrograph of an ultrathin section of infected barley leaf showing pinwheel-type
inclusions. Bar represents 100 nm. Photo courtesy of Prof. H.-H. Steinbiss,
Max Planck Institut für Zuchtungsforschung, Köln, Germany.
Electron micrograph of an ultrathin section of infected barley leaf showing densely packed
membranous inclusions. Bar represents 500 nm. Photo courtesy of Prof. H.-H. Steinbiss,
Max Planck Institut für Zuchtungsforschung, Köln, Germany.
Electron micrograph of an ultrathin section of infected barley leaf, cv. Tapir,
showing crystal-like inclusion. Bar represents 500 nm. Photo courtesy of Prof. H.-H.
Steinbiss, Max Planck Institut für Zuchtungsforschung, Köln, Germany.