Glasshouse Crops Research Institute, Littlehampton, Sussex, England
A. A. Brunt
Glasshouse Crops Research Institute, Littlehampton, Sussex, England
Type MemberPotato virus Y
Flexuous filamentous particles, normally 720-900 nm long and c.
11 nm in diameter,
sedimenting at c.
150 S, and with a buoyant density in CsCl of 1.31 g/cm3
The particles consist of up to 2000 subunits of a single protein species
(M. Wt 32 to 34 x 103
arranged as a helix (pitch c.
3.4 nm) enclosing the genome. The genome is a
single molecule of
single-stranded RNA (M. Wt 3.0 to 3.5 x 106
), and constitutes
5% of the particle
Thermal inactivation point (10 min) 50 to 75°C (usually 55 to 60°C);
longevity in sap 1 to
50 days (usually 2 to 4 days); and dilution end-point 10-1 to 10-6
10-3 to 10-4). Most
have restricted, or very restricted, host ranges,
but the different viruses occur in a wide range of monocotyledonous and dicotyledonous
induce mosaic or mottle symptoms in leaves; many also induce colour-breaking in flowers,
distorted fruits and seeds, and some cause considerable losses of crop yield and quality.
potyviruses are transmitted in the non-persistent manner by aphids, and epidemic levels
of field spread
often occur. Potyviruses are also transmitted by inoculation of sap, and at
least 12 of them are
carried in a small proportion of the seeds of some host species.
The virus particles occur, and are probably assembled, in the cytoplasm; those of
many of the viruses
reach moderately high concentrations in plant sap, but the particles of some are
difficult to extract and
purify. The viruses induce the formation of characteristic cytoplasmic inclusion bodies.
Definitive and possible members of the group are listed in
the table. A virus is considered to be a
definitive member of the group if it:- (1) has filamentous particles of characteristic
properties; (2) is transmitted non-persistently by aphids; (3) induces the formation of
cytoplasmic inclusions (pinwheels); (4) is clearly serologically
distinguishable from morphologically
Serological relationship to other definitive potyviruses is not an essential
criterion for membership
of the group but is reliable confirmatory evidence.
Table 1. Definitive and possible members of the potyvirus group*
Amaranthus leaf mottle (Lovisolo & Lisa, 1976)
Araujia mosaic (Charudattan et al., 1980)
Bean common mosaic (BCMV; 73)
Bean yellow mosaic (BYMV; 40)
Bearded iris mosaic (147)
Beet mosaic (53)
Bidens mottle (161)
Blackeye cowpea mosaic (Lima et al., 1979)
Carnation vein mottle (CarVMV; 78)
Carrot thin leaf (218)
Celery mosaic (CeMV; 50)
Clover yellow vein (ClYVV; 131)
Cocksfoot streak (CkSV; 59)
Colombian datura (Kahn & Bartels, 1968)
Commelina mosaic (Morales & Zettler, 1977)
Cowpea aphid-borne mosaic (134)
Daphne Y (Forster & Milne, 1976)
Dasheen mosaic (191)
Datura shoestring (Giri & Agrawal, 1971)
Euphorbia ringspot (Bode & Lesemann, 1976)
Gloriosa stripe mosaic (Koenig & Lesemann, 1974)
Guinea grass mosaic (190)
Helenium Y (Kuschki et al., 1978)
Henbane mosaic (HMV; 95)
Hippeastrum mosaic (117)
Hyacinth mosaic (Derks & Vink-van den Abeele, 1980)
Iris mild mosaic (116)
Iris fulva mosaic (IFMV; Barnett & Alper, 1977)
Iris severe mosaic (Brunt & Phillips, 1980)
Leek yellow stripe (240)
Lettuce mosaic (LtMV; 9)
Mungbean mottle (Sun et al., 1977)
Narcissus degeneration (Brunt, 1980)
Narcissus late season yellows (Brunt, 1980)
Narcissus yellow stripe (76)
Onion yellow dwarf (158)
Papaya ringspot (84)
Parsnip mosaic (91)
Passionfruit woodiness (PWV; 122)
Pea seedborne mosaic (PSbMV; 146)
Peanut mottle (141)
Pepper mottle (PeMV; Purcifull et al., 1975)
Pepper veinal mottle (PVMV; 104)
Pepper severe mosaic
(Feldman & Garcia, 1977)
Plum pox (70)
Pokeweed mosaic (97)
Potato A (54)
Potato Y (PVY; 37, 242)
Primula mosaic (Lisa & Lovisolo, 1976)
Soybean mosaic (93)
Statice Y (Lesemann et al., 1979)
Sugarcane mosaic (SCMV; 88)
Tamarillo mosaic (Mossop, 1977)
Tobacco etch (TEV; 55)
Tobacco vein mottling (Sun et al., 1974)
Tomato (Peru) (Raymer et al., 1972)
Tulip breaking (71)
Turnip mosaic (TurMV; 8)
Watermelon mosaic (WMMV; 63)
Wisteria vein mosaic
(Conti & Lovisolo, 1969;
B. Potyviruses regarded as strains of members listed in A,
or of uncertain relationship to those members
Aquilegia mosaic (Marani & Pisi, 1976)
Azuki bean mosaica
(Tsuchizaki et al., 1970)
Bidens mosaic (Kuhn et al., 1978)
Bryonia mottle (Lockhart & Fischer, 1979)
Clover (Croatian) mosaic
(Taraku et al., 1977)
Crinum (Pares & Bertus, 1978)
Datura 437 (Damsteegt, 1974)
Datura mosaic (Qureshi & Mahmood, 1978)
Dendrobium mosaic (Inouye, 1976)
(Edwardson et al., 1970)
Dioscorea greenbanding (Hearon et al., 1978)
Dioscorea trifida (Migliori & Cadilhac, 1976)
Freesia mosaic (Brunt, 1974)
Garlic yellow streak
(Mohamed & Young, 1981)
(Hansen & Lesemann, 1978)
Groundnut eyespot (Dubern & Dollet, 1980)
Kennedya V (Dale et al., 1975)
Lupin mottleb (Hull, 1968)
Maize dwarf mosaicc (MDMV; 88)
Malva vein-clearing (Schmidt & Schmelzer, 1964)
Mungbean mosaicd (Kaiser et al., 1968)
Nothoscordum mosaic (McKinney, 1929;
Gold et al., 1957)
Ornithogalum mosaic (Smith & Brierley, 1944)
Passionfruit ringspot (De Wijs, 1974)
Pea necrosisb (Bos et al., 1974)
Pea mosaicb (40)
Sweet potato A (Sheffield, 1957;
Hollings & Stone, 1977)
Sweet potato feathery mottle
(Campbell et al., 1974)
Sweet potato russet crack
(Campbell et al., 1972)
Teasel mosaic (Gemignani, 1965)
(Lockhart & Betzold, 1980)
Wild potato mosaic
(Jones & Fribourg, 1979)
* Acronym and Description number or other
reference given in parentheses
aregarded as a strain of cowpea aphid-borne mosaic
boften regarded as a strain of BYMV
cregarded as a strain of SCMV
dregarded as a strain of BCMV
ea virus of uncertain affinity, with properties resembling both carlaviruses and
Geographical Distribution etc
Potyviruses usually occur wherever their principal host plants are grown, but they
prevalent in tropical and sub-tropical countries.
Association with Vectors
Most of the definitive potyviruses are transmitted by aphids in a non-persistent,
manner. Virus is acquired most efficiently after probes of only a few minutes during
which there is
merely superficial insertion of the stylets into the epidermis, and acquisition is
enhanced if the
aphids are previously starved for 1 to 3 h. Infection likewise follows feeding of a
few minutes; the
viruliferous aphid usually remains infective for less than 1 h if it continues to feed,
or 4 h if
starved. There is no evidence for a latent period between acquisition and transmission,
nor for virus
multiplication in the vector. Although a given potyvirus may be transmitted by several
considerable specificity occurs, and there are marked differences in efficiency of
different clones or colonies of one aphid species, or between different strains of the
same virus. All
potyviruses tested so far require a helper factor for their transmission
(Govier & Kassanis, 1974
this factor is labile proteinaceous material of apparent M. Wt 100 to 200 x
, which is probably coded for by the viral genome and perhaps assists
in attaching virus
particles to the mouth-parts of the vector aphid
(Govier, Kassanis & Pirone, 1977
factors may also be involved
Members of very few other invertebrate taxa have been reported to transmit definitive
WMMV and CeMV were reported to be inefficiently transmitted by the leaf miner
(Zitter & Tsai, 1977);
apparent soil-transmission of SCMV in the absence
of root contact, suggested the involvement of a soil-living vector
(Bond & Pirone, 1970).
Potyviruses are a very successful group of pathogens which flourish in a wide range of
environmental conditions; they are most successful in tropical or sub-tropical countries,
continuous or successive crops are grown throughout the year. Many different factors
rate of spread and their severity in crops, but the most important are the proximity of
and the number, activity and occurrence of the alate forms of vector species.
A low incidence of
infection early in the life of the crop often ultimately results in a high incidence
and severe disease.
Potyviruses do not survive in dead leaves or other host debris, nor for long periods
in the vector. In
temperate climates, they survive in perennial or vegetatively propagated crops.
Because most have
narrow, often extremely restricted, host ranges comparatively few are able to survive in
host species; even where this does occur, it is often of only minor importance.
The most dangerous
virus sources are infected planting material, or infected volunteer plants from
A consequence of the extreme host-specialisation of different potyviruses is the
occurrence of numerous
strains, or pathotypes, which may have survived through the absence of inter-strain
competition in common
(Hollings & Brunt, 1981).
However, in a number of host species, two or more different
potyviruses are quite often found in the same individual plant.
Relations with Cells and Tissues
Potyvirus particles are sometimes found scattered randomly throughout the cytoplasm of
cells and occasionally within plasmodesmata (e.g.
Weintraub, Ragetli & Lo, 1974
occur in uniseriate arrays parallel to the tonoplast or cytoplasmic lamellae, or in
projecting into or bridging the cell vacuole (e.g.
Lawson & Hearon, 1971
membrane-associated aggregates present in negatively-stained sap are possibly either
fragments of the
virus-containing strands or tonoplast-associated particles entrapped during cellular
pieces of the adjacent membrane
(Brunt & Atkey, 1974
Infected cells sometimes contain unusual
aggregates of mitochondria or chloroplasts
(Weintraub, Agrawal & Ragetli, 1973
Kitajima & Lovisolo, 1972
Kitajima & Costa, 1973
Cytoplasmic inclusions. Potyviruses induce the formation of conical or
cytoplasmic inclusions (CCI), the structure of which has been elucidated from
ultrastructual studies of
Rubio Huertos & Lopez-Abella, 1966),
(McDonald & Hiebert, 1974a)
and, more recently, computer-assisted analytical
(Mernaugh, Gardener & Yocom, 1980).
Fully-formed inclusions each have a central core
from which radiate 10-20 thin striated rectangular or triangular curved plates
lamellae or septa). CCI seen in transverse section are described
as pin-wheels and in
longitudinal section as bundles. Sections of the lamellae,
when not obviously associated with
the pin-wheel core, are described as laminated inclusions
if straight or unfolded, as scrolls
or tubes if rolled inwardly, and as laminated aggregates
if two or more are closely associated or
partially fused. CCI are generally considered to be either cylindrical
(Andrews & Shalla, 1974)
in shape, but computer-assisted mathematical interpretations of serial
transverse sections of TEV-CCI suggest that some might also be hour-glass-shaped (elliptic
(Mernaugh et al., 1980).
CCI are initially closely associated with plasmodesmata (e.g.
Lawson & Hearon, 1971),
and this suggests that they may be concerned with the intercellular transport of
and/or their nucleic acid and protein components
(Andrews & Shalla, 1974).
Potyviruses have been
sub-grouped according to the predominant type of CCI they induce
CCI are detectable by light microscopy in suitably stained epidermal leaf strips
(Christie & Edwardson, 1977).
Amorphous inclusions or X-bodies (masses of cytoplasmic inclusions aggregated with
ribosomes, virus particles, endoplasmic reticulum, mitochondria and/or other organelles)
commonly induced by potyviruses in chronically-infected plants.
The lamellae of the CCI have surface striations with a periodicity of about 5 nm.
and/or their fragments can be extracted and purified from infected plants; with
some viruses, their
yields (16 to 18 A280 units/kg leaf tissue) are consistently greater
than those of
(Hiebert & McDonald, 1973).
CCI contain a single virus-specific polypeptide species
(M. Wt 67 to 70 x 103).
Nuclear inclusions. A few potyviruses, notably TEV, also induce the formation of
nuclear inclusions (CNI)
which are readily detectable by light microscopy in suitably
stained epidermal strips
(Christie & Edwardson, 1977).
CNI appear to be flat crystals 6 to 8
µm square when viewed from above, but to be slightly curved plates in side view.
TEV-CNI can be extracted and purified, yields of 2 to 8 x 108 inclusions/kg
being readily obtained
(Knuhtsen, Hiebert & Purcifull, 1974).
Extracted CNI each consist of thin
rectangular plates which may be present in regular stacks but are often offset at
45° to each other.
The plates have a clearly discernible periodic substructure with striations 10.2 nm apart
primary axes intersecting at 90°; this periodicity is also clearly visible in CNI
seen in situ
by freeze-etch electron microscopy
(McDonald & Hiebert, 1974b).
In transverse section,
the CNI appear to be multilayered pyramids.
TEV-CNI contain two polypeptide species (M. Wt 49.8 and 54.5 x 103)
serologically unrelated to those of the associated virus particles or CCI, or to
healthy plant protein
(Knuhtsen et al., 1974).
CNI of various shapes and sizes induced by other potyviruses
(Christie & Edwardson, 1977)
have yet to be similarly characterised.
The modal length of potyvirus particles was originally defined as 730 to 760 nm
(Brandes & Wetter, 1959
but the size range was later extended slightly to 720 to 770 nm
although most potyviruses have particles within these limits, those of HMV
(Lovisolo & Bartels, 1970
and several potyviruses from flower bulbs
(Brunt & Atkey, 1971
were subsequently found to be
straighter and mostly 850 to 950 nm long. Particles of HMV, BYMV and PVMV are rigid,
straight and c.
850 nm long in the presence of Mg++
ions, but flexuous and c
750 nm long in the
absence of Mg++
(Govier & Woods, 1971
such morphological changes are sometimes
reversible. Similar changes occur with particles of other potyviruses such as CkSV
(Chamberlain & Catherall, 1977
(Hollings & Stone, 1971
but those of IFMV are unusual in reacting
in the reverse manner to the presence or absence of Mg++
(Barnett & Alper, 1977
Particles of some potyviruses easily fragment during purification, giving apparent
lengths; e.g. 590 to 700 nm with C1YVV
(Singh & Lopez-Abella, 1971
Hollings & Stone, 1974
and 680 nm with TurMV
(Shepherd & Pound, 1960
Potyvirus particles usually show very little
substructure, although some have a discernible central canal 2-3 nm diameter in
preparations. The protein subunits are arranged in a helix with a pitch of c
3.4 nm (Varma et al., 1968
A particle weight of 60 to 70 x 106
daltons, estimated from data for
nucleic acid and protein contents, indicates that each particle contains 1700-2000
that are possibly arranged 8-9 per turn of the helix.
The u.v. absorbance spectra of potyviruses are typical of nucleoproteins,
with maximum at 260 to
262 nm and minimum at 240 to 246 nm. The A260/A280
ratios of 1.14-1.25, and
Amax/Amin ratios of 1.11-1.27 are typical of
nucleoproteins containing 5-6%
The absorption coefficient (A0.1%, 1cm at 260 nm) which has been
determined for only a few potyviruses, ranges from 2.4 to 2.9. Several potyviruses
are stable in
CsCl at 20 to 25°C, and have buoyant densities of 1.318 to 1.336 g/cm3
(Huttinga & Mosch, 1974;
Damirdagh & Shepherd, 1970).
The M. Wt of the single capsid protein of potyviruses is now generally regarded as
c. 32 x 103 for TEV
(Hiebert & McDonald, 1973)
and c. 36.5 x 103
for MDMV (strain of SCMV)
(Hill, Ford & Benner, 1973).
Values c. 26-28 x 103
reported earlier are probably due to proteolytic degradation of the protein
(Huttinga & Mosch, 1974),
for increasing amounts of lower M. Wt material are commonly detectable by
polyacrylamide/SDS gels following storage of virus preparations at c. 2°C
(Brunt & Kenten, 1971;
Moghal & Francki, 1976).
Other explanations for protein
heterogeneity, however, have been proposed
(Hill & Benner, 1980).
Amino acid analyses indicate
that the structural subunits of potyviruses such as BYMV, LtMV, BCMV, PWV, PVY and
c. 290 amino acids
(Moghal & Francki, 1976);
earlier reports probably greatly
underestimated the number of residues. Protein from PVY particles, dissociated with
in 1 to 100 mM phosphate solutions (pH 6 to 9) to form long flexuous particles
(McDonald, Beveridge & Bancroft, 1976;
Goodman et al., 1976).
The 3 S and 10 S protein components
in such preparations first polymerise to form stacked rings, each about 40 nm long.
reassemble into filaments c. 10.5 nm in diameter, and of various lengths up to
PVY-protein polymerises with PVY-RNA or papaya mosaic virus-RNA to form helical virus-like
that are non-infective
(McDonald & Bancroft, 1977).
Potyviruses contain 5 to 6% single-stranded positive-sense RNA
preparations have been obtained from some potyviruses such as MDMV
(Pring & Langenberg, 1972
PVY, TurMV and TEV
(Makkouk & Gumpf, 1974
Hill & Benner, 1976
formaldehyde-treated PVY-RNA sediment at 39 S and 24 S respectively
(Pring & Langenberg, 1972
Makkouk & Gumpf, 1974
By electrophoresis in polyacrylamide gels, the
estimated M. Wt (x 106
) of the genome RNA were: TurMV-RNA, 3.5; PVY-RNA, 3.2;
(Hill & Shepherd, 1972
Hari et al., 1979
density-gradient centrifugation, the M. Wt of MDMV-RNA was estimated at 2.7 x 106
of PVY-RNA at 3.1 x 106
(Pring & Langenberg, 1972
Makkouk & Gumpf, 1974
TEV-RNA is reported to contain strands with or without poly(A) which are equally infective
(Hari et al., 1979
the activity of poly(A) polymerase is greatly enhanced in TEV-infected
Nucleotide base ratios have been determined for several potyviruses;
most values lie in the ranges
G 21-26; A 23-30; C 20-27; U 18-29, but that of PSbMV is reported as
G22.8; A44.0; C17.6; U15.6
(Hampton & Mink, 1975).
Although little is known about their replication, potyviruses are thought to replicate
cytoplasm. In recent in vitro
Dougherty & Hiebert (1980a
found that the 39 S single-stranded RNA molecules of TEV and PeMV
each induce the formation of six gene products of which one is the coat protein and
another is the
cytoplasmic inclusion (CCI) protein; the TEV products also include the two nuclear
proteins. The estimated total M. Wt of the products were 340 x 103
or 324 x
(PeMV); these values account for 95% and 93% of the estimated coding
capacity of the
TEV-RNA and PeMV-RNA, respectively. Although TEV-RNA and PeMV-RNA induce the
production of several
products in in vitro
translation experiments, each nucleic acid is
considered to act as a
(Dougherty & Hiebert, 1980c
Such studies have also permitted
the tentative genetic mapping of both nucleic acids, although there is some disagreement about the
location in TEV-RNA of the coat protein gene
(Dougherty & Hiebert, 1980c
Hellman et al., 1980
Relationships within the Taxon
Serological relationships among potyviruses are complex. Most of the definitive
are serologically related to at least one other member of the group, and in many
several other potyviruses. But present techniques have failed to detect any serological
relationship between many pairs of potyviruses, and relationships may be only indirect
several members. Thus, relationships were found between intact particles of LtMV and BYMV,
between BYMV and BCMV, but not between BCMV and LtMV
(Alba & Oliveira, 1976
strains of one potyvirus may differ considerably in their serological relationships
potyviruses. Although some potyviruses react adequately in agar-gel immunodiffusion,
first be fragmented into small lengths, e.g.
(Tomlinson et al., 1965
or the coat protein dissociated into subunits by chemical treatments (e.g.
(Shepard et al., 1974
However, dissociated proteins are very poor immunogens,
and may not react with antisera to intact particles
(Moghal & Franki, 1976
relationships observed between intact particles of two potyviruses may not occur
dissociated particle proteins.
The proteins of the characteristic CCI induced by potyviruses are antigenically
the coat protein, and those of serologically unrelated potyviruses show considerable
differences even when the viruses are propagated in the same plant species; however,
of serologically closely related potyvirus strains appear to be immunochemically
(Hiebert et al., 1971;
Purcifull, Hiebert & McDonald, 1973).
Cross-protection occurs between a number of potyviruses (e.g. TEV, PVY and HMV;
Bawden & Kassanis, 1941)
but not between others, even when the latter are recognised as strains of
the same potyvirus (e.g different strains of PVY
or of MDMV
(Gillaspie & Koike, 1973)).
Two or more potyviruses can occur, and have synergistic effects, in naturally
(Hollings & Brunt, 1981).
Several attempts have been made to evaluate criteria for differentiating
for defining virus strains, and for dividing potyviruses into sub-groups.
The properties used have
included host range, cross-protection, particle length and serology
Lindsten, Brishammar & Tomenius, 1976),
host range and serology
(Jones & Diachun, 1977),
serology and amino acid
analyses of the particle protein
(Moghal & Francki, 1976),
and morphology of CCI
Suggested sub-groupings of potyviruses have so far shown various anomalies and
inconsistencies, and none has been generally accepted. Serological comparisons,
using both intact
and dissociated particles, seem to offer the most practical method at present
for establishing the
identity of new isolates; but among potyviruses there exists a multitude of
strains and pathotypes
that differ mainly in biological properties, such as host range or pathogenicity,
and which form
an almost continuous range of variants for which a species concept is not applicable
Affinities with Other Groups
By a combination of properties, potyviruses are readily differentiated from
However, they show some similarities to at least nine other
viruses which also have filamentous particles and induce the formation of cytoplasmic
but, unlike potyviruses, have vectors other than aphids. The affinities of such viruses are
uncertain; until the taxonomic significance of vector type and inclusion formation have been
further considered, they are probably best excluded from the potyvirus group.
The better known viruses of this type,
and wheat streak mosaic,
infect cereal crops in America and Europe; they have filamentous
particles mostly c. 700 nm long, induce CCI indistinguishable from those of
potyviruses but are transmissible by eriophyid mites. It has been suggested previously
viruses should be included in the carlavirus group
(Brandes & Bercks, 1965),
Edwardson, 1974), or in a separate group or a
sub-group of the potyvirus
Lapierre & Spire, 1969).
Another CCI-forming virus,
sweet potato mild mottle,
has filamentous particles mostly
c. 800 nm long; as it is transmissible by whiteflies and is serologically
unrelated to 40
potyviruses, it is also for the present probably best excluded from the group
(Hollings, Stone & Bock, 1976).
Some cereal viruses, namely
barley yellow mosaic,
rice necrosis mosaic,
wheat spindle streak mosaic and
wheat yellow mosaic,
induce CCI but are transmissible by the fungus Polymyxa graminis and have rigid
particles of two modal lengths
(Inouye & Fujii, 1977);
these viruses also are probably best
excluded from the potyvirus group.
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