|Includes viruses in the genera Luteovirus and Polerovirus and those in the family Luteoviridae not yet assigned to a genus.|
P. M. Waterhouse
Division of Plant Industry, CSIRO, Canberra, Australia
F. E. Gildow
Department of Plant Pathology, Pennsylvania State University, USA
G. R. Johnstone
Tasmania Department of Agriculture, Hobart, Australia
Geographical Distribution etc
Association with Vectors
Relations with Cells and Tissues
Relationships within the Taxon
Notes on Tentative Members
Affinities with Other Groups
The name luteovirus (Latin, luteus = yellow) was coined because infected plants tend to show yellowing symptoms. Other characteristic symptoms are reddening, leaf curling, leaf rolling and brittleness. The concentration of virus particles within the plant is low (less than 100 µg/l of sap) and particles have been observed only in phloem tissues. Luteoviruses are transmitted neither by mechanical inoculation nor through seed, but are transmitted by aphids in a persistent (circulative, non-propagative) manner. Most members show a high degree of vector specificity and some luteoviruses can act as helpers for the aphid-transmission of associated viruses. The International Committee on Taxonomy of Viruses defined the luteovirus group in 1975 (Shepherd et al., 1976). It has since been reviewed by Duffus (1977b), Francki et al. (1985) and Rochow & Duffus (1981).
Table 1(a) Properties of definitive members of the luteovirus group (probable strains or synonyms are shown in italics and preceded by = )
RNA M. Wt
protein M. Wt (× 10-3)
|Barley yellow dwarf (BYDV)-MAV|
|Gr||Sitobion avenae||26, 30, 24T||1.85||23.5||1.88-1.92||115-118||1.39||32; a-d|
|Gr||S. avenae, Rhopalosiphum padi||26, 24T||2.0||24.4||1.76||115||1.40||32; a-d|
|Barley yellow dwarf (BYDV)-RPV|
|Gr||R. padi||26, 30, 24T||1.85-2.0||24.4||1.71-1.79||115-118||32; a-d|
|= Rice guillaume (RGV)|
|Bean leaf roll (BLRV)|
|Le||Acyrthosiphon pisum||27, 23T||2.4||23||1.83||1.32*||286|
|= Legume yellows (LYV)|
|= Michigan (lucerne) alfalfa (MiAV)|
|= Pea leaf roll|
|Beet western yellows (BWYV)|
|Am, Ch, Co, Cr, Le, So||Myzus persicae||27, 26T||1.9||24||89; i; j|
|= Beet mild yellowing (BMYV)|
|Ch, Cr||M. persicae||26||2.0||24-25.4||1.8||116||1.42||k, l|
|= Malva yellows (MYV)|
|Ch, Co, Cr, Ma, So||M. persicae||m|
|= Turnip mild yellows (TuYV)|
|Co, Cr||M. persicae||n|
|Carrot red leaf (CRLV)|
|Groundnut rosette assistor (GRAV)|
|Le||Aphis craccivora||28-30||2.1||24||1.86||115||1.34*||o, p|
|Indonesian soybean dwarf (ISDV)|
|Le||Aphis glycines||26, 24T||q|
|Potato leafroll (PLRV)|
|Am, So||M. persicae||24-25||2.0||26.3||1.78||115-127||1.39; 1.32*||36; 291|
|= Solanum yellows (SYV)|
|= Tomato yellow top (TYTV)|
|Soybean dwarf (SDV)|
|= Subterranean clover red leaf (SCRLV)|
|Le||Aul. solani||25||2.0||22.6||1.85||114||t, u|
|= Strawberry mild yellow edge (SMYEV)|
|Fragaria spp.||Chaetosiphon fragaefolii||23||v, w|
|Tobacco necrotic dwarf (TNDV)|
Table 1(b) Probable and possible members of the luteovirus group
|Probable members||Main host family||Main vector species||Comments||Reference|
|Banana bunchy top (BBTV)||Musa spp.||Pentolonia nigranervosa||Double-stranded RNA profile typical of a luteovirus||x|
|Milk vetch dwarf||Le||A. craccivora||Isometric particles purified and seen in thin sections of phloem tissue||y|
|Millet red leaf||Gr||R. maidis, S. avenae, Sch. graminum||Possibly a form of BYDV||z|
|Physalis mild chlorosis||Cr, So||M. persicae||Possibly a form of BWYV||aa|
|Tobacco vein distorting (TVDV)||So||M. persicae||Acts as a helper virus||bb|
|Tobacco yellow vein assistor (TYVAV)||So||M. persicae||Acts as a helper virus||cc|
|Tobacco yellow net||So||M. persicae||dd|
|Beet yellow net||Ch||M. persicae||ee|
|Celery yellow spot||Um||R. conii||ff|
|Cotton anthocyanosis||Ma||Aphis gossypii||gg|
|Filaree red leaf||Geraniaceae||Acyrth. pe!argonii||hh|
|Grapevine ajinashika||Vitis spp.||Vector unknown||ii|
|Physalis vein blotch||So||M. persicae||jj|
|Raspberry leaf curl||Rosaceae||Aphis rubicola||kk|
T= Measurement of particles seen in thin sections. * = Buoyant density in caesium sulphate solutions. Abbreviations for family names: Am Amaranthaceae; Ch Chenopodiaceae; Co Compositae; Cr = Cruciferae; Gr = Gramineae; Le = Leguminosae; So = Solanaceae; Ma = Malvaceae; Um = Umbelliferae.
References: a: Brakke & Rochow, 1974;
b: Scalla & Rochow, 1977;
c: Paliwal, 1978;
d: Hammond et al., 1983;
e: Amici et al., 1978;
f: Duffus, 1979;
g: Thottappilly et al., 1977;
h: Hampton, 1983;
i: Falk et al., 1977;
j: Falk & Duffus, 1984;
k: Chevallier et al., 1983;
l: Govier, 1985;
m: Costa et al., 1959;
n: Watson, 1964;
o: Casper et al., 1983;
p: Rajeshwari & Murant, 1988;
q: Iwaki et al., 1980;
r: Milbrath & Duffus, 1978;
s: Thomas, 1984;
t: Johnstone et al., 1982;
u: Ashby & Kyriakou, 1983;
v: Martin & Converse, 1985;
w: Spiegel et al., 1986;
x: Dale et al., 1986;
y: Inouye et al., 1979;
z: Yu et al., 1957;
aa: MacKinnon, 1965;
bb: Smith, 1946;
cc: Adams & Hull, 1972;
dd: Sylvester, 1954;
ee: Sylvester, 1948;
ff: Freitag & Severin, 1945;
gg: Costa, 1957;
hh: Frazier, 1951;
ii: Namba et al., 1979;
jj: MacKinnon & Lawson, 1966;
kk: Bennett, 1930.
Aphids that have acquired a luteovirus do not cease to transmit it after moulting and studies of BYDV transmission by R. padi (Gildow, 1985) indicate that luteovirus particles pass by cellular transport through the hindgut into the aphids haemocoel. The particles then circulate in the haemolymph throughout the aphid. Current evidence indicates that luteoviruses do not replicate in their vectors (although Weidemann (1982) suggested that they may do so to a small extent), but aphids that have begun to transmit a luteovirus may continue to do so for 2-3 weeks without re-acquisition. Ultrastructural studies on BWYV, BYDV and PLRV suggest that they are transmitted following endocytosis of virus particles from the haemocoel into the aphids accessory salivary gland. The particles are then transported within coated vesicles through the salivary gland secretory cell, and released by exocytosis into the salivary duct (Gildow & Rochow, 1980a; Gildow 1982, 1987).
A characteristic feature of the luteoviruses is their high degree of vector specificity (Table 1). Each luteovirus is transmitted efficiently by only one or a few species of aphid. Vector specificity is believed to result from interactions between the particle protein and membrane surfaces in the aphids accessory salivary gland; these interactions regulate transport of virus particles to the salivary duct (Gildow & Rochow, 1980b). Vector specificity is not absolute, however, and some luteoviruses are transmitted inefficiently by species other than the main vector (Rochow, 1969). Transmission efficiency has also been reported to vary with the age of the aphid (Gill, 1970; Upreti & Nagaich, 1971; Zhou & Rochow, 1984), and among distinct populations or clones of a single aphid species (Bjorling & Ossiannilsson, 1958; Cockbain & Costa, 1973; Gildow & Rochow, 1983; Rochow, 1960). Genetic variability of aphids, as well as the viruses, evidently influences vector specificity and transmission efficiency.
A number of luteoviruses occur in the field as part of a complex, either with other luteoviruses, such as BWYV and SDV in legumes (Johnstone & Duffus, 1984) and various BYDV serotypes in cereals (Rochow & Muller, 1974), or with members of other virus groups, as with the virus complexes found in strawberries (Prentice, 1946). Some viruses depend on luteoviruses for their aphid transmission (Table 2), for example carrot mottle virus depends on CRLV, and groundnut rosette virus depends on GRAV. These pairs of viruses occur as complexes that seem to be very stable and may show a synergistic effect with regard to symptoms.
Table 2. Luteoviruses which have a helper activity and their associated dependent virus
|Helper virus||Vector||Dependent virus||Reference|
|BYDV-RMV||Rhopalosiphum maidis||BYDV-MAV||Rochow, 1975|
|BYDV-RMV||R. maidis||BYDV-RPV||Rochow, 1982|
|BYDV-RPV||R. padi||BYDV-MAV||Rochow, 1970|
|BYDV-RPV||R. padi||BYDV-RMV||Rochow, 1982|
|BYDV-RPV||R. padi||BYDV-SGV||Rochow, 1982|
|BYDV-PAV||R. padi||BYDV-RMV||Rochow, 1982|
|BYDV-PAV||R. padi||BYDV-MAV||Rochow, 1982|
|BLRV||Acyrthosiphon pisum||Bean yellow vein-banding||Cockbain, 1978; Cockbain et al., 1986|
|BWYV||Myzus persicae||Lettuce speckles mottle||Falk et al., 1979|
|BWYV*||M. persicae||Carrot mottle||Waterhouse & Murant, 1983|
|CRLV||Cavariella aegopodii||Carrot mottle||Watson et al., 1964|
|GRAV||Aphis craccivora||Groundnut rosette||Hull & Adams, 1968|
|GRAV*||A. craccivora||Tobacco yellow vein||Adams & Hull, 1972|
|PLRV*||M. persicae||Carrot mottle||Waterhouse & Murant, 1983|
|TVDV*||M. persicae||Tobacco yellow vein||Adams & Hull, 1972|
|TVDV||M. persicae||Tobacco mottle||Smith, 1945; 1946|
|TYVAV||M. persicae||Tobacco yellow vein||Adams & Hull, 1972|
|TuYV||M. persicae||Lettuce speckles mottle||Falk et al., 1979|
* = Shown to act as a helper experimentally but not known to do so in nature.
Ultrastructural examinations of infected plants have been reported for several luteoviruses (DArcy & De Zoeten, 1979; Esau & Hoefert, 1972; Faoro et al., 1978; Jayasena et al., 1981; Jensen, 1969; Kojima et al., 1969; Kubo, 1981; Murant & Roberts, 1979; Shepardson et al., 1980). The most detailed study was that of Gill & Chong (1979) on BYDV isolates infecting oats, and showed that at least two distinct sequences of events may be involved in replication of viruses assigned to the luteovirus group. Based on cytopathological ultrastructure involving alterations of the nucleus, site of virus accumulation and types of vesicles produced, these authors suggested dividing BYDV isolates into subgroup 1 (MAV, PAV, SGV) and subgroup 2 (RPV, RMV). In oats infected with isolates of subgroup 1, virus particles seem to move from sites of initial inoculation in sieve elements through plasmodesmata into adjacent companion cells. Densely staining filaments (2-4 nm diameter) and single membrane-bound vesicles (50-230 nm diameter) form in the cytoplasm near the plasmodesmata. Filaments are later observed within the nucleus, which becomes distorted and begins to deteriorate soon after infection. Virus particles are first observed to occur in the cytoplasm, suggesting a cytoplasmic site for assembly. At about this time the mitochondria, plastids and ribosomes begin to disintegrate. Isolates in subgroup 2 initiate infection of companion cells in a similar manner; however, the vesicles produced are bounded by a second membrane which is continuous with the endoplasmic reticulum. A second type of membrane system (composed of tubules) proliferates, and the dense filaments are rare in the cytoplasm and do not occur in the nucleus. The nucleus does not deteriorate and virus particles are first observed surrounding the nucleolus within the nucleus. In addition, extensive wall thickenings develop in the infected parenchyma cells.
Ultrastructural changes induced by BWYV and PLRV seem to be similar to those caused by BYDV isolates of subgroup 2 (Esau & Hoefert, 1972; Shepardson et al., 1980). However, cytopathological effects vary with host species and virus isolate (D'Arcy & De Zoeten, 1979; Gill & Chong, 1981; Kojima & Yanase, 1984).
Nucleic acid: The genomes of all luteoviruses so far analysed consist of single-stranded RNA with a M. Wt of c. 2.0 x 106. The genome of PLRV was at first reported to be double-stranded DNA (Sarkar, 1976) but this has not been confirmed in more recent work (Rowhani & Stace-Smith, 1979; Takanami & Kubo, 1979b). The RNA molecules of PLRV, BYDV and CRLV each represent 28-30% of the particle weight (Harrison, 1984; Paliwal, 1978; Waterhouse & Murant, 1982). One isolate of BWYV, but not others, has a second RNA component (M. Wt 0.86 x 106) which was found to be associated with increased virulence (Falk & Duffus, 1984). However, this RNA component is probably not subgenomic (Falk & Anderson, 1987). The RNA extracted from TNDV particles also included two small RNA molecules (M. Wt 1 x 105), but their origin and significance is presently unknown (Takanami & Kubo, 1979a,1979b).
An isolate of BYDV-RPV studied by Miller et al. (1987) has an associated small circular self-cleaving single-stranded RNA (351 nt) which has no homology with the viral genome and therefore appears to be satellite RNA.
Coat protein: The coat protein subunits of luteoviruses so far studied are all of M. Wt c. 24,000. The coat protein subunit of BLRV was originally reported to be c. 32,500 (Ashby & Huttinga, 1979) but a more recent estimate is c. 23,000 (R. O. Hampton, cited by Ashby, 1984). The amino acid composition of the coat protein subunits has been determined for only three luteoviruses: TNDV (Kubo, 1981), BYDV-PAV (P. M. Waterhouse & A. A. Kortt, unpublished data) and SDV (P. M. Waterhouse & A. A. Kortt, unpublished data):
The relatively low amounts of aromatic amino acids (mainly tyrosine and tryptophan) in the coat protein subunits of TNDV, SDV and BYDV may well account for the unusually high A260/A280 ratios observed for particle preparations of these and some other luteoviruses.
The complete nucleotide sequence of a BYDV-PAV serotype has been determined and its genome organization inferred from open reading frames (Miller et al., 1988a,1988b). The gene nearest to the 5' end encodes the RNA-dependent RNA polymerase, the coat protein gene is located near the middle of the genome and there is a possibility of translational readthrough from the coat protein gene to yield a 69 kd protein.
The nucleotide sequence of a satellite RNA associated with an isolate of BYDV-RPV is also known (Miller et al., 1987). It has been inferred from the sequence that the satellite RNA has a high degree of secondary structure and is not translated.
Subgenomic RNA species have been detected in nucleic acid extracts from PLRV-infected potato (M. Wt 1 x 106; Barker et al., 1984) and from BYDV-PAV -infected oats (2.8 and 0.8 kb; Gerlach et al., 1987). Five species of double-stranded RNA have been extracted from tissue infected with BYDV-RPV (Gildow et al., 1983) or BWYV (Falk & Duffus, 1984) and four species from tissue infected with BYDV-MAV (Gildow et al., 1983). This information and the incomplete translation of PLRV or SDV RNA in vitro suggests that luteoviruses may be translated via subgenomic messenger RNA species.
Sequence homology has been detected in the polymerase gene of BYDV and that of carnation mottle virus and in the coat protein gene of BYDV and that of southern bean mosaic virus (Miller et al., 1988a, 1988b).
A number of luteoviruses can assist the aphid-transmission of dependent viruses such as carrot mottle virus (Table 2). It has been shown for two of these dependent viruses that their genomic RNA species can become encapsidated in the coat protein of the helper virus (Falk et al., 1979; Waterhouse & Murant, 1983), and this is thought to explain how they become transmissible by the aphid vector of the helper virus. It has also been shown that the dependent virus can change its helper virus and consequently its aphid vector (Adams & Hull, 1972; Waterhouse & Murant, 1983).
Serological relationships among luteoviruses.
Where possible SDIs have been used to determine the degree of relationship but in some cases qualitative assessments have been used. Numbers refer to the references listed below. The strong serological relationship between TuYV antiserum and PLRV antigen (22) may be due to the antiserum containing some antibodies against PLRV.
References: (1) Amici et al., 1978; (2) Ashby, 1984; (3) Ashby & Kyriakou, 1983; (4) Ashby & Johnstone, 1985; (5) Ashby & Huttinga, 1979; (6) J. E. Duffus, unpublished data; (7) Duffus, 1979; (8) Duffus & Rochow, 1978; (9) Duffus & Russell, 1972; (10) Duffus & Russell, 1975; (11) Duffus & Thottapilly, 1983; (12) Hu et al., 1985; (13) Johnstone, 1983; (14) Kubo & Takanami, 1978; (15) Kyriakou et al., 1983; (16) Casper et al., 1983; Reddy et al., 1985; Rajeshwari & Murant, 1988; (17) Roberts et al., 1980; (18) Rochow & Carmichael, 1979; (19) Rochow & Duffus, 1978; (20) Rochow & Duffus, 1981; (21) Spiegel et al., 1986; (22) Thomas, 1984; (23) Waterhouse & Murant, 1981.