Virions are 25 to 30 nm in diameter, hexagonal in outline and have no envelope (Figure 1). Amino acid sequence homology modelling using the X-ray crystal structure of rice yellow mottle virus (genus Sobemovirus) as a guide suggests that particles have 180 subunits arranged in T=3 icosahedra. Particles are composed of two CPs that encapsidate a genomic single stranded RNA.
Virion Mr is 5.6–6.0×106; buoyant density in CsCl is 1.39–1.42 g cm−3; S20,w is 106–127S. Virions are moderately stable and are insensitive to treatment with chloroform or non-ionic detergents, but are disrupted by prolonged treatment with high concentrations of salts. Luteovirus and polerovirus particles are insensitive to freezing.
Virions contain a single molecule of infectious, linear, positive sense ssRNA. The genome size is fairly uniform ranging from 5.6 kb to 6.0 kb. The RNAs do not have a 3′-terminal poly(A) tract. A small protein (VPg) is covalently linked to the 5′ end of the genomic RNAs of poleroviruses and the one enamovirus. The 5′ termini of barley yellow dwarf virus-PAV (BYDV-PAV) genomic RNA can be phosphorylated after treatment with alkaline phosphatase suggesting that the 5′ termini of luteovirus genomic RNAs are phosphorylated.
There is a single major CP of 21–23 kDa encoded by ORF3 and smaller amounts of a “readthrough” protein, which is a fusion of the products of ORF3 and that of the contiguous ORF5. The readthrough protein may be associated with aphid transmission and/or virus particle stability.
Genomic RNAs of members of the Luteoviridae contain five or six ORFs that are predicted to encode proteins of between 4 and 132 kDa (Table 1; Figure 2). In poleroviruses and by extension the enamovirus, ORF0 (not present in members of the genus Luteovirus) encodes a symptom and host range determinant that functions as a suppressor of RNA silencing. Where present, it overlaps with ORF1. ORFs 1 and 2 overlap and encode the replication-related proteins. The major CP is encoded by ORF3, which is followed in frame by ORF5. The product of ORF4 (overlapping completely with ORF3, but absent from enaomovirus genomic RNA) has been shown to be required for long-distance movement of some luteoviruses and poleroviruses. Some luteovirus and polerovirus genomes contain an ORF 6, predicted to encode a small (≤6 kDa) protein, but no functions have been assigned to the proteins. Genera can be distinguished on the basis of the arrangements and sizes of the ORFs. Replication-related proteins encoded by ORFs 1 and 2 of the luteoviruses are not homologous to products of the corresponding ORFs of poleroviruses and the enamovirus. They are most similar to those of viruses in the family Tombusviridae, while the products of ORFs 1 and 2 of the poleroviruses and the enamovirus are related to those of sobemoviruses.
The differences among luteoviruses, poleroviruses and the enamovirus are principally in the 5′ end of the genome. ORFs 0, 1 and 2 are translated from the genomic RNA. ORF2 is translated by frameshift from ORF1 and thus shares an amino terminus with the product of ORF1. Polerovirus and enamovirus VPgs are cleaved from the products of ORF1 by upstream serine protease domains. ORFs 3, 4 (luteoviruses and poleroviruses) and 5 are expressed from a subgenomic RNA (sgRNA). ORF1 (poleroviruses and the enamovirus) and ORF4 (luteoviruses and poleroviruses) are expressed by leaky scanning. ORF5 is translated via a readthrough of the termination codon at the end of ORF3. Luteoviruses produce one or two additional sgRNAs, the larger of which from BYDV-PAV contains ORF6. Some poleroviruses produce additional sgRNAs.
There are no data on post-translational modification. Particles of some strains of cereal yellow dwarf virus-RPV (CYDV-RPV) contain 322 nt satellite RNAs. Virions of some isolates that consist of pea enation mosaic virus-1 (PEMV-1) together with the umbravirus, pea enation mosaic virus-2 (PEMV-2), contain 717-nt satellite RNAs in addition to genomic RNAs.
Table 1 Proteins of the different ORFs with sizes (kDa) and possible function(s)
Function of product
Suppressor of RNA silencing
Helicase motifs in luteoviruses; protease and VPg in polero- and enamoviruses
RNA-dependent RNA polymerase
Major coat protein
Minor coat protein expressed as C-terminal fusion to core coat protein; possible aphid transmission and virus particle stability factor
Luteovirus and polerovirus particles are strongly immunogenic. Species within a genus are more closely related serologically than are species in different genera. Serological relationships may be detected when comparing disrupted virus particles that are not detectable when intact virions are tested. In gel diffusion assays, aphid-transmissible isolates sometimes display antigenic determinants that are absent from aphid-non-transmissible isolates. No serological relationships have been reported between enamoviruses and either luteoviruses or poleroviruses.
Several members of the family Luteoviridae have host ranges largely restricted to one plant family. For example, BYDVs and CYDVs infect several species in the family Poaceae, bean leafroll virus (BLRV) and soybean dwarf virus (SbDV) infect mainly legumes, and carrot red leaf virus infects mainly plants in the family Umbelliferae. Other members of the family Luteoviridae infect plants in several or many different families. For example, beet western yellows virus (BWYV) infects more than 150 species of plants in over 20 families.
Members of the family Luteoviridae have been reported from Arctic, temperate, sub-tropical, and tropical regions. Some of the viruses are found worldwide, such as BYDV, BWYV and potato leafroll virus (PLRV). Others have more restricted distributions, such as tobacco necrotic dwarf virus, which has been reported only from Japan, and groundnut rosette assistor virus, which has been reported from south Saharan countries in Africa.
Transmission is in a circulative, non-propagative manner by specific aphid vectors. Viruses are acquired by phloem feeding, enter the hemocoel of the aphid via the hindgut (e.g., BYDV-PAV) or posterior midgut (e.g., PLRV) by a receptor mediated transport process, circulate in the hemolymph and enter the accessory salivary gland by a second receptor mediated transport event. Inoculation results from introduction of viruliferous saliva into the phloem tissues via the salivary duct during aphid feeding. PEMV-1 is readily transmitted mechanically, a property dependent on its multiplication in cells co-infected with PEMV-2 (Umbravirus).
Luteovirus and polerovirus particles are largely confined to phloem cells; PEMV-1, with PEMV-2, is found in phloem and mesophyll tissues. Virus particles are found in both the nuclei and cytoplasm of infected cells. Luteoviruses and poleroviruses often cause phloem necrosis that spreads from inoculated sieve elements and causes symptoms by inhibiting translocation, slowing plant growth and inducing the loss of chlorophyll, which results in characteristic yellowing and dwarfing of infected plants.
Type species Barley yellow dwarf virus-PAV
Genome properties are the key features. There is no ORF0 and frameshift from ORF1 into ORF2 occurs at the termination codon of ORF1, and ORF1 and ORF2 overlap by less than 20 nt. ORF1 and ORF2 encode replication-related proteins that are most similar to those of viruses in the family Tombusviridae. The length of the non-coding sequence between ORF2 and ORF3 is about 100 nt. There is no evidence for the presence of a 5′ genome-linked protein. ORF4 is present and contained within ORF3. ORF5 is greater than 1350 nt in length.
Virion buoyant density in CsCl is 1.39–1.40 g cm−3; S20,w is 106–118S.
Sizes of positive sense ssRNA genomes are between 5,677 nt for BYDV-PAV and 5,964 nt for BLRV.
In addition to the characters listed under distinguishing features, viruses within the genus produce two or three subgenomic RNAs from minus-strand templates, the largest of which expresses ORFs 3-5. The 3′-noncoding region contains a transcription enhancer that interacts with the 5′-nontranslated regions of genomic and large subgenomic RNAs to effect cap independent translation initiation.
Criteria used to demarcate species of the genus include:
Barley yellow dwarf virus-MAV
Barley yellow dwarf virus-MAV - PS1
Barley yellow dwarf virus-PAS
Barley yellow dwarf virus-PAS - 129
Barley yellow dwarf virus-PAV
(Barley yellow dwarf virus-rgv=rice giallume)
Barley yellow dwarf virus-PAV - Australia
Bean leafroll virus
(Legume yellows virus)
(Michigan alfalfa virus)
(Pea leafroll virus)
Bean leafroll virus - Michigan
Rose spring dwarf-associated virus
Rose spring dwarf-associated virus - California
Soybean dwarf virus
(Subterranean clover red leaf virus)
Soybean dwarf virus - Tas-1
Species names are in italic script; names of isolates are in roman script; names of synonyms are in roman script and parentheses. Sequence accession numbers [ ] and assigned abbreviations ( ) are also listed.
Barley yellow dwarf virus-GAV
Type species Potato leafroll virus
Polerovirus genomic RNAs have VPgs linked to their 5′ termini and possess an ORF0 and a non-coding region between ORF2 and ORF3 of about 200 nt. ORF1 and ORF2 encode replication-related proteins, which are most similar to those of sobemoviruses. The frameshift from ORF1 into ORF2 occurs upstream of the termination of ORF1, and ORFs 1 and 2 overlap by more than 400 nt. Polerovirus genomes differ from those of the enamovirus in that ORF4 is present within ORF3 and ORF5 is greater than 1200 nt.
Virion buoyant density in CsCl is 1.39–1.42 g cm−3; S20,w is 115–127S.
Sizes of ssRNA genomes are between 5,641 nt for turnip yellows virus and 5,987 nt for PLRV.
See “Distinguishing features” above.
See criteria for the genus Luteovirus.
Beet chlorosis virus
Beet chlorosis virus - 2a
Beet mild yellowing virus
Beet mild yellowing virus - 2ITB
Beet western yellows virus
(Malva yellows virus)
(Turnip mild yellows virus)
Beet western yellows virus - USA
Carrot red leaf virus
Carrot red leaf virus - UK1
Cereal yellow dwarf virus-RPS
Cereal yellow dwarf virus-RPS - Mex1
Cereal yellow dwarf virus-RPV
Cereal yellow dwarf virus-RPV - NY
Chickpea chlorotic stunt virus
Chickpea chlorotic stunt virus - Et-fb-am1
Cucurbit aphid-borne yellows virus
Cucurbit aphid-borne yellows virus - N
Melon aphid-borne yellows virus
Melon aphid-borne yellows virus - Beijing
Potato leafroll virus
(Solanum yellows virus)
(Tomato yellow top virus)
Potato leafroll virus - UK:Scotland
Sugarcane yellow leaf virus
Sugarcane yellow leaf virus - Florida
Tobacco vein distorting virus
Tobacco vein distorting virus - China:Longlin
Turnip yellows virus
Turnip yellows virus - FL-1
Cotton leafroll dwarf virus
Suakwa aphid-borne yellows virus
* Sequences do not comprise the complete genome.
Type species Pea enation mosaic virus-1
Enamovirus (PEMV-1) genomic RNA contains an ORF0, but does not contain an ORF4 (present in luteoviruses and poleroviruses). The non-coding intergenic region between ORF2 and ORF3 is about 200 nt in length. ORF1 and ORF2 encode replication-related proteins that are most similar to those of sobemoviruses. Frameshift from ORF1 into ORF2 occurs upstream of the termination of ORF1, and ORF1 and ORF2 overlap by more than 400 nt. The PEMV-1 genome contains an ORF5 of about 900 nt.
Enamovirus virions have a Mr of about 5.6×106, buoyant densities in CsCl of 1.42 g cm−3, and S20,w of 107–122S.
Genomic RNA of PEMV-1 is 5,706 nt and has a 5′ VPg.
Virions produced in plants infected with PEMV-1 together with PEMV-2 (Umbravirus) are moderately antigenic.
PEMV-1 occurs as part of a complex with PEMV-2 (Umbravirus) and induces mosaic symptoms and enations. Unlike other members of the family Luteoviridae, PEMV-1 is readily transmitted mechanically, a property dependent on its multiplication in cells co-infected with PEMV-2. Aphid transmissibility is conferred by PEMV-1, but can be lost after several mechanical passages. Virions are found in mesophyll tissue as well as in vascular tissue. The genome of PEMV-1 is capable of autonomous replication in protoplasts, but is dependent on PEMV-2 to support systemic invasion.
Pea enation mosaic virus-1
Pea enation mosaic virus-1 - WSG
Species names are in italic script; names of isolates are in roman script. Sequence accession numbers [ ] and assigned abbreviations ( ) are also listed.
Barley yellow dwarf virus-GPV
Barley yellow dwarf virus-GPV - 04FX6
Wheat yellow dwarf virus-RPV
Barley yellow dwarf virus-RMV
Barley yellow dwarf virus-RMV - Illinois
Barley yellow dwarf virus-bv
Barley yellow dwarf virus-SGV - NY
Chickpea stunt disease associated virus
Chickpea stunt disease associated virus - IC
Groundnut rosette assistor virus
Groundnut rosette assistor virus - M16GCP
Indonesian soybean dwarf virus
Indonesian soybean dwarf virus - IND
Sweet potato leaf speckling virus
Sweet potato leaf speckling virus - Peru
Tobacco necrotic dwarf virus
Tobacco necrotic dwarf virus - Japan
Species names are in italic script; names of isolates, strains and synonyms are in roman script. Sequence accession numbers [ ] and assigned abbreviations ( ) are also listed.
Chickpea yellows virus
Lentil stunt virus
The three genera within the family Luteoviridae share very similar structural protein genes (ORFs 3 and 5) whose products show varying levels of serological relatedness. Phylogenetic analysis of the predicted amino acid sequences of the polymerases (ORF2) clearly separate the members of the family Luteoviridae into the three genera (Figure 3).
The nucleotide sequences of BLRV and SbDV (genus Luteovirus) lack ORF0, like those of luteoviruses, and the predicted amino acid sequences of their replication proteins are similar to those of the luteoviruses. However, their structural proteins are more closely related to those of poleroviruses (Figure 3). Conversely, sugarcane yellow leaf virus (genus Polerovirus) contains an ORF0 and its ORFs 1 and 2 are most closely related to those of other poleroviruses, whereas ORFs 3 and 4 are most closely related to those of the luteoviruses and ORF5 is most closely related to the readthrough protein gene of the enamovirus. These viruses may be recombinants between the genera.
Viruses in the family Luteoviridae have replication-related and structural proteins that are sufficiently similar to those in other genera to suggest evolutionary relationships. The putative luteovirus polymerases resemble those of members of the family Tombusviridae. In contrast, polymerases of poleroviruses and enamoviruses resemble those of viruses in the genus Sobemovirus. These polymerase types are thought to be very distant in evolutionary terms. The CP amino acid sequences of PLRV and rice yellow mottle virus, a sobemovirus, share 33% similarity, which has been used to predict the structure of PLRV and other members of the family Luteoviridae. It has been suggested that the genomes of the Luteoviridae originated by recombination between ancestral genomes containing the structural protein genes characteristic of the family Luteoviridae and genomes containing either of the two polymerase types.
Enamo: from pea enation mosaic virus.
Luteo: from Latin luteus, “yellow”.
Polero: from potato leaf roll virus.
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