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Arch Virol (2009) 154:1967–1972
DOI 10.1007/s00705-009-0506-6
VIROLOGY DIVISION NEWS
Virgaviridae: a new family of rod-shaped plant viruses
Michael J. Adams • John F. Antoniw •
Jan Kreuze
Received: 16 June 2009 / Accepted: 26 August 2009 / Published online: 28 October 2009
Ó Springer-Verlag 2009
Abstract The new plant virus family Virgaviridae is
described. The family is named because its members have
rod-shaped virions (from the Latin virga = rod), and it
includes the genera Furovirus, Hordeivirus, Pecluvirus,
Pomovirus, Tobamovirus and Tobravirus. The chief characteristics of members of the family are presented with
phylogenetic analyses of selected genes to support the
creation of the family. Species demarcation criteria within
the genera are examined and discussed.
The International Committee on Taxonomy of Viruses
(ICTV) has recently approved a proposal to create a plant
virus family Virgaviridae. The family is named because
its members have rod-shaped virions (from the Latin
virga = rod), and it includes the genera Furovirus, Hordeivirus, Pecluvirus, Pomovirus, Tobamovirus and Tobravirus. The chief characteristics of members of the family
are:
1.
2.
Alpha-like replication proteins that form a distinct
phylogenetic ‘‘family’’ [5].
Single-stranded RNA ? sense genomes with a
30 -t-RNA-like structure and no polyA tail.
M. J. Adams (&) J. F. Antoniw
Department of Plant Pathology and Microbiology,
Rothamsted Research, Harpenden,
Hertfordshire AL5 2JQ, UK
e-mail: mike.adams@bbsrc.ac.uk
J. Kreuze
Germplasm Enhancement and Crop Improvement Division,
International Potato Center, Lima, 12, Peru
3.
4.
Rod-shaped virions 20–25 nm in diameter with a
central ‘‘canal’’.
Coat proteins of 19–24 kDa.
It contains some viruses in which there is a single cellto-cell movement protein (MP) of the ‘30K’ superfamily
[7] and others that encode a triple gene block (TGB) [8].
There are also differences in the number of genomic RNAs
(1, 2 or 3 depending on the genus), but sequence analysis of
the polymerase and other genes suggests that the viruses
form a coherent taxonomic unit (see below). Some properties of the six genera included in the family are summarized in Table 1, and their genome organization is
shown in Fig. 1. Biologically, the viruses are fairly diverse.
They have been reported from a wide range of herbaceous
and mono- and dicotyledonous plant species, but the host
range of individual members is usually limited. All members can be transmitted experimentally by mechanical
inoculation, and for those in the genus Tobamovirus, this is
the only known means of transmission. In some genera,
transmission is by soil-borne vectors, while members of the
genus Hordeivirus are transmitted through pollen and seed.
The only genus with rod-shaped virions excluded from this
list is Benyvirus, because this is much more distantly
related in phylogenetic analyses of the polymerase (see
below) and because (unlike the others) its members have a
polyadenylated genome and a polymerase that is processed
by autocatalytic protease activity.
On the basis of their analysis of the RNA-dependent
RNA polymerase (RdRp) gene from a wide range of
viruses, Koonin and Dolja [5] included viruses from the six
genera described in this paper within RdRp Supergroup 3,
which they sub-divided into three lineages that they suggested might correspond to orders. One of these lineages,
which they named Tobamo, included the six genera
123
1968
M. J. Adams et al.
Table 1 Major properties of the genera included in the new family Virgaviridae
Genus
RNAs
RdRPa
MPb
CPc
30 Structured
Transmission
Furovirus
2
RT
‘30K’
19K ? RT
t-RNAVal
‘‘Fungus’’
Hordeivirus
3
Separate
TGB
22K
t-RNATyr
Seed
Pecluvirus
2
RT
TGB
23K
t-RNAVal
‘‘Fungus’’ ? seed
Val
Pomovirus
3
RT
TGB
20K ? RT
t-RNA
Tobamovirus
1
RT
‘30K’
17–18K
t-RNAHis
Mechanical
Tobravirus
2
RT
‘30K’
22–24K
t-RNA-
Nematode
a
b
‘‘Fungus’’
Relation of RdRp to the replication protein (Methyltransferase, Helicase); RT, in a readthrough domain at the C-terminus
MP movement protein either of the ‘30K’ superfamily [7] or a Triple gene block (TGB [8])
c
CP coat protein size (with indication of RT, a readthrough domain at the C-terminus if present)
d
t-RNAVal/Tyr/His/-, t-RNA-like structure accepting valine, tyrosine, histidine or not aminoacylated, respectively
Fig. 1 Diagram showing the genome organization of the six genera
included in the family Virgaviridae. Domains marked in the
replication proteins are Methyltransferase (M), Helicase (H) and
RNA-dependent RNA polymerase (R). Triple gene block proteins
(TGB) are cross-hatched, and coat proteins are in black. MP,
movement protein of the ‘30K’ superfamily; C, cysteine-rich protein.
Positions of ‘‘leaky’’ stop codons are shown by triangles (filled
triangles). tVal/Tyr/His/-: t-RNA-like structure accepting valine, tyrosine, histidine or not aminoacylated, respectively. Brackets indicate
ORFs that are missing from some strains
considered here, together with the families Closteroviridae
and Bromoviridae and the genus Idaeovirus. Phylogenetic
analysis (using several different methods) of the RdRp
domain, of the whole replication protein or of the fused
Methyl transferase–Helicase–RdRp domains continues to
support this grouping and shows that the genus Benyvirus is
much too distantly related to be grouped in this family (see
Fig. 2). The inclusion within the branch of the families
Closteroviridae and Bromoviridae also justifies the inclusion of all six genera within the single family Virgaviridae.
The replication proteins constitute the majority of the
genomes of these viruses and provide the best phylogenetic
trees, but there are also indications of relatedness amongst
123
the other genes. For example, the TGB proteins of the
genera Hordeivirus, Pecluvirus and Pomovirus are clearly
related and form a distinct group separate from those of the
genus Benyvirus and the filamentous viruses in the family
Flexiviridae (recently split into two families). A tree for
TGBp1 sequences is provided in Fig. 3, and more details
supporting this classification of the TGB proteins are provided by Morozov and Solovyev [8]. The small size of the
coat protein and its inherent variability make it less suitable
for phylogenetic analysis. Nevertheless, significant groupings of genera occur (Furo- with Pomo-; Peclu- with
Hordei- and Tobra- a bit more distant) which correspond
with those found within the RdRp (Fig. 4). There are also
close relationships between the small cysteine-rich proteins
of Furovirus, Hordeivirus, Pecluvirus and Tobravirus,
although those of Pomovirus do not align well with them
(data not shown).
The taxonomic structure of the new family and the
species currently included are listed in Table 2.
Sequence differences between and within the existing
species in the family were examined and compared with
molecular criteria for species discrimination provided by
the relevant study groups in the 8th ICTV report [2].
Individual pairwise comparisons were therefore made
using the nt and aa sequences of each fully sequenced gene
from every available accession in the family Virgaviridae
contained in the international databases. Comparisons used
the GCG [1] program GAP (with a gap creation penalty of
50 and a gap extension penalty of 3 for nt comparisons and
values of 8 and 2, respectively, for aa comparisons). This
program aligns the two sequences selected and calculates
the percentage identity and similarity between them. To
assist with the large numbers of comparisons, software was
written (Antoniw, unpublished) to generate batch files that
were run in GCG and also to extract and summarize data
from the output files. Some of the chief features of the data
for the replication protein, the RdRp and the coat protein
Virgaviridae: a new family of rod-shaped plant viruses
1969
Fig. 3 Phylogenetic (neighbor-joining) tree of the amino acid
sequences of the TGBp1 proteins of members of the genera included
in the family Virgaviridae together with other TGB-containing
viruses. Numbers on branches indicate percentage of bootstrap
support out of 1,000 bootstrap replications (when [60%). The scale
indicates JTT amino acid distances. Tree produced in MEGA4 [9].
A tree of similar typology was obtained by maximum-likelihood
analysis (PROML in PHYLIP [3])
Fig. 2 Phylogenetic tree of the amino acid sequences of the fused
Met–Hel–RdRp domains of the members of the six genera included in
the family Virgaviridae together with some other related viruses.
Distantly related genera and families that formed well-supported
monophyletic clades were collapsed into a triangle, the length of
which corresponds to the variation found within the clade. The
recently established order Tymovirales includes the families Tymoviridae and Flexiviridae (which has also been divided). The
neighbour-joining (NJ) tree is shown, but nearly identical trees were
produced from the alignment using Maximum Composite Likelihood
(ML) and Bayesian tree building algorithms. Percentage bootstrap
support (out of 1,000 replications) for NJ and ML trees and posterior
probability for the Bayesian tree are, respectively, indicated on the
corresponding branches separated by slashes if they differed from
each other. Values are only indicated on the major branches when
[60%, and when values were identical, only one number is indicated
(asterisk). The consensus tree generated by ML did not support the
inclusion of BBNV into a Pomovirus clade and grouped the genus
Idaeovirus within the Bromoviridae clade. The scale indicates JTT
amino acid distances. Alignments were made from translated
nucleotide sequences using the ClustalW algorithm in the Alignment
Explorer module of MEGA4 [9] as described previously [6]. A total
of 500 amino acid positions corresponding to 1,500 nt positions were
used for the alignment. NJ and ML trees were generated using
standard settings for these algorithms in MEGA4 [9] from protein and
back-translated nucleotide alignments, respectively. The Bayesian
tree was generated from back-translated nucleotide alignment using
MrBayes v3.1.2 [4], employing the general time reversible model
with gamma-shaped rate variation with a proportion of invariable
sites; 1,000,000 generations of MCMC analysis were the point at
which the average standard generation of split frequency between two
parallel runs had reached 0.009565
Fig. 4 Phylogenetic (neighbor-joining) tree of the amino acid
sequences of the coat proteins of members of the genera included
in the family Virgaviridae. Numbers on major branches indicate
percentage of bootstrap support out of 1,000 bootstrap replications
(when [60%). The scale indicates JTT amino acid distances. Tree
produced in MEGA4 [9]. A tree of similar typology was obtained by
maximum-likelihood analysis (PROML in PHYLIP [3])
genes are summarized in Table 3. Within some genera,
there are rather few species and sequences, but some
conclusions may nevertheless be reached. For the genus
Tobravirus, it is already known that coat protein sequences
(from RNA2) are of little taxonomic value [2], and this
appears also to be the case for the genus Pecluvirus. Within
the replication protein and RdRp, isolates of the same
species usually had [90% nt or aa sequence identity.
Comparisons between genera show that some existing
123
1970
M. J. Adams et al.
Table 2 List of species recognised within the genera belonging to the new family Virgaviridae with accession numbers for complete genome
nucleotide sequences
Species
Abbreviation
Isolate genome sequence(s)
Chinese wheat mosaic virus
CWMV
AJ012005 ? AJ012006 (NC_002359 ? NC_002356); AJ271838 ? AJ271839;
AB299271 ? AB299272
Oat golden stripe virus
OGSV
AJ132578 ? AJ132579 (NC_002358 ? NC_002357)
Soil-borne cereal mosaic virus
SBCMV
AJ132576 ? AJ132577 (NC_002351 ? NC_002330); AF146278 ? AF146282;
AJ252151 ? AJ252152
Soil-borne wheat mosaic viruse
SBWMV
L07937 ? L07938 (NC_002041 ? NC_002042); AB033689 ? AB033690a
Sorghum chlorotic spot virus
SrCSV
AB033691 ? AB033692 (NC_004014 ? NC_004015)
Genus Furovirus
Genus Hordeivirus
Anthoxanthum latent blanching virus
ALBV
No sequences available
Barley stripe mosaic viruse
BSMV
J04342 ? X03854 ? M16576 (NC_003469 ? NC_003481 ? NC_003478);
U35768 ? U35772 ? U13918; U35766 ? U35769 ? U13916;
U35767 ? U35770 ? U13917; AY789693 ? AY789694 ? AY787207
Lychnis ringspot virus
LRSV
No complete genome sequences available
Poa semilatent virus
PSLV
No complete genome sequences available
IPCV
X99149 ? AF447397 (NC_004729 ? NC_004730)
PCV
L07269 ? Z97873 (NC_003668 ? NC_003520)
Beet soil-borne virus
BSBV
Z97873 ? U64512 ? Z66493 (NC_003520 ? NC_003518 ? NC_003519);
EF545138 ? EF545140 ? EF545142; EF545139 ? EF545141 ? EF545143;
FJ971717 ? FJ971718 ? FJ971719
Beet virus Q
BVQ
AJ223596 ? AJ223597 ? AJ223598 (NC_003510 ? NC_003511 ? NC_003512)
Broad bean necrosis virus
BBNV
D86636 ? D86637 ? D86638 (NC_004423 ? NC_004424 ? NC_004425)
Potato mop-top viruse
PMTV
AJ238607 ? AJ243719 ? AJ277556 (NC_003723 ? NC_003724 ? NC_003725)
Brugmansia mild mottle virus
BruMMV
AM398436 (NC_010944)
Cucumber fruit mottle mosaic virus
CFMMV
AF321057 (NC_002633)
Cucumber green mottle mosaic virus
CGMMV
D12505 (NC_001801); AB015146; AF417242; AF417243; EF611826; AB369274;
EU352259
Frangipani mosaic virus
FrMV
No complete genome sequences available
Hibiscus latent Fort Pierce virus
HLFPV
No complete sequence but FJ196834,AY596456 and AY250831 provide the coding
sequences]
Hibiscus latent Singapore virus
HLSV
AF395898 (NC_008310)
Kyuri green mottle mosaic virus
KGMMV
AJ295948 (NC_003610); AB015145; AB162006
Obuda pepper virus
ObPV
D13438 (NC_003852); L11665
Odontoglossum ringspot virus
ORSV
X82130 (NC_001728); U34586; U89894; S83257; AY571290; DQ139262
Paprika mild mottle virus
PaMMV
AB089381 (NC_004106)
Pepper mild mottle virus
PMMoV
M81413 (NC_003630); AB000709; AJ308228; AB069853; AY859497; AB126003;
AB113116; AB113117; AB254821; AB276030
Rehmannia mosaic virus
ReMV
EF375551 (NC_009041)
Ribgrass mosaic virus
RMV
No complete genome sequences available
Sammons’s Opuntia virus
SOV
No sequences available
Streptocarpus flower break virus
SFBV
AM040955 (NC_008365)
Sunn-hemp mosaic virus
SHMV
An almost complete sequence is provided from a combination of U47034 and J02413
Tobacco latent virus
TLV
No complete genome sequences available
Tobacco mild green mosaic virus
TMGMV
M34077 (NC_001556); AB078435; DQ821941; EF469769
Tobacco mosaic viruse
TMV
V01408 (NC_001367); V01409; X68110; AF165190; AJ011933; D63809; AF273221;
AF395127; AF395128; AF395129; AB369275; AB369276
Tomato mosaic virus
ToMV
AF332868 (NC_002692); AF155507; AJ243571; Z92909; X02144; AJ132845;
AJ417701; AB083196; DQ873692
Turnip vein-clearing virus
TVCV
U03387 (NC_001873); Z29370
Genus Pecluvirus
Indian peanut clump virus
e
Peanut clump virus
Genus Pomovirus
Genus Tobamovirus
123
Virgaviridae: a new family of rod-shaped plant viruses
1971
Table 2 continued
Species
Abbreviation
Isolate genome sequence(s)
Ullucus mild mottle virus
UMMV
No sequences available
Wasabi mottle virus
WMoV
AB017503 (NC_003355)c; AB017504
Youcai mosaic virus
YMoV
U30944 (NC_004422); AF254924 (NC_002792)d; D38444; AY318866; DQ223770;
AB261175; EU571218
Zucchini green mottle mosaic virus
ZGMMV
AJ295949 (NC_003878); AJ252189
Genus Tobravirus
a
Pea early browning virus
PEBV
X14006 ? X51828 (NC_002036 ? NC_001368)
Pepper ringspot virus
PepRSV
L23972 ? X03241 (NC_003669 ? NC_003670)
Tobacco rattle viruse
TRV
AF166084 ? Z36974 (NC_003805 ? NC_003811); AF034622 ? AF034621
Probably a different species
b
There are sequences annotated as Ribgrass mosaic virus, but the definition of this species appears uncertain
c
Annotated as crucifer tobamovirus wasabi strain
d
Annotated as Ribgrass mosaic virus but seems to belong here while the definition of RMV appears uncertain
e
Denotes type species
Table 3 Values from pairwise sequence comparisons for three genome regions amongst viruses in the family Virgaviridae
Most distantly related isolates of same species
Most closely related species
Most distantly related species
aa
nt
aa
aa
Furovirus
95.1
94.3
82.5
72.7
52.7
56.5
Hordeivirus
96.5
94.7
NA
NA
NA
NA
Pecluvirus
NA
NA
88.6
78.0
88.6
78.0
Pomovirus
99.7
99.6
54.9
59.2
45.3
54.9
Tobamovirus
94.4
86.8
93.8
83.6
39.3
49.4
Tobravirus
98.8
99.2
63.6
63.0
52.9
57.8
Furovirus
96.7
95.9
90.4
78.9
72.4
68.0
Hordeivirus
98.1
98.4
NA
NA
NA
NA
Pecluvirus
Pomovirus
NA
99.2
NA
99.4
95.1
76.6
79.4
70.3
95.1
65.0
79.4
64.2
Tobamovirus
95.4
87.2
96.2
86.0
52.8
57.1
Tobravirus
99.2
99.0
79.8
71.6
75.5
68.7
Furovirus
92.0
86.2
95.5
94.2
43.2
49.1
Hordeivirus
98.0
97.7
55.6
60.1
40.8
48.1
Pecluvirus
40.6
50.1
66.5
64.8
36.5
45.8
Pomovirus
97.7
98.7
53.0
58.8
29.1
42.4
Tobamovirus
87.7
88.5
93.0
90.9
26.7
38.9
Tobravirus
38.6
45.2
89.2
77.5
36.2
48.6
nt
nt
Replication protein
RdRp
Coat protein
Amino acid (aa) and nucleotide (nt) identities are provided for each genus, showing the most distantly related isolates of the same species and the
minimum and maximum values for comparisons between different species. Criteria for species discrimination listed in the in 8th ICTV report [2]
are also shown
Furovirus: less than about 75 or 80% nt identity on RNAs 1 and 2, respectively
Hordeivirus: no criteria provided
Pecluvirus: no molecular criteria provided
Pomovirus: less than about 80% identical over the whole sequence; less than about 90% identical in CP amino acid sequence
Tobamovirus: less than 10% overall nt sequence difference is considered to characterize strains of the same species
Tobravirus: nucleotide sequences of RNA-1 show \75% identity; RNA-2 sequences are of limited value
123
1972
species in the genus Tobamovirus are rather closely related
and there may be merit in re-examining the species
demarcation criteria within this genus.
Acknowledgments Rothamsted Research receives grant-aided
support from the Biotechnology and Biological Sciences Research
Council of the UK.
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