MOLECULAR PLANT PATHOLOGY (2002) 3(4), 177–183
Pathogen profile
Blackwell Science, Ltd
Barley yellow dwarf virus: Luteoviridae or Tombusviridae?
W. A L L E N M I L L E R * , S I J U N L I U A N D R A N D Y B E C KE T T
351 Bessey Hall, Iowa State University, Ames, Iowa 50011, USA
SUMMARY
Barley yellow dwarf virus (BYDV), the most economically
important virus of small grains, features highly specialised
relationships with its aphid vectors, a plethora of novel
translation mechanisms mediated by long–distance RNA
interactions, and an ambiguous taxonomic status. The structural
and movement proteins of BYDV that confer aphid transmission
and phloem-limitation properties resemble those of the
Luteoviridae, the family in which BYDV is classified. In contrast,
many genes and cis -acting signals involved in replication
and gene expression most closely resemble those of the
Tombusviridae.
Taxonomy: BYDV is in genus Luteovirus, family Luteoviridae. BYDV includes at least two serotypes or viruses: BYDV-PAV
and BYDV-MAV. The former BYDV-RPV is now Cereal yellow
dwarf virus-RPV (CYDV-RPV). CYDV is in genus Polerovirus, family Luteoviridae. Genus Luteovirus shares many features with
family Tombusviridae.
Physical properties: ∼25 nm icosahedral (T = 3) virions.
One major (22 kDa) and one minor (50 – 55 kDa) coat protein.
5.6–5.8 kb positive sense RNA genome with no 5′-cap and no
poly(A) tail.
Host range: Most grasses. Most important in oats, barley
and wheat. Also infects maize and rice.
Symptoms: Yellowing and dwarfing in barley, stunting in
wheat; reddening, yellowing and blasting in oats. Some isolates
cause leaf notching and curling.
Key attractions: Model for the study of circulative transmission of aphid-transmitted viruses. Plethora of unusual translation mechanisms. Evidence of recombination in recent
evolutionary history creates taxonomic ambiguity. Economically
important virus of wheat, barley and oats, worldwide.
Useful websites/meetings : International
symposium:
‘Barley Yellow Dwarf Disease: Recent Advances and Future
Strategies’, CIMMYT, El Batan, Mexico, 1 – 5 September 2002,
*Correspondence: E-mail: wamiller@iastate.edu
© 2002 BLACKWELL SCIENCE LTD
http://www.cimmyt.cgiar.org/Research/wheat/Conf_BYD_02/
invitation.htm
http://www.cimmyt.org/Research/wheat/BYDVNEWS/htm/
BYDVNEWS.htm
Aphid transmission animation:
http://www.ppws.vt.edu/~sforza/tmv/bydv_aph.html
I N T RO D U C T I O N
In 1951, BYDV was recognised by Oswald and Houston (1951) as
a new virus and the causal agent of a yellow dwarf disease
epiphytotic of barley, wheat and oats in California. Since then it
has provided fascinating insights in diverse areas of biology,
including virus–vector interactions, translational control mechanisms, and virus evolution that has led to a taxonomic dilemma.
A G RO N O M I C I M P O R T A N C E
BYDV has long been considered to be the most significant viral
disease agent of small grain cereals, worldwide. BYDV causes
particularly severe yield losses in oats due to blasting and low
seed set. BYDV stunts wheat, in which it is widespread and
causes significant yield losses, but often goes undetected or
misdiagnosed. Application of insecticides on wheat in the United
Kingdom and Australia to control the aphid vectors of BYDV
usually results in substantial yield increases (Plumb and Johnstone,
1995) that are attributable to the absence of BYDV infection.
Natural resistance genes are few. The Yd2 gene in barley is the
most widely used (Burnett et al., 1995), whereas oats harbour
multigenic tolerance (Jin et al., 1998). Oats (Koev et al., 1998)
and barley (Wang et al., 2000) have been genetically engineered
to resist BYDV using portions of the viral genome as transgenes.
However, no transgenic lines have been released for use by
growers. Concerns about perceived risks imposed by transgenic
BYDV resistant crops are the subject of controversy (Kaiser, 2001;
Miller et al., 1997), whereas the benefits of new resistance genes,
such as reduced pesticide inputs and increased yields, are readily
apparent. For more details on the economic importance and
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sequences (Fig. 1). Soybean dwarf virus (SbDV) shares close
sequence and genome organizational similarity to BYDV but has
yet to be assigned to a genus. For comprehensive reports on all
aspects of Luteoviridae, see ‘The Luteoviridae’ (Smith and Barker,
1999). Currently, BYDV is officially classified as two viruses,
BYDV-MAV and BYDV-PAV, but they are virtually identical except
for the structural genes which affect vector specificity. Thus, we
feel that these are merely strains or serotypes of the same virus
and refer to them as a single virus to avoid confusion. More
importantly, we present evidence throughout this review that
genus Luteovirus (BYDV-PAV and BYDV-MAV), ironically has
more features in common with the Tombusviridae family than it
does with other members of the Luteoviridae.
A P H I D T RA N S M I S S I O N
Fig. 1 Genome organizations of viruses related to BYDV. POL, RNA-dependent
RNA polymerase; CP, major coat protein; RTD, readthrough domain; 3′ TE, 3′
cap-independent translation element; frag, 18 nt conserved fragment of the 3′
TE; fs, frameshift signal; rt, readthrough site. Stem-loops and terminal bases are
shown at-3′ ends of genomes. Dashed lines: major subgenomic RNAs. Yellow
shading, features in common with Tombusviridae (not all genera shown). Red, shared
among Polerovirus, Enamovirus and Sobemovirus genera. Blue: ‘Luteoviridae block’.
worldwide occurrence of the diseases, we refer the reader to the
book, ‘BYDV: Forty Years of Progress’ (D’Arcy and Burnett, 1995).
C U R RE N T C L A S S I F I C A T I O N
BYDV is the sole member of genus Luteovirus and the type
member of the Luteoviridae family (formerly luteovirus group) which
was defined originally as those viruses that: (i) are transmitted
only by aphids in a persistent manner and not mechanically;
(ii) circulate but do not replicate in the aphid; (iii) are confined to
the phloem in the plant; (iv) have 25 nm icosahedral particles
consisting of a major ∼22 kDa coat protein and a minor component of about 52 kDa encapsidating a 5.7-kb RNA (D’Arcy et al.,
2000). Cytopathological and serological differences first led to
division of the BYDV serotypes into two subgroups. Subsequent
nucleotide sequencing revealed that the divisions were too great
to confine the serotypes into one virus species. Former BYDV
serotype RPV (BYDV-RPV) was given a new name, Cereal yellow
dwarf virus-RPV (CYDV-RPV) and placed in genus Polerovirus
along with four other non-BYDV viruses in the Luteoviridae. A
third genus, Enamovirus, consists only of RNA-1 of the bipartite
Pea enation mosaic virus (PEMV). Its organization resembles
poleroviruses, but lacks ORF 4 and has rather different cis-acting
BYDV is transmitted by a wide range of grass-feeding aphids. In
pioneering research, William Rochow uncovered remarkably
specific relationships between BYDV strains and different aphid
vector species that led to a classification system based on vector
specificity (Rochow, 1969). Isolates transmitted primarily by
Rhopalosiphum padi are called RPV (now CYDV-RPV), those
transmitted by Sitobion (formerly Macrosiphon) avenae are called
MAV, and those transmitted by both aphid species are called PAV.
Other isolates are transmitted by Rhopalosiphum maidis (RMV),
Schizaphis graminum (SGV), or both R. padi and S. graminum
(GPV, a likely CYDV serotype; Wang et al., 1998). Isolates with
other aphid vector preferences no doubt exist. Serological differentiation of the isolates correlates well with the above vector
specificities, so they are now called serotypes. Transmission efficiency of BYDVs also varies significantly among the biotypes or
clones of single aphid species (reviewed by Power and Gray,
1995; Young and Filichkin, 1999).
Specificity of BYDV transmission by aphids is determined
largely by interactions between the virus capsid proteins
(Rochow, 1970) and aphid accessory salivary gland (ASG) membranes (Gildow and Gray, 1993). When BYDV virions are ingested
by aphids they bind to the epithelial cells in the hindgut and
penetrate the haemocoel by receptor-mediated uptake. Most BYDV
serotypes pass through the hindgut membrane barrier and enter
the haemocoel, even in non-vector aphid species (Gildow, 1993).
In the haemocoel, the readthrough domain of the coat protein
(CP-RTD, see below) on the surface of virions interacts with symbionin, a homologue of the Escherichia coli GroEL protein, that
is produced by endosymbiotic bacteria of genus Buchnera in the
aphid haemocoel (Filichkin et al., 1997). Binding of symbionin
probably protects BYDV virions from proteolysis in the haemolymph (Young and Filichkin, 1999). The circulating virions
encounter the ASG that has two barriers that determine vector
specificity: the basal lamina and the plasma membrane. The virus
is taken up selectively by receptor-mediated endocytosis into the
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Barley yellow dwarf virus
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ASG. Upon feeding, the virions enter host plants via the salivary
canal (Gildow and Gray, 1993). Promising research directed toward
identifying ASG receptors that bind BYDV seroytpe-specifically
is underway (Li et al., 2001).
The extremely complex epidemiology of BYDV involves
critical combinations of the viruses, aphid vectors, host plants
susceptible to both virus and aphid vectors, and environmental
conditions (Irwin and Thresh, 1990; Power and Gray, 1995).
G E N O M E O RG A N I Z A T I O N A N D G E N E
FUNCTIONS
The BYDV genome harbours six open reading frames (ORFs)
(Fig. 1). The 5′-proximal ORFs are the only genes necessary for
BYDV RNA replication in protoplasts. ORF2 encodes the RNAdependent RNA polymerase (RdRp). It is expressed only fused to
ORF1 via low frequency −1 ribosomal frameshifting in the region
of overlap (Paul et al., 2001), resulting in a high ratio of the ORF1
product (P1) to the P1-P2 fusion (RdRp). ORF 3 encodes the major
coat protein (CP). In-frame translational readthrough of the ORF3
stop codon is necessary for translation of ORF5 which exists fused
to CP as a readthrough domain (RTD). The RTD is necessary for
aphid transmission, but not for virion assembly (Chay et al.,
1996). ORF4 permits infection of the phloem tissue of the entire
plant (Chay et al., 1996). The homologue of ORF4 in Potato leafroll polerovirus (PLRV) has many biochemical properties of a cellto-cell movement protein including nonspecific single stranded
nucleic acid binding, ability to be phosphorylated, and localisation to the plasmodesmata (Schmitz et al., 1997).
The poleroviruses have an extra ORF (0) at the 5′ end that is
absent in BYDV. ORF O from PLRV induces virus symptoms on its
own (van der Wilk et al., 1997a). ORF1 of poleroviruses, while in
a similar position as ORF1 of genus Luteovirus is much larger,
has no sequence homology and encodes different functions,
including a proteinase motif and the viral genome-linked protein
(VPg) (van der Wilk et al., 1997b) which is absent in BYDV. BYDV,
but not the very similar SbDV, has a small, variable 4.3–7.2 kDa
(depending on the isolate) ORF 6 near the 3′ end. Its function
is unknown. ORFs 3, 4 and 5 are the only sequences in which
Luteovirus and Polerovirus genera share homology (Fig. 1),
comprising what we call the ‘Luteoviridae block’.
N O V E L T RA N S L A T I O N M E C H A N I S M S
The BYDV genome utilises a remarkable array of translational
control signals not known previously on any RNA. This includes
a 100 nt cap-independent translation element (3′ TE), between
ORFs 5 and 6, that facilitates very efficient initiation of
translation at the ORF1 AUG (Wang et al., 1997). For translation,
a stem-loop in the 3′ TE must base-pair to a stem-loop in the 5′
untranslated region (UTR), presumably to deliver translation
Fig. 2 Control of BYDV gene expression. Genomic (gRNA) and subgenomic
(sgRNA) RNAs are bold black lines. ORFs are shown above RNAs. White ORFs
are translatable from the indicated RNA, black ORFs are not. Boxes on the bold
lines (RNAs) control cap-independent translation [white (in vitro and in vivo),
and light grey (in vivo only)], ribosomal frameshifting (dark grey), in-frame
readthrough of CP stop codon (black). Secondary structures of translational
control regions, 3′-terminus (replication origin), and subgenomic promoters
(minus strand) are indicated; thick, grey loops base-pair to distant regions as
shown by dotted lines with double arrowheads.
factors and/or ribosomes to the 5′ end (Guo et al., 2001) (Fig. 2).
This base-pairing allows circularization of mRNA that is a
prerequisite for translation of normal mRNAs. However, host
mRNA circularises via assembly of initiation factors that bind the
cap, poly(A) tail, and each other, to form a protein bridge
between the 5′- and 3′ end (Hentze, 1997). The RNA base-paired
bridge in BYDV RNA represents a novel way of recruiting translational machinery.
The 3′ TE structure and potential base-pairing to a stem-loop
in the 5′ UTR is present in SbDV RNA, and in genus Necrovirus of
the Tombusviridae (Guo et al., 2001). A 17 nt, conserved core
motif of the 3′ TE is also present in the 3′ UTRs of genus Dianthovirus (Tombusviridae) (Wang et al., 1997). Genera Tombusvirus
and Carmovirus of the Tombusviridae also harbour 3′ UTR
sequences that confer cap-independent translation (Qu and
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Morris, 2000; Wu and White, 1999). No 3′ TE-like elements are
known in genus Polerovirus, including CYDV-RPV, or Enamovirus.
The −1 ribosomal frameshift signals also involve remarkably
long–distance interactions. BYDV contains the canonical −1
frameshift signals at the overlap of ORFs 1 and 2. These include
a shifty site (GGGUUUU in BYDV) followed by a highly structured
RNA tract. However, this is insufficient for frameshifting in BYDV
genomic RNA. Additional sequences, located 4 kb downstream in
the viral 3′ UTR are necessary (Paul et al., 2001). A stem-loop in
this region has potential to base-pair to a bulge in the stem-loop
adjacent to the frameshift site (Fig. 2). The shifty site and adjacent bulged stem-loop closely resemble those in genus Dianthovirus (Tombusviridae) (Kim and Lommel, 1998), but are totally
different from the compact pseudoknot that mediates frameshifting in the Polerovirus and Enamovirus genera (Kim et al., 1999).
A third non-canonical translation event controlled by distant
downstream sequences is in-frame ribosomal readthrough of the
ORF 3 (CP) stop codon (Fig. 2). This requires a peculiar tract of
CCNNNN repeats that begin about 25 nt downstream and at
least two elements about 700–750 nt downstream of the stop
codon (Brown et al., 1996). Unlike other replication and translation signals, these readthrough control signals are present in all
Luteoviridae and unknown in other virus families. This is consistent with their location in the ‘Luteoviridae block’.
SUBGENOMIC RNAS
ORFs 1 and 2 are the only genes translated from genomic RNA.
ORFs 3, 4, and 5 all are translated from sgRNA1 (Fig. 2). Translation of ORF 4 initiates at the second AUG of the RNA via a leaky
scanning mechanism that is influenced by the sequence context
and secondary structure around the AUGs (Dinesh-Kumar and
Miller, 1993). ORF 6 is translatable from sgRNA2 in vitro ( Wang
et al., 1999), but its product has yet to be detected in infected cells.
Enigmatic sgRNA3 encodes no ORFs, yet accumulates to very high
levels in infected plants weeks after inoculation ( Kelly et al., 1994).
The cis-acting sequences required for sgRNA synthesis
(‘promoters’) are surprisingly diverse. sgRNAs 1 and 2 have the
same six bases as genomic RNA at the 5′ end (GUGAAG), but the
promoters are otherwise dissimilar. All three have different
secondary structures (Koev and Miller, 2000). The minimal
sgRNA2 promoter spans the 3′ TE, hinting at a possible regulatory
connection between translation initiation and sgRNA2 synthesis.
We propose that sgRNA2 is generated by termination during (–)
strand synthesis caused by base pairing in the 3′ TE. This would
be the same mechanism as for genus Dianthovirus, except that
the dianthoviral base-pairing is intermolecular (Sit et al., 1998).
This is supported by mutations in the BYDV sgRNA2 promoter that
cause slight changes in the 5′ end of sgRNA2 ( Moon et al., 2001).
SgRNA2 may regulate translation in trans. When genomic RNA
and sgRNAs 1 and 2 are translated together in vitro at ratios
resembling those in infected cells, sgRNA2 by virtue of the 3′ TE
at its 5′ end, inhibits translation of the other two RNAs (Wang
et al., 1999). This is probably by competition for translation
factors. Translation of sgRNA1 is only slightly inhibited by
sgRNA2 while that of genomic RNA is almost completely shut off.
We proposed that, as sgRNA2 accumulates in infected cells it
triggers a switch from early (polymerase) to late (structural and
movement proteins) gene expression by selectively inhibiting
translation of genomic RNA (Wang et al., 1999).
LUTEOVIRIDAE OR TOMBUSVIRIDAE?
In addition to the numerous gene expression control signals that
BYDV shares with Tombusviridae but not genus Polerovirus,
coding regions and replication elements also support these relationships. The 3′ terminus, where replication initiates, ends in
CCC in all of the diverse genera of the Tombusviridae, and in genus
Luteovirus (Fig. 1). However, poleroviral RNAs all terminate in GU.
Tombusviridae RNAs and BYDV RNA harbour a stable stem-loop
just upstream of the terminal CCC. It is essential for replication
(Koev et al., 2002; Song and Simon, 1995; Turner and Buck,
1999). No such structure is predicted or known in poleroviruses.
The similarities of replication origins are reflected in the
RdRps that copy them. It has long been known that the RdRp of
BYDV is closely related to those of the Tombusviridae (dianthoviruses in particular), but more distantly related to those of the
poleroviruses (Figs 1 and 3). In contrast, the polerovirus RdRps
are more closely related to those of genus Sobemovirus (Fig. 3).
Moreover, poleroviruses and sobemoviruses harbour a VPg at the
5′ end of the RNA. The VPg primes RNA synthesis by a replication
mechanism that is fundamentally very different from that of
RNAs that lack such an entity (Paul et al., 1998). It requires a
complex interplay of the RdRp and a viral protease that is absent
in BYDV as well. By all replication criteria, BYDV clearly belongs
in the Tombusviridae.
So why classify BYDV in the Luteoviridae at all? One obvious
reason is that the genes in the Luteoviridae block (ORFs 3, 4 and
5), seem to confer the viral phenotypes relevant to the grower
and the plant pathologist. Particle morphology and its highly specific relationship with aphid vector are conferred by ORFs 3 and 5.
The confinement to the phloem may be due to a phloem-specific
movement protein encoded by ORF 4. Are these phenotypes
sufficient for classification as a group? Already, Enamovirus has
been awarded membership in Luteovidae despite lack of phloemlimitation. (Technically speaking, PEMV-1 is phloem-limited in
the absence of PEMV-2 which is not in the Luteoviridae, but
PEMV-1 does not occur alone—and is thus not phloem-limited—
in nature.) Icosahedral, multicomponent Brome mosaic virus RNA
was engineered to produce and be encapsidated by the coat
protein of rod-shaped Tobacco mosaic virus (Sacher et al., 1988).
Yet this rod-shaped chimera is clearly a modified BMV and not a
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Barley yellow dwarf virus
Fig. 3 Phylogenetic trees of the polymerase (ORF 2) of BYDV and related
viruses. Sequences were aligned with PILEUP and trees made with DAUP using the
GCG DNA sequence analysis package (Madison, WI). Not all Tombusviridae
genera are shown.
man-made Tobamovirus. By the same reasoning, BYDV is essentially a member of Tombusviridae that acquired the movement
and structural proteins of a Polerovirus (Fig. 1 and Miller et al.,
1997). The movement proteins and genome organizations of
various genera of Tombusviridae differ widely (e.g. Dianthovirus
and Necrovirus in Fig. 1), yet all are grouped together in the same
family.
NEW VARIATION WITHIN BYDV ISOLATES
Classification of isolates within BYDV may also warrant modification. Classification based on vector specificity has withstood
the test of time and is important for epidemiological purposes. As
sequences of many BYDV CP genes have been compiled, it is
clear that the CP sequences in the most common serotype, PAV,
can be subdivided into at least two subgroups which La Pierre
and colleagues termed ‘cpA’ and ‘cpB’ (Mastari et al., 1998). Until
recently, CP genes of all fully sequenced BYDV genomes were
cpA. Recently, we sequenced the entire genome of a novel
isolate, PAV-129, discovered by Stewart Gray and colleagues
to break the standard BYDV tolerance in oats (Chay et al., 1996),
181
Fig. 4 Relationships of the major coat protein (ORF 3) of BYDV isolates in
serotypes PAV and MAV. Trees made as in Fig. 3. Proposed subgroups A and B
modified from Mastari et al. (1998) are indicated.
and we found that its CP fit in cpB ( Fig. 4). Moreover, the remainder
of the genome differs substantially from all other BYDV isolates.
While all other fully sequenced BYDV isolates (representing three
continents), including MAV have 97% identity to each other in
ORFs 1 and 2, PAV-129 has only 80 and 88% homology, respectively, in these ORFs (Fig. 3).
With regard to cis-acting signals, PAV-129 has major insertions
that extend a stem-loop in the 3′ TE (Guo et al., 2000), PAV-129
lacks any homology to the other BYDVs in the sgRNA3 promoter
region (Koev and Miller, 2000), and the very 3′ end of the PAV-129
genome has a distinctly different sequence (but retains the
terminal CCC and adjacent Tombusvirus-like stem-loop (Koev
et al., 2002). All other BYDVs (including MAV) have only minor
single nucleotide polymorphisms in these regions. Thus, the cpA
and cpB dichotomy may apply to the entire genomes which we
call subgroup A and subgroup B. Except for the ORFs 3, 4, 5, the
subgroup A isolates are more similar to MAV than they are to
PAV-129 (Fig. 3) and possibly the other members of subgroup B.
Yet even PAV-129 is not very divergent from other PAV isolates
because a chimera, containing the 5′ half of the genome of PAVAus (subgroup A) and the 3′ half from PAV-129, replicated in
protoplasts (Koev et al., 2002) and in whole plants (SL, unpublished
observation).
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There is no reason to assume a priori a correlation between
serotype-based classification and classification based on cis- and
trans replication sequences. Perhaps, for example, an MAV serotype will be found with a PAV-129-like genome sequence (outside
ORFs 3, 4, 5). In fact, SbDV has a BYDV-like (Tombusvirus-like)
genome, but has a Luteoviridae block more closely related
to those in genus Polerovirus than to BYDV (Rathjen et al., 1994).
Based on the dendrogram in Fig. 4 it would be interesting to
know the full-length genomic sequence of PAV-CN which has the
most distant PAV CP sequence, perhaps revealing a third PAV
subgroup.
Finally, our recent complete sequence of a severe CYDV-RPV
isolate from Mexico and California, CYDV-RPV-Mex1, revealed
what may be a different virus from CYDV-RPV-NY. ORFs 0, 1 and
2 of these two viruses have only 41%, 53%, and 81% amino acid
sequence identity, respectively. Yet the Luteoviridae block ORFs
are so similar (CP, RTD, ORF 4 have 92%, 87%, and 90% amino
acid sequence identity, respectively) that both isolates were
placed in the same serotype. In summary, the serotype (aphid
transmission phenotype) and genome sequence are two independent ways of categorizing BYDV isolates.
CONCLUSIONS
The International Committee on the Taxonomy of Viruses defines
a virus species as ‘a polythetic class of viruses that constitute a
replicating lineage and occupy a particular ecological niche’ (van
Regenmortel, 2000). BYDV clearly fits in the replicating lineage
of the Tombusviridae. However, the ecological niche, as determined by the virus’ interaction with its hosts and vectors, is that
of the Luteoviridae. Thus, BYDV may never be assigned tidily into
a single family. We propose that all of the families in Figs 1 and
3 be grouped into a large order, Tombusvirales. However, this
doesn’t answer the family question. Classification of BYDV at this
level may remain always in the eye of the beholder.
ACKNOWLEDGEMENTS
The authors thank the USDA National Research Initiative (grant
no. 2001-35319-10011) and NSF (grant no. MCB-9974590) for
research funding.
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