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Annu. Rev. Phytopathol. 1997. 35:167–90
c 1997 by Annual Reviews Inc. All rights reserved
Copyright °
BARLEY YELLOW DWARF
VIRUSES
W. Allen Miller and Lada Rasochová ∗
Plant Pathology Department and Molecular, Cellular and Developmental Biology
Program, Iowa State University, Ames, Iowa 50010-1020;
e-mail: wamiller@iastate.edu; http://www.public.iastate.edu/∼wamiller/
KEY WORDS:
luteovirus, aphid transmission, translation, RNA virus, satellite RNA
ABSTRACT
Barley yellow dwarf viruses represent one of the most economically important
and ubiquitous groups of plant viruses. This review focuses primarily on four
research areas in which progress has been most rapid. These include (a) evidence
supporting reclassification of BYDVs into two genera; (b) elucidation of gene
function and novel mechanisms controlling gene expression; (c) initial forays
into understanding the complex interactions between BYDV virions and their
aphid vectors; and (d ) replication of a BYDV satellite RNA. Economic losses,
symptomatology, and means of control of BYD are also discussed.
INTRODUCTION
Every year barley yellow dwarf viruses (BYDVs) cause substantial losses
throughout the world wherever their hosts, mainly wheat, barley, and oats,
occasionally rice and maize, are grown (57). In addition to their economic importance, the gene expression mechanisms, evolution and taxonomy, satellite
RNA, and intimate interactions with their aphid vectors are quite fascinating
and unlike those of any other viruses. These latter aspects form the subject of
this review. For more comprehensive coverage of barley yellow dwarf disease
and epidemiology the reader is referred to the book, Barley Yellow Dwarf: Forty
Years of Progress (24). This review provides an up-to-date overview focusing
mostly on the viruses rather than the disease or epidemiology, and emphasizing
recent discoveries since the publication of the above book.
∗ Current address:
Plant Pathology Department, University of Wisconsin, Madison, Wisconsin
53706.
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0066-4286/97/0901-0167$08.00
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CLASSIFICATION
Serotypes
BYDVs present challenges in classification. They are members of the luteovirus
group (82), which is defined as having icosahedral, T = 3, 25–30 nm virions that
are nonmechanically transmissible, but rather are transmitted only by aphids
in a persistent, circulative manner; and are confined to the phloem in the plant.
Differences among BYDV isolates were first characterized by Rochow (88, 90),
who identified five isolates from New York that are transmitted preferentially by
different aphid vectors. The isolates and their major vectors (in parentheses) are:
RPV (Rhopalosiphum padi), RMV (Rhopalosiphum maidis), MAV (Sitobion
avenae), SGV (Schizaphis graminum), and PAV (R. padi, S. avenae, and others).
These are distinguishable serologically (114). Laboratories worldwide use
antibodies to classify local isolates into one of the above serotypes. However,
aphid-transmission properties do not always correlate with serotype (21, 58),
and symptoms can vary widely among different PAV isolates (18). Thus, the
simple five-serotype scheme may have been overapplied.
Subgroups
Numerous observations support division of barley yellow dwarf viruses into
two viruses and even into separate genera. The former notion was first proposed based on cytopathological differences (45) and subsequently supported
by serological evidence (114) and, most strikingly, by differences in genome
organization (66, 70) (Figure 1). Currently, the PAV, MAV, and SGV serotypes,
and any isolates that resemble them are subgroup I BYDVs, whereas RPV,
RMV, and isolates that resemble them are members of subgroup II (82). The
International Committee on the Taxonomy of Viruses (ICTV) working group
on luteoviruses is considering a reclassification in which subgroup I serotypes
would be called BYDV, and members of subgroup II would be renamed cereal
yellow dwarf virus (CYDV) (P Waterhouse, personal communication).
This dichotomy extends to other luteoviruses at the level of gene homologies
and organization (discussed in more detail in References 66 and 70). Beet western yellows luteovirus (BWYV) and potato leafroll luteovirus (PLRV) resemble
subgroup II BYDVs. Soybean dwarf luteovirus has a subgroup I-like organization and replicase, but the structural genes are most similar to those of subgroup
II (85). The chasm between subgroups is so deep that the subgroup II BYDVs
are more similar to PLRV and BWYV in genome organization, replication
genes, and cis-acting signals than they are to subgroup I BYDVs. Conversely,
other than in the structural genes, subgroup I BYDVs are more closely related
to SDV than to BYDVs in subgroup II. Hence, the ICTV is also considering
raising each subgroup category to the level of virus group or genus. The groups
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Figure 1 Genome organization of the BYDVs. Boxes indicate open reading frames, numbered
as in Martin et al (63), with molecular weight of protein products in kilodaltons (K). Black-shaded
ORFs are conserved between subgroups. Abbreviations: CP, major coat protein gene; POL, putative
polymerase gene; AT, readthrough domain probably required for aphid transmission; MP?, putative
cell-to-cell movement protein. Checkered POL ORF has homology to Tombusviridae, especially
dianthoviruses. Striped POL ORF is homologous to sobemoviruses. Unshaded ORFs have no
significant similarity to ORFs of any virus, with the exception of a possible protease motif in
ORF 1 of subgroup II. Known positions of subgenomic RNAs are shown below the genomes.
would all be members of the Luteoviridae family. Thus, not only would RPV
and PAV be different viruses, they would be in different genera. This reclassification proposal is supported not only by the major differences discussed above,
but by additional differences between gene function, expression mechanisms,
replication strategies, and the ability to support a satellite RNA, all discussed
in this review.
We compare subgroup I with subgroup II BYDVs, using current nomenclature. PAV is the best studied BYDV, especially at the molecular level. It is also
the most widespread (23) and usually causes the most severe symptoms. RPV
is the best studied subgroup II BYDV, but it is much less well characterized
than other subgroup II luteoviruses (BWYV and PLRV), or PAV. Thus, we refer
to PAV and RPV as representative members of each subgroup, but often use
BWYV or PLRV as additional representatives of subgroup II.
We also compare BYDVs with related viruses outside the luteovirus group.
The polymerase and translational frameshift signals of subgroup I luteoviruses
are more similar to those in red clover necrotic mosaic (RCNMV) and other
dianthoviruses than they are to those in subgroup II luteoviruses (70, 117).
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Conversely, the polymerase genes of subgroup II luteoviruses are most closely
related to those of sobemoviruses. Pea enation mosaic virus (PEMV), the
sole member of the enamovirus group, has two RNAs, each encoding its own
polymerase (27). The polymerase of RNA1 is subgroup II-like (26) and that of
RNA2 is subgroup I-like (28). PEMV is aphid transmissible, probably by the
same mechanism as luteoviruses, but it is also mechanically transmissible (27).
Knowledge about these viruses is applied to BYDVs throughout this review.
ECONOMIC IMPORTANCE
BYDVs can have a serious impact on, and be an important limiting factor for,
grain production wherever cereals are grown. However, global yield losses
due to the BYDVs are difficult to estimate because of insufficient information.
Average yield losses attributable to natural BYDV infection can range between
11 and 33% (57); in some areas the losses were reported to reach up to 86%.
The relationship between the disease incidence and yield loss was found to be
linear in wheat and oats. A 1% increase in BYD disease incidence caused yield
reduction to increase from 20 to 50 kg/ha in wheat and from 30 to 60 kg/ha in
oats (F Nutter, personal communication). Hewings & Eastman (48) calculated
that hypothetical 5% losses caused by BYDVs in the United States in 1989
would result in crop losses valued at $847.0 million for corn, $387.1 million for
wheat, $48.5 million for barley, and $28.0 million for oats. A PAV-like virus
may also cause sugarcane yellow leaf disease in Brazil, Hawaii, and Australia
(104a). Thus the range of economically important crops affected by BYDVs
may be greater than previously thought.
INTERACTIONS WITH PLANTS
The host range of BYDVs consists of more than 150 species in the Poeaceae
(23). An Australian isolate of PAV, but not either of two diverse isolates of
RPV, can replicate in Nicotiana tabacum protoplasts (LR, unpublished). No
BYDV isolate is known that can infect dicot plants.
Symptoms
Symptoms induced by luteoviruses are often difficult to distinguish from symptoms caused by other pathogens, nutritional deficiencies, or cold weather (23).
The symptoms in wheat are not always obvious; often they are limited to stunting
that can result in substantial yield loss while remaining undetected. In contrast,
BYDV causes yellowing and stunting in barley, and yellowing, reddening, leaf
stiffness, reduced tillering and heading, and numerous sterile florets in oats
(23). Recently, a virus serologically related to PAV was found to be associated
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Figure 2 Northern blot hybridization showing viral genomic RNAs isolated from oats inoculated
with various BYDV isolates. Inoculation, RNA extraction, and northern blot hybridization were
performed as described in Reference (84). For each RNA tested, the same blot was hybridized, then
stripped, and reprobed with the three different probes. The 50 RPV(−) and 30 RPV(−) probes are
complementary to the nucleotides 809–1191 and 5026–5723, respectively, of the RPV-NY genome.
The 50 PAV(−) probe is complementary to bases 1–546 of the PAV-IL genome.
with sugarcane yellow leaf disease, which results in yellowing, reddening, and
impaired growth of sugarcane (104a).
BYDV isolates vary greatly in symptom severity. A severe isolate of PAV
(PAV-129) causes stunting and corkscrewing symptoms in otherwise PAVtolerant varieties of oat (18). We have sequenced its genome (5). PAV-129
differs from other sequenced PAV isolates more in the polymerase gene (88%
amino acid sequence identity) than does MAV [98% identity to Australian and
Purdue isolates of PAV (102)]. It also differs the most from ten other PAV
isolates (16) and MAV in the 30 untranslated region of the genome. In contrast,
the coat protein gene of PAV-129 is more PAV-like (87% identity) than MAVlike (70% identity). Thus the virulence determinants are not obvious from the
sequence. A severe isolate of RPV (RPV-Mex1) isolated by Bertschinger at
CIMMYT in Mexico causes severe stunting, corkscrewing, and leaf notches
in wheat. We have sequenced the 30 half of its genome (5). The coat and
readthrough proteins of RPV-NY and RPV-Mex1 have more than 90% similarity except for a ten-codon extension at the carboxy-terminus of the RPV-Mex1
readthrough protein gene. Strikingly, a large region of the 50 half of the genome
bears no homology to either RPV-NY or PAV, based on northern blot hybridization (Figure 2).
Interactions between BYDVs
Cross-protection occurs between BYDVs of subgroup I but not between BYDVs
of subgroup II or between subgroup I and II BYDVs (116). While similar
BYDVs can cross-protect against one another, mixed infections with unrelated
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BYDVs, i.e. one from each subgroup, can have the opposite effect. Mixed
infections of PAV and RPV give more severe symptoms, including more stunting
and higher virus titer, than do infections with either virus alone (1, 73). This
is consistent with the phenomenon observed among many luteo- and luteo-like
viruses (73). In all cases, the synergistic interaction involves a replicating RNA
with a subgroup I-like polymerase and one with a subgroup II-like polymerase,
suggesting a positive interaction between the two polymerases or the RNAs that
they recognize. This interaction has important practical applications. First, it
is unlikely that transgenic plants expressing a subgroup I BYDV polymerase
will be resistant to a subgroup II BYDV. More importantly, such transgenic
plants could be more susceptible than untransformed plants to a virus of the
opposite subgroup if they express the synergy-conferring gene at high enough
levels (73, 104).
GENE FUNCTION
Replication Proteins
Gene functions are not well characterized for BYDVs and are currently under
investigation in many laboratories. Sequence comparisons revealed that open
reading frame (ORF) 2 encodes the catalytic domain of the RNA-dependent
RNA polymerase (Figure 1) (75, 102, 107). There is no evidence that the product of this ORF, P2, is translated by itself in luteoviruses of either subgroup.
Rather, it appears to be expressed only fused to P1 (product of ORF 1) via
translational frameshifting (see Gene Expression), in a P1-2 fusion (Figure 1).
Consistent with a role in RNA replication, deletion mutations in ORFs 1 or 2
of PAV (77) or BWYV (86) destroyed the ability to replicate in plant cells.
Because P1 is expressed by itself (the most abundant form) and fused to P2, it
has two functions. In its rarer form, fused to P2, it is part of the RNA-dependent
RNA polymerase. Its function when expressed by itself is unknown for PAV.
Habili & Symons (46) proposed that it is a helicase. It makes sense that a
replicase-associated protein would have such a function, keeping (+) and (−)
strands apart during RNA synthesis. However, Koonin & Dolja (54) and Gibbs
(39) assert that this ORF has no homology to known helicases and that RNA
viruses with genomes under 6 kb lack helicases.
ORF 1 of subgroup II-like RNA1 of PEMV (26) and all subgroup II luteoviruses including RPV (70) have homology to the catalytic triad of chymostrypsin-like proteases. This implies that the P1-2 fusion protein has a protease
in its N-terminal half, and the polymerase in its C terminus. Such an arrangement resembles poty-, como-, and picornaviruses that have a VPg-proteasepolymerase polyprotein, which subsequently self-cleaves as replication initiates. The VPg is a genome-linked protein covalently attached to the 50 end of
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some viral RNAs including those of subgroup II luteoviruses (64, 78). Thus
we speculated that the VPg of RPV might be encoded in the 50 end of ORF 1,
upstream of the protease domain. However, the Vpg of PLRV was recently
mapped to a position between the protease and polymerase domains (F van
der Wilk, personal communication). Luteoviruses also appear to differ from
others in that the Vpg would be produced in large molar excess to the polymerase which is expressed only as a result of a rare frameshift event (6, 31).
In contrast to our speculation several years ago (76), ORF 4 does not encode
a genome-linked protein (VPg). Despite much phylogenetic (70), biochemical
(98), and genetic (77, 86) evidence that ORF 4 does not encode the VPg, some
researchers still refer to ORF 4 as encoding the VPg. Furthermore, we now have
direct chemical evidence that PAV RNA lacks a VPg (E Allen, unpublished).
Structural Proteins
Much progress has been made recently in elucidating the roles of the proteins
most conserved among all luteoviruses, those encoded by ORFs 3, 4, and 5.
Besides its obvious function in forming virions, the coat protein (encoded by
ORF 3) may have roles in virus movement in plants (119) and in replication.
Mutations that render ORF 3 untranslatable reduced accumulation of genomic
RNA of both BWYV (86) and PAV (77). This may be due to simple increased
sensitivity of the genomic RNA to nucleases during extraction because it cannot
be encapsidated, or the CP may be involved more directly in RNA replication.
The coat protein is obviously required for aphid transmission and it may confer
aphid vector-specificity (see Aphid Transmission).
ORF 5 is expressed as a carboxy-terminal extension to the CP, produced
in low abundance by in-frame readthrough of the CP ORF stop codon (see
Translation, below). The CP and the extended form containing the readthrough
domain (RTD) make up the virion (19, 36, 111), with the RTD probably located
on the surface (35). A significant portion of the C terminus of the RTD is
cleaved proteolytically to give the truncated form of the CP-RTD fusion (MW
51–58 kDa) that is found in purified virions. Substantial evidence indicates that
this truncated CP-RTD is required for aphid transmission (see Aphid Transmission). The C-terminal portion that is cleaved off may be involved in systemic
movement in the plant (see below). None of the RTD is required for virion
formation. Deletions in this ORF in PAV and in BWYV actually increased
RNA replication in protoplasts and did not affect the ability of the RNA to be
encapsidated (77, 86).
Movement Protein
ORF 4 probably codes for a cell-to-cell movement protein. This protein may
facilitate viral genome movement only through the specialized plasmodesmata
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of phloem cells and thus explain confinement of virus to these cell types. P4
of PLRV has many of the biochemical properties expected of a movement
protein. It binds single-stranded nucleic acid nonspecifically (97); it has a
protein-protein binding domain (99); and it localizes to the membrane fraction
[referred to in (98)]. Knocking out ORF 4 (but not the overlapping CP gene)
did not affect accumulation of PAV (77) or BWYV (119) in protoplasts. PAV
mutants containing this mutation could not be transmitted to plants (17). Virus
from protoplasts mixedly infected with two mutant PAVs, one containing this
ORF 4 knock-out mutation and the other containing a deletion in ORF 5, was
able to infect plants. The only viral genome that accumulated in plants from
this mixed inoculum was that containing the deletion in ORF 5 (17). Thus P4
is required for systemic infection of plants but not for infection of protoplasts.
This is consistent with a cell-to-cell movement function. In contrast, ZieglerGraff et al (119) constructed a mutant BWYV genome with three stop codons
interrupting ORF 4. Progeny virus replicated well, maintained the mutations,
and was aphid transmissible to other hosts. In both PAV (17) and BWYV (7),
mutations in the RTD reduced virus titer in plants, leading Ziegler-Graff et al
(119) to propose that a domain in the C terminus of the RTD was required for
movement in the plant, perhaps redundant to, or stimulated by, the P4 function.
GENE EXPRESSION
BYDVs use a combination of RNA-templated transcription and noncanonical translation mechanisms to express their six genes from a single genomic
RNA. One of the most remarkable features of BYDVs, PAV in particular, is
the plethora of unusual mechanisms by which the genes are translated. These
include cap-independent translation, ribosomal frameshifting, in-frame stop
codon readthrough, and leaky scanning [reviewed in more detail in References
(66, 70, and 69)].
Subgenomic RNA Synthesis
Viral RNAs with 50 truncations but the same 30 ends as genomic RNA are generated in infected cells. These subgenomic RNAs serve as messages for the
50 -distal open reading frames. The 50 end of subgenomic RNA 1 (sgRNA1) of
PAV has been mapped to base 2769 by Dinesh-Kumar et al (32), and to base
2670 by Kelly et al (52). This difference may be due to strain variation, but we
now have data that support the base 2670 start site (G Koev, personal communication). The apparent 50 end of 2769 is probably incorrect owing to an unlucky
combination of misleading results. The 50 end determined by Kelly is appealing
because it shares sequence with the 50 end of the genome: (A) GUGAAG (A
in parentheses is absent in sgRNA1), and is similar to the 50 end of sgRNA2 at
base 4809: AGUGAAGA (52). SgRNA1 is the mRNA for ORFs 3, 4, and 5
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(32). SgRNA2 can act as mRNA for ORF 6 in vitro (52). The first ten codons
of ORF 6 vary only in the wobble position giving silent mutations (no change in
amino acid sequence), suggesting that its product, P6, is functional. However,
the remaining codons are not conserved, as the rest of the ORF is the most
variable region in the BYDV genome (16). P6 has not been detected in vivo,
despite considerable efforts (M Young, personal communication). Mutation of
the ORF6 start codon reduces but does not eliminate genomic RNA replication
in protoplasts (77). The role of sgRNA3, which seems to have no message
function and which differs at its 50 terminus (GACGACC) (52) from the other
viral RNAs, is unknown.
Subgroup II BYDV sgRNAs have not been studied, but the 50 ends of genomic
and sgRNAs of other subgroup II luteoviruses begin in ACAAA (68), as does
genomic RNA. This sequence is also present within 20 bases of the 50 ends of
PAV genomic and sgRNAs (70). One candidate start site for sgRNA1 of RPV
(70) at base 3576 begins in ACAAACGUA, which is a perfect match with the
start site of RCNMV sgRNA1 (118). If this is the start site for RPV sgRNA, we
can expect that subgenomic promoter analysis of RCNMV may apply to RPV.
Alteration of the ACAAA to ACUAA in an infectious transcript of RCNMV had
little effect on sgRNA synthesis (118). Changes that may weaken a proposed
minus-strand stem-loop structure, which flanks the complement of the RCNMV
sgRNA1 50 end, eliminated sgRNA synthesis (118). However, whether it is
secondary structure or actual RNA sequence that provides promoter function
was not determined. In our laboratory, mutations at bases flanking the PAV
sgRNA1 start at base 2670 knocked out sgRNA1 synthesis with little effect on
genomic RNA replication (BR Mohan, personal communication). Alteration
of the ORF6 start codon to AUC abolished accumulation of sgRNA2 (77).
Either this mutation disrupted the promoter of sgRNA2, which begins 114 bases
upstream, or by making sgRNA2 untranslatable, the stability is decreased.
It has been assumed that sgRNAs are synthesized by internal initiation of
the polymerase on full-length minus stranded RNA (118), based on studies of
brome mosaic (71) and other viruses. This may be the case for BYDVs, but
also plausible is the possibility that the replicase terminates prematurely at a
defined site during minus strand synthesis (69). Plus strand synthesis would then
initiate at the 30 end of this 30 terminally truncated minus stranded RNA to make
plus stranded sgRNA. The extensive homology between 50 termini of genomic
and sgRNAs, and the abundant, subgenomic-sized double-stranded RNAs in
BYDV-infected tissue (42), support this possibility. Functional dissection of
subgenomic promoters will determine which mechanism applies.
Translation
In all luteoviruses, ORFs 3 and 4, and in subgroup II luteoviruses, ORFs 0 and 1 (65, 106, 119), are translated by leaky scanning.
LEAKY SCANNING
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According to this mechanism, if the first (50 -proximal) AUG on an mRNA
is in a poor context, some scanning ribosomes can ignore this AUG and start
protein synthesis at the second AUG. The AUGs of ORFs 4 and 1 are the second
AUGs on their mRNAs and are indeed in better contexts than the first AUGs,
which initiate ORFs 3 and 0, respectively (70). Both products of ORFs 3 and 4
(CP and P4) can be translated from sgRNA1 of PAV (32), RPV (108), BWYV
(105), and PLRV (96). In addition to the primary sequence context controlling
AUG choice as expected, further observations led us to propose a new mechanism by which pausing of ribosomes during initiation at the second (ORF 4)
AUG transiently “melts” secondary structure, which enhances initiation at the
upstream (ORF 3) AUG by the following ribosome (33). The arrangement of
ORF 4 completely nested within, and out of frame of, ORF 3 led to the hypothesis that ORF 4 evolved relatively recently as a kind of accident during
out-of-frame translation of ORF 3 (51).
RIBOSOMAL FRAMESHIFTING In all luteoviruses, the polymerase is translated
by minus 1 (−1) ribosomal frameshifting. During the elongation process in
translation of ORF 1, a small fraction of translating ribosomes slip back one
base at a specific sequence, called the shifty heptanucleotide, and then resume
translation in a new reading frame. This shift allows the ribosomes to bypass
the stop codon of ORF 1. This has been demonstrated for several luteoviruses
including PAV (6, 31, 38, 70). The consensus signals known to facilitate −1
frameshifting for polymerase expression in corona-, retro-, and yeast viruses
are the shifty site with the consensus XXXYYYZ, followed by a region of
substantial secondary structure, usually a pseudoknot (34). These sequences
and structures are present or predicted in all luteoviruses (70). They are also
present in other −1 frameshifting plant viruses, all of which are members
of the groups most closely related to luteoviruses, including cocksfoot mottle
sobemovirus (61), both PEMV RNAs (26, 28), and the dianthoviruses (53). The
actual frameshift signals differ between the subgroups. PAV and MAV have
GGGUUUU as the shifty site, followed by a region that can be folded into two
stem-loops in which the loops base-pair to each other, or into a large stem-loop
(6). We favor the latter structure, based on phylogenetic comparisons (70). A
shifty site of GGGAAAC followed by a small, conserved pseudoknot has been
found for BWYV (38) and predicted for RPV (70).
More recently, we found an additional sequence required for frameshifting by
PAV. Remarkably, it is located four kilobases downstream of the frameshift site
(113)! In vitro translation of PAV genomic RNA transcripts carrying various
deletions revealed that a region 30 of, and possibly including, ORF 6 is necessary
to achive full −1 frameshifting in wheat germ extracts (Figure 3; C Paul,
personal communication). This is higher than the very low level observed in
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Figure 3 Map of cis-acting signals regulating PAV RNA translation (69). Bold line indicates
RNA on which boxes with different fill patterns demarcate the locations of sequences required for
the indicated translational event. Solid-headed arrows indicated long-distance interactions. Openheaded arrows indicate subgenomic RNA synthesis. sgRNA3 is not shown because it contains no
ORFs and does not appear to be translated (52). Reprinted with permission of Academic Press.
reporter gene studies in oat cells using constructs that lacked the downstream
region (6). We have no idea of the mechanism, but this is only the first example
of downstream elements controlling translation of PAV RNA (see below).
READTHROUGH As mentioned above, ORF 5 is expressed by readthrough of
the coat protein gene stop codon during translation of sgRNA1 (32), i.e. when
the ribosomes reach the stop codon, a small portion of them do not stop, but
continue translating in the same frame 30 of the stop codon. The actual rate of
readthrough is difficult to estimate because the ratio of CP-RTD fusion protein
to CP in purified virions varies greatly (between 1:100 and 1:4) among BYDV
serotypes (36, 111) and even among individual virus preparations. In the most
reliable cell-free wheat germ translation system, the rate was about one percent.
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Researchers in our laboratory studied the cis-acting signals required for
readthrough of the PAV CP ORF stop codon by translating an in vitro transcript
of sgRNA1 containing various mutations (8). In addition, these mutations were
placed in a PAV cDNA clone such that resulting infectious transcripts contained
a modified reporter gene (GUS) inserted in ORF 5 so that readthrough of the CP
gene stop codon was required for GUS activity in oat protoplasts. Using these
two assays, two regions 30 to the stop codon were identified as necessary for
readthrough (8). One is a repeated sequence motif: CCN NNN, located about
20 bases 30 to the stop codon. A second sequence, located 697 to 758 bases
30 of the stop codon, was also required (Figure 3). It occurs naturally within
ORF 5, but functions well in the GUS-expressing virus, in which it is located
two kilobases downstream of the CP stop codon and in the untranslated region
following the GUS ORF. Highly conserved bases at and flanking the CP stop
codon were not necessary. Deletions in and around the homologous regions
in infectious clones of BWYV also destroyed or greatly reduced accumulation
of RTD in infected plants (11). In PEMV, a single, naturally occurring base
change in the region homologous to the downstream readthrough element of
PAV prevented readthrough and aphid transmissibility of the virus (29).
As in the case of frameshifting, we do not know the mechanism of readthrough. Long-distance base-pairing between the two required sequence elements can be imagined (8) but this is not conserved among luteoviruses. Gibbs
& Cooper provided evolutionary evidence that these two regions may interact during RNA replication (40). They proposed that strand-switching by the
replicase facilitated recombination at these sites. Furthermore, Demler et al
(29) found a natural PEMV deletion mutant in which a large region of the
readthrough ORF, including portions of the proximal and distal elements and
all the sequence between them, was deleted. This deletion could be explained
by an intramolecular strand-switching event that would be favored if the two
sequence elements were located in close proximity. If they are in proximity during replication, they could also interact during translation, and facilitate
readthrough. The only type of readthrough control that remotely resembles this
is that of selenocysteine-encoding genes. A sequence called the SECIS element
in the 30 UTR, located kilobases downstream of a UGA (stop) codon, facilitates
recognition of the UGA codon by a special tRNA charged with the amino acid
selenocysteine (109). The luteovirus readthrough resembles this only in that
the distal element functions at large, variable distances downstream. There is
no structural similarity, nor is readthrough dependent on a UGA or any other
particular stop codon (8).
CAP-INDEPENDENT TRANSLATION SIGNAL IN THE 30 UNTRANSLATED REGION OF
PAV RNA An unexpected finding was that a sequence we call the 30 translation
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enhancer (30 TE), located between ORFs 5 and 6, confers very efficient translation on mRNAs lacking the 50 cap structure that is normally required for
translation of eukaryotic mRNAs (Figure 3) (113). In order for the 30 TE to
function, the mRNA must also contain the 50 UTR of either PAV genomic RNA
or sgRNA1. This cap-independent translation has been observed in wheat germ
translation extracts (113) and in oat protoplasts (112). Deletion or mutation of
the 30 TE reduces translation of uncapped mRNA by more than an order of
magnitude and renders the virus unable to replicate (112). Addition of a cap
restores translatability (113). The only other known eukaryotic mRNA that has
a cap-independent translation signal in its 30 UTR is satellite tobacco necrosis
virus (STNV) RNA (25, 101). There is little or no sequence homology between
STNV and PAV RNA. However, a portion of the 30 TE sequence is conserved in
all subgroup I luteoviruses and in the 30 UTR of tobacco necrosis virus (TNV)
RNA, the helper for STNV. Because TNV RNA is naturally uncapped, the sequence homologous to the 30 TE may facilitate translation initiation. As we
would expect, PAV RNA also appears to lack a 50 cap (112; WAM, unpublished). This 30 TE phenomenon may be confined to subgroup I luteovirus and
TNV RNAs. No sequence with homology to the 30 TE was detected in subgroup
II luteoviruses, even though it is expected that subgroup II luteoviral genomes
would also translate cap-independently because other VPg-containing genomes
can do so (14, 91).
APHID TRANSMISSION OF BYDVS
BYDV virions pass through at least three barriers in the aphid (Figure 4) by
specific uptake. They do not replicate in the aphid. Each BYDV serotype is
Figure 4 Schematic diagram of aphid feeding and luteovirus transmission (from Reference 17).
Arrows indicate circulative pathway of transmission. ASG, the accessory salivary gland; HG,
hindgut; MG, midgut; PSG, principle salivary gland.
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transmitted efficiently by only a limited number of aphid species (80). The vector specificity of BYDVs does not always correlate with serotype (47, 56, 58).
For example, Creamer & Falk (21) described an RPV isolate from California
(RPV-CA) that is transmitted efficiently by Sitobion avenae, which gives it the
transmission phenotype of PAV. The genomes of RPV-CA and the type RPVNY isolate exhibit sequence homology in the 30 halves but are unrelated in their
50 halves, based on the northern blot hybridization (Figure 2). The transmission
phenotypes of BYDVs also may be altered transiently by heterologous encapsidation during mixed infections (22, 89, 115). (For more detailed discussions
of aphid transmissiion, see References 45a and 80.)
Role of the Readthrough Domain
Aphid transmission of luteoviruses requires that the genome be encapsidated
(17). BYDV virions contain 180 subunits of CP (82). A few copies of CP in the
virion also contain the RTD discussed above (36, 111). BYDV mutants deficient
in the RTD can form virus particles (36, 77) but are not aphid transmissible (17).
These experiments can be difficult to interpret because a portion of the RTD
may also be required for efficient virus movement within the plant (7). Chay et
al (17) avoided this problem by using a complementation experiment in which
an RTD mutant that replicated better than wild-type RNA in protoplasts was
heterologously encapsidated in wild-type CP and CP-RTD that were provided
by a co-infecting PAV transcript containing a mutation in another gene. The
RTD mutant RNA could then be transmitted by aphids to plants, in which it
replicated and spread. The virus in these plants could not be transmitted by
aphids. Thus the absence of aphid transmission of the RTD mutant that was
observed originally was not due to an inability to replicate or spread in the
plant. Similarly, mutations in ORF 5 of BWYV knocked out its ability to
be transmitted by aphids to plants (7, 11). In these experiments, infectious
DNA clones of the virus were transmitted to Nicotiana clevelandii plants by
Agrobacterium-mediated inoculation. Those with mutations in ORF 5 were
not transmittable by aphids to other plants. As mentioned previously, BYDV
virions purified from plants contain an approximately 50-kDa, C-terminally
truncated form of the RTD (19, 36, 111), suggesting that the amino terminal
half of the RTD provides the aphid transmission function.
Interactions within the Aphid
How do the CP and RTD interact with the aphid? After acquisition from the
phloem, virions are transported to the aphid hindgut. The virus must then
cross three distinct transmission barriers to complete the transmission process
(Figure 4) (41, 43). The first barrier is the hindgut epithelium. The virus is
transported into the hemocoel in coated vesicles (41). The recognition at the
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hindgut membrane appears to be luteovirus-specific but not serotype-specific,
as most BYDVs can be acquired into hemolymph of both vectors and nonvectors, whereas unrelated viruses, such as BMV, that are not transmitted in a
circulative manner are excluded. It is likely that a hindgut receptor interacts
with CP domain(s) shared among most BYDVs (18, 41). The readthrough protein appears not to be required for the translocation of BYDV virions across
the hindgut membrane because PAV mutants lacking the RTD still accumulate
in the hemolymph (17).
IN THE HEMOLYMPH Infectious virus can remain in the hemolymph for the life
of the aphid if the aphid is not continuously feeding (80). Virions may persist
by interacting with the most abundant protein in the aphid, called symbionin,
that is produced by a bacterial endosymbiont. Symbionin is closely related to
heat-shock proteins in the GroEL family. GroEL is a chaperonin, i.e. a protein
that facilitates proper folding of other proteins. Van den Heuvel et al (103) reported in vitro binding of PLRV virions to symbionin. In vitro, PAV virions, and
RTD in particular, specifically bind symbionin (SymL) isolated from R. padi
and S. avenae, but not GroEL (35). PLRV was reported to bind symbionin-like
molecules from both vectors and nonvectors (103). Therefore, it is unlikely
that symbionin determines vector specificity of luteoviruses. Van den Heuvel
et al (103) speculated that the interaction between virions and symbionin is
involved in maintaining virus integrity and thus infectivity. Symbionin binding
may also permit the virus to evade the aphid immune system (45a). Filichkin
et al (35) proposed that the interaction occurs with the N terminus of the RTD
that is conserved among luteoviruses. If the purpose of the interaction is indeed
to stabilize virions, localization of binding to the RTD appears to be inconsistent with the observations of Chay et al (17) who detected virions lacking
RTD in hemolymph (above). However, the level of virus lacking RTD was
possibly reduced to a level below a threshold required for aphid transmission,
but still detectable by the PCR method they used (17). Treatment of aphids
with antibiotics to kill the endosymbiotic bacteria and purge symbionin from
the hemolymph inhibited the ability of aphids to transmit luteoviruses (103).
However, this treatment made the aphids sick and thus may have inhibited
their ability to transmit virus only indirectly. The biological role of symbionin
remains to be demonstrated.
ENTERING THE ACCESSORY SALIVARY GLAND Once the virus reaches the accessory salivary gland (ASG) it must penetrate the ASG basal lamina and plasmalemma to be released into salivary canals and ducts (Figure 4). The virus is
then excreted in the aphid saliva during the feeding. Both basal lamina and basal
plasmalemma of ASG have been implicated in vector-specific transmission of
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BYDVs (43, 80). The association of BYDVs with basal lamina probably requires specific interaction between the BYDV capsid and binding sites on basal
lamina (43). PAV and MAV virions did not attach to the basal lamina of nonvectors. Similarly, BMV virions failed to accumulate in the basal lamina when
injected into the aphid’s hemocoel. However, RPV did concentrate in basal
lamina of a nonvector but was unable to cross the ASG basal plasmalemma
(44).
The transport of BYDVs across the ASG plasmalemma occurs in coated
vesicles, probably via a receptor-mediated endocytosis (41). The receptor on
the ASG plasmalemma as well as domains on BYDV virions that interact with
the receptor are unknown, and identification of these entities is a major goal
of current research. Because the RTD is not required for virions to enter the
hemocoel, but is required for aphid transmission, it may be required for transport of luteoviruses across the ASG membranes (17). The coat protein may be
the major determinant of vector specificity. By examining exchanges of regions
of the CP gene between infectious genomic clones from serotypes with different vector specificities, Young and colleagues found that a portion of the CP
itself seemed to harbor the vector-specificity determinant (M Young, personal
communication). Thus, even though the RTD is required for transmission, it
may not be the component that determines the precise vector specificity that
distinguishes BYDV isolates.
SATELLITE RNA
During the process of genome sequencing, a 322-nt, single-stranded, noncoding
satellite RNA (satRPV RNA) was discovered serendipitously in an Australian
isolate of RPV (72). This mysterious RNA is difficult or impossible to detect
in the field and has been found only in Australian RPV-like isolates only after
greenhouse propagation. It has no significant sequence similarity to BYDV
genomic RNA (72) and it depends on RPV genomic RNA for replication (93).
SatRPV RNA is the only known satellite of a luteovirus, although a different
class of satellite RNAs is associated with some luteo-like viruses (27).
SatRPV RNA replicates by a symmetrical rolling circle mechanism (93).
This resembles that of satRNA of tobacco ringspot virus (satTRSV RNA) (10)
and several other viroid-like satellite RNAs (9). Linear and circular monomers
and linear multimeric replication intermediates of both strands, which are
formed during replication by this mechanism, were detected in satRPV RNAinfected cells (93). Newly formed multimers self-cleave into monomers in
vitro at sequences that fold into hammerhead ribozyme structures, one in each
strand (72). The (+) strand hammerhead is an unusual derivation from the
consensus structure. It has additional base-pairing that results in a pseudoknot
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that inhibits self-cleavage (74). This alternative conformation may serve as a
molecular switch. The hammerhead conformation performs the self-cleavage
function, and the pseudoknot conformation is required for some other step of
replication (M Aulik, personal communication).
The known range of helper viruses that support satRPV RNA is limited to
subgroup II luteoviruses. RPV and BWYV support satRPV RNA replication
(83). PAV and a BWYV-associated RNA (ST9a RNA), which encodes a subgroup I-like polymerase, do not replicate satRPV RNA (83, 93). SatRPV RNA
can be transmitted to plants by aphids that acquired virus from infected protoplasts. It reduces accumulation of RPV helper virus RNA in oat plants and
protoplasts, and ameliorates symptoms caused by RPV in oats (84). SatRPV
RNA had no effect on PAV RNA accumulation and did not affect symptoms
caused by the severe mixed infection of RPV and PAV BYDVs in oats (84)
or by BWYV and ST9a RNA in shepherd’s purse plants (83). SatRPV RNA
symptom modulation seems to be determined by the competition between the
satRPV RNA and its helper virus for both replication and encapsidation. Because satRPV RNA can replicate and move systemically in monocotyledonous
and dicotyledonous hosts, the helper virus (probably the replicase gene) and not
the type of plant host range is the limiting factor for satRPV RNA replication
(83).
DISEASE CONTROL
BYDV is controlled mainly by the use of plant lines that are tolerant or resistant to certain BYDV isolates to varying degrees. Spread of the disease can
be controlled by aphicides (67a) or by carefully timed planting when aphid
populations are monitored (79). However, this is economically feasible only in
the most intensive agricultural systems. Usually, especially in the developing
world where disease pressure is high, growers simply live with losses to BYDV.
Breeding for resistance, either by conventional or transgenic methods, remains
the most feasible means of disease control.
Natural Tolerance to BYDVs
Well-characterized resistance genes to BYDVs are few. Tolerance is conditioned by one to four genes in oats (13). In general, tolerance or resistance is
specific only against certain isolates of a serotype or subgroup (45b). A single
partially dominant gene, Bdv1, confers tolerance to BYDV in some wheat varieties (94). Genes of resistant wild wheatgrasses (Thinopyrum or Agronpyron
species) have been introgressed into wheat in interspecific crosses to produce
wheat lines containing a portion of the wheatgrass chromosome that confers
substantial resistance to BYDVs (2, 55, 92). The best characterized resistance
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to BYDV is conditioned by the Yd2 gene in barley, which confers resistance
only to subgroup I BYDVs (1, 12). Barley lines containing the Yd2 gene express
a unique polypeptide that is tightly linked to Yd2 (49). It encodes a putative
subunit of a vacuolar proton-translocating ATPase (37). A high-resolution map
of chromosome 3H around the Yd2 locus has been generated, and cloning of
the Yd2 gene is imminent (37). This will provide a major breakthrough in our
understanding of BYDV-plant interactions.
Transgenic Resistance
Research on transgenic resistance to BYDVs has until recently lagged behind
that of other viruses because of the absence of efficient transformation methods
of hosts of BYDVs. PLRV has become a model for transgenic resistance to
luteoviruses, mainly because of the ease of transformation of potato. Genes
encoding coat protein (3, 50), replicase (100), or putative movement protein
(98) have been reported to confer resistance. In one case, potato plants lacking the transgene acquired resistance during the transformation process (81),
presumably owing to somaclonal variation. Potato plants expressing P4 were
more resistant to potato viruses X and Y than to PLRV (98). The replicase
genes have provided a high level of resistance to PLRV in several generations
of field trials in northeastern Oregon (100).
Now that transformation of wheat (4), barley (110), and oats (95) is routine, several groups have transformed these hosts with BYDV genes, but as of
this writing, we are unaware of any examples of resistance published in peerreviewed journals. Lemaux et al generated barley transgenic for the PAV CP
(110), some of which were reported at a scientific meeting to be resistant (60).
Other transgenic resistance reported only at meetings include coat proteinmediated resistance in oats (59) and wheat (20, 67). In collaboration with
D Somers (University of Minnesota), we have transformed oat plants with the
replicase gene of PAV. One resulting tolerant line lacked a transgene, suggesting
somaclonal variation. A transgenic tolerant line showed a recovery phenotype
in which symptoms decreased with time after inoculation (G Koev, personal
communication). However, none of the lines was immune to BYDV infection.
Stable, effective transgenic resistance to BYDV may have been achieved in
other labs but not disclosed because of the proprietary nature of the research.
In the near future, barring unforeseen regulatory barriers, transgenic resistance
to BYDV will be available publicly in cultivars of wheat, barley, and oats.
SUMMARY
Because of the economic importance of the BYDVS, more research is needed.
There are surprisingly few data on the dollar value of yield reduction caused
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by the BYDVs. The specific locations and timing of virus outbreaks, and the
particular causal isolates, need to be monitored. This is will allow breeders
to decide which BYDV isolate to target with transgenic resistance in a given
locality. It will help growers decide whether to pay the extra premium for
BYDV-resistant crops. Another area of applied research may be to engineer
aphid-resistant crops. This could obviate the need for BYDV resistance.
BYDVs have become a surprisingly valuable source of basic research knowledge. Studies of PAV have provided fascinating insight into mechanisms of decoding the genetic code not known previously in any organism (69). Structurefunction analyses of the self-cleavage structure in the satellite RNA of RPV (74)
contributed to understanding of the three-dimensional structure of hammerhead
ribozymes (15). Hammerhead ribozymes have great potential as anticancer and
antiviral therapeutics. The work on aphid transmission is providing fascinating
new knowledge of insect cell biology and physiology. Progress since the first
review on luteovirus molecular biology in 1990 (63) has been immense, but it
has only opened up more avenues for research and heightened the excitement
about future studies.
ACKNOWLEDGMENTS
The authors thank M Young, F Nutter, E Allen, BR Mohan, S Wang, R Beckett,
C Paul, M Aulik, and G Koev for making unpublished data available, and
S Gray for providing Figure 4 and reviewing the manuscript. This work was
funded in part by grants from the USDA Risk Assessment Grants Program no.
94-39210-0531, and USDA National Research Initiative grant no. 94-373030469. This is paper No. J-17193 of the Iowa State University Agricultural and
Home Economics Experiment Station Project 3270, and supported by Hatch
Act and State of Iowa funds.
Visit the Annual Reviews home page at
http://www.annurev.org.
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