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J Virol, July 1998, p. 6247-6250, Vol. 72, No. 7
0022-538X/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
A Single Amino Acid Change in Turnip Crinkle Virus
Movement Protein p8 Affects RNA Binding and Virulence on
Arabidopsis thaliana
Kristin K.
Wobbe,1,2,3
Muslum
Akgoz,3
D'Maris Amick
Dempsey,1 and
Daniel F.
Klessig1,*
Waksman Institute and Department of Molecular
Biology and Biochemistry, Rutgers, the State University of New Jersey,
Piscataway, New Jersey 08854-80201;
Department of Molecular Biology, Massachusetts General
Hospital, Boston, Massachusetts 021142; and
Department of Chemistry and Biochemistry, Worcester
Polytechnic Institute, Worcester, Massachusetts 016093
Received 16 January 1998/Accepted 16 April 1998
 |
ABSTRACT |
Comparison of the symptoms caused by turnip crinkle virus strain M
(TCV-M) and TCV-B infection of a resistant Arabidopsis thaliana line termed Di-17 demonstrates that TCV-B has a greater ability to spread in planta. This ability is due to a single amino acid
change in the viral movement protein p8 and inversely correlates with
p8 RNA binding affinity.
| |
TEXT |
The mechanisms by which viruses move
in plants are not yet well understood. It has long been known that
viral proteins are essential to this process, and in the past few years
rapid progress has been made in determining their functions (for recent
reviews, see references 3, 9, 10, 11, 25, and
26). Cell-to-cell movement of turnip crinkle virus
(TCV), a member of the carmovirus group, requires the presence of two
small proteins, p8 and p9 (12), and in some hosts the coat
protein is also required (12, 19). Currently, the process by
which TCV moves from cell to cell is unknown, and the biochemical
functions of the proteins involved have not been elucidated.
An Arabidopsis thaliana line termed Di-17 that uniformly
developed necrotic lesions when inoculated with the M strain of TCV has
been derived from ecotype Di-0 (7). Viral RNA was restricted to these lesions and, for the most part, the remainder of the Di-17
plants exhibited no further symptoms. Therefore, these lesions appear
to be part of a resistance-associated phenomenon known as the
hypersensitive response (HR). Despite the development of an HR, a small
percentage (0 to 25%) of Di-17 plants developed systemic disease
symptoms 1 to 3 weeks postinoculation (p.i.), indicating that the virus
had spread to the uninoculated portions of the plant (7).
TCV-M is associated with a virulent satellite (Sat C), whose presence
intensifies the symptoms developed by turnip and susceptible ecotypes
of Arabidopsis (1, 21, 27, 28). This effect
appears to be dependent on the TCV coat protein (16, 17).
TCV-B is more virulent than TCV-M on Di-17 plants.
To
determine if the spread of TCV-M in Di-17 plants is influenced by the
presence of Sat C, the symptoms exhibited by TCV-M-infected plants were
compared with those produced by inoculation with TCV-B, a closely
related strain of TCV (2, 23) that does not carry Sat C. All
inoculations were carried out as previously described (7).
In three independent experiments, a minimum of 23 Di-17 plants were
inoculated with virions of either TCV-M or TCV-B. All of the plants
developed lesions synchronously at 3 days p.i. By 3 weeks after
inoculation with TCV-M, 23% of the plants (average of three
experiments) showed mild systemic symptoms. However, 69% of the plants
inoculated with TCV-B developed systemic disease symptoms, a threefold
increase over the percentage of plants inoculated with TCV-M. These
symptoms appeared at approximately the same time and were of similar
severity as those caused by TCV-M (i.e., curling of the bolt and vein
clearing of the cauline leaves; data not shown). The mild symptoms
correlated with the presence of viral RNA (data not shown).
Though TCV-B is not associated with Sat C, it contains a defective
interfering (DI) RNA, DI RNA G, which increases the disease severity on
susceptible cruciferous plants (20). To eliminate effects
due to the different small RNAs, we obtained the genomic clones for
each virus (2, 23). These were used to produce genomic RNA
in vitro (13, 14), which was passaged through turnip to
obtain large amounts of highly infectious viral RNA. This RNA was
normalized by visualization on ethidium-bromide-stained gels (data not
shown); this analysis also demonstrated the absence of small DI and Sat
RNAs (data not shown).
Following inoculation with the Sat- and DI-free forms of the TCV RNAs
obtained from infected turnip, all of the Di-17 plants
developed
lesions. As was previously observed with the virions,
there was a large
disparity in the number of plants that developed
systemic disease
symptoms. RNA synthesized from TCVms (the TCV-M
genomic clone) produced
systemic disease symptoms in 16% of the
plants, while that from pT1d1
(the TCV-B genomic clone) caused
disease in 53%. These disease
symptoms have been correlated with
the presence of TCV RNA (data not
shown). Because this disparity
in systemic infection was observed in
the absence of symptom-altering
Sat and DI RNAs, the high level of
virulence of TCV-B appears
to be due to genomic differences between the
two viruses.
The movement protein domain of TCV-B causes larger lesions and
increased virulence.
The genomes of TCV-B and TCV-M have
previously been cloned and sequenced and shown to contain 16 nucleotide
differences which are scattered throughout the genome (Fig.
1A and references 2, 6, and 23). Of these 16 nucleotide changes, 4 result
in changes at the amino acid level, 1 results in changes in the
replicase coding sequences, 1 results in changes in p8, and 2 result in changes in the coat protein.
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FIG. 1.
Structure of TCV and chimeric genomes and their effects
on lesion size and virulence. (A) Genetic organization of TCV. The
positions and functions of the TCV open reading frames are diagrammed.
The boxes below represent TCV-M and TCV-B sequences. The vertical bars
between the boxes denote nucleotide changes that are silent at the
protein level, while the asterisks represent nucleotide changes that
result in different amino acids in the proteins. The locations of the
restriction enzyme sites used to produce the chimeric genomic clones
are shown. The sizes of the fragments produced by these enzymes are
noted at the bottom of panel A. (B) Sizes of lesions produced by
chimeric genomes. The genomes are represented by a three-letter code
wherein the first letter represents the origin of the replicase region,
TCV-B (B) or TCV-M (M), the second letter represents the origin of the
p8 and p9 regions, and the third letter represents the origin of the
coat and 3' end. The lesions produced by all possible combinations of
the three TCV regions were measured with verniers at 3 (hatched bars)
and 6 (solid bars) days p.i. Each bar on the graph represents the
average of 20 lesions produced by each chimeric genome on several
plants. The standard deviations (error bars) are noted on the graph. As
the lesions are not completely symmetrical, the smallest axis was
chosen for measurement. (C) Virulence of different chimeric genomes.
Plants inoculated with the chimeric genomes were observed for 3 weeks
p.i. and scored for the presence of disease symptoms in uninoculated
portions. For each experiment, the genome causing the highest
percentage of plants with systemic disease symptoms was given the value
of 100%, and the remaining genomes were expressed as relative
percentages. This experiment was performed six times, and the total
relative percentage was averaged over each of the six independent
experiments. This procedure was necessary due to variability from
experiment to experiment in the absolute numbers of plants that
developed symptoms due to environmental effects. Standard deviations
(error bars) are noted on the graph.
|
|
To identify the alteration(s) responsible for the difference in
virulence on Di-17 plants, a series of chimeric viral genomic
clones
were produced. The genomic clones of TCV-B and TCV-M were
divided into
three regions, using internal
EcoRI and
BglI
sites
and an
XbaI site from the vector at the 3' end of the
genome to
produce all possible chimeras. In vitro-synthesized genomes
were
then passaged through turnip, and the level of viral RNA was
quantitated
and normalized as before.
All Di-17 plants inoculated with the chimeric RNAs developed lesions on
the inoculated leaves. These lesions, however, differed
markedly in
size at 3 days p.i. and later at 6 days p.i. (Fig.
1B). Based on the
sizes of these lesions, the chimeric genomes
could be divided into two
groups: all viruses containing the TCV-B
movement domain produced
lesions that were roughly 40% larger
than those caused by chimeras
containing the TCV-M movement domain.
The prevalence of systemically infected Di-17 plants was also monitored
(Fig.
1C). As before, the chimeric clones could be
divided into two
groups, based on the percentage of inoculated
plants that developed
systemic symptoms. Because the actual number
of plants that developed
systemic symptoms varied somewhat from
experiment to experiment, all
data are expressed as the relative
percentages of plants that developed
disease symptoms. Averaging
the results from six independent
experiments, each of which encompassed
15 to 35 plants inoculated with
RNA from either chimeric clone,
indicated that RNAs containing the
movement region from TCV-M
induced systemic disease symptoms in 20 to
30% (relative) of the
plants, while those containing the movement
region from TCV-B
induced systemic disease symptoms in 80 to 90%
(relative) of the
plants. Therefore, the increase in virulence
correlates with the
development of larger lesions, and both phenotypes
map to the
421-nt region encoding the movement proteins (MPs) of TCV-B.
The p8 MPs of TCV-B and TCV-M differ at one amino acid.
Sequence analysis of the MP domains from TCV-B and TCV-M revealed a
single nucleotide difference (data not shown; 2, 6, 23). This G
A transition changes amino acid 25 of the p8 MP from lysine in TCV-M to glutamate in TCV-B (Fig.
2). Interestingly, the surrounding
peptide sequence (Fig. 2) reveals that this region of p8 is highly
basic, containing either eight (TCV-B) or nine (TCV-M) basic residues
in a region of 14 amino acids whose overall charge is +7 or +9,
respectively. It is significant that the chimeras MBM and BMB are the
equivalents of reciprocal site-directed mutants of TCV-M and TCV-B,
respectively, since there is only one nucleotide difference between
these and their parent clones, MMM and BBB. This has been confirmed by
sequence analysis of the MP domains from MBM and BMB (data not shown).
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FIG. 2.
Fine map of the region encoding the movement proteins.
The 0.42-kb EcoRI-to-BglI movement region is
represented by the open box, with the single nucleotide change noted by
the asterisk. The open reading frames (ORFs) or portions of open
reading frames contained within this region are delineated by the solid
boxes and labeled. The amino acid (aa) sequence of p8 immediately
surrounding the amino acid difference between strains M and B at
residue 25 is diagrammed, along with the corresponding difference in
net charge of this region.
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|
The p8 proteins of TCV-M and TCV-B bind RNA differentially.
It
has been hypothesized that the p8 protein binds the viral RNA genome
and thereby facilitates cell-to-cell movement (12). Moreover, the highly basic nature of the region surrounding amino acid
25 suggests that it might be responsible for forming nonspecific salt
bridges with the negatively charged phosphate groups on the RNA
backbone. To test this hypothesis and assess the effects of the two
different amino acids at position 25, the coding sequences of the TCV-B
and TCV-M p8 genes (BamHI-to-HindIII
fragment) were cloned into the pET15b vector (BamHI to
HindIII; Novagen) and expressed as His-tagged fusions in
Escherichia coli. After purification from the soluble
fraction according to manufacturer's specifications (Novagen pET
system manual), the His-p8 fusion proteins were tested for their
ability to bind to nucleic acid in a gel retardation assay (data not
shown). His-p8 proteins appeared to bind in a highly cooperative manner
to the 5' 229 nucleotides of the TCV genomic RNA; the probe existed in
only two detectable forms, free RNA and a completely retarded complex.
Furthermore, His-p8 also bound RNA generated from the polylinker region
of pBluescript KS+ (Stratagene), suggesting that there is no sequence
specificity to binding (data not shown). This behavior is similar to
that of many other plant virus movement proteins (see, for example, references 4, 5, 8, and 24).
While the overall binding characteristics of the His-p8B and His-p8M
fusion proteins were similar with regard to substrate
specificity, the
relative affinities of these two proteins for
RNA were different. The
ability of purified p8 proteins to bind
32P-labeled TCV RNA
under increasing NaCl concentrations was measured
by cross-linking
analysis (
4) (Fig.
3).
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FIG. 3.
Cross-linking of His-p8M and His-p8B to RNA. A uniformly
labeled 5' 229-nucleotide fragment of the TCV genome was incubated with
either His-p8B or His-p8M in the presence of the indicated salt
concentrations. The reaction mixtures were then irradiated with UV
light, treated with RNase A, and subjected to sodium dodecyl
sulfate-polyacrylamide gel electrophoresis on a 15% gel. (A)
Autoradiogram. The numbers above each lane indicate the molar NaCl
concentration in each reaction mixture. The image was obtained with a
digital camera. (B) Quantitation of cross-linking data. The data are
the averages of results of four independent experiments. Dashed line,
binding by His-p8B; solid line, binding by His-p8M. Error bars denote
standard deviations. Quantitation was done by densitometry of the X-ray
film.
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|
Both proteins exhibited remarkable salt tolerance, with 60% as much
binding at 0.4 M NaCl as was detected at 0.17 M NaCl.
The ability of
His-p8B to bind RNA, however, was more sensitive
to salt concentration,
showing an 80% reduction in binding at
0.6 M NaCl, while His-p8M
binding was reduced only 50% (Fig.
3B).
The greater salt sensitivity
exhibited by His-p8B suggests that
it binds RNA through an interaction
with lower affinity and less
stability than that observed for His-p8M.
There are several possible explanations for the differing abilities of
the p8 proteins to bind RNA. If the basic region of
p8 is indeed
important for RNA binding, changing a basic amino
acid to an acidic
amino acid may weaken the overall stability
of the interaction.
Alternatively, this amino acid change might
significantly affect
protein structure. Protein structure predictions,
however, show only
very minor differences between p8M and p8B
(
15a). Further
studies will obviously be necessary to determine
the function of this
region of the protein.
The ability of TCV-B to cause larger lesions and systemic disease
symptoms in a higher percentage of infected Di-17 plants
may be related
to the reduced affinity of p8B for RNA. Perhaps
the viral RNA genome is
translocated through the plasmodesmata
as a complex with p8. The rate
at which this complex is dissociated
might then control how rapidly new
cells are infected, since the
next step in viral proliferation is
translation of the genome,
and viral MPs can substantially block this
process in vitro (
15).
Thus, the weaker interaction of p8B
with the viral genome might
increase the rate of the uncoating process
relative to that of
the p8M-RNA complex. If all of the subsequent steps
in the infection
process occurred at the same rate, this could explain
the difference
in the sizes of the lesions caused by the two viruses.
Alternatively, the decreased RNA binding affinity of p8B may not be
responsible for the larger lesions and the greater number
of Di-17
plants developing systemic disease symptoms after inoculation
with
TCV-B. It is possible that p8 acts as an elicitor (or avirulence
factor) that induces the resistance response and that p8M is recognized
by the plant either more rapidly or more effectively than p8B.
This
might be expected to result in an earlier induction of the
plant's
defense responses, including the HR. However, there was
no detectable
difference in the time of lesion appearance on TCV-B-
or TCV-M-infected
plants. Furthermore, it was recently suggested
that the TCV coat
protein is responsible for elicitation of the
resistance response in
Di-0 plants (
17,
23).
Another possible explanation is that p8B interacts more efficiently
than p8M with the plasmodesmata or other cellular components
involved
in cell-to-cell spread. This could result in increased
numbers of cells
being infected by the time the HR is initiated,
thus leading to larger
lesions after TCV-B infection. In addition,
if more cells become
infected prior to the activation of plant
defense responses, there is a
greater probability that virions
may enter the vasculature and cause a
systemic infection.
These arguments suggest that the development of systemic symptoms is
due to the outcome of early interactions between plant
and virus. After
the initial recognition of the virus by the plant,
the plant responds
by initiating defense responses, one of which
is the HR. The
combination of these responses typically results
in the restriction of
viral pathogens to cells within or immediately
surrounding the lesion
(
7,
22). While the plant is initiating
defense responses,
the virus is replicating and spreading to the
surrounding cells. If the
virus is very efficient in this process,
a larger number of cells will
become infected by the time the
defense response is effective, thus
increasing the chances that
a viral genome or virion will escape the
defensive barrier. Conversely,
if the plant establishes the defensive
barrier rapidly enough,
viral spread will cease. Thus, the development
of systemic disease
may rest on the outcome of this initial early race
between the
plant and the virus, which in this case appears to be
influenced
by the sequence of the p8 MP.
| |
ACKNOWLEDGMENTS |
We gratefully acknowledge the assistance of Jack Morris and Anne
Simon, who provided both critical information and materials, including
TCV genomic clones and sequences.
K.K.W. also thanks Frederick M. Ausubel, who graciously allowed her to
work in his laboratory for a year and provided partial support during
this work (a grant from Hoescht AG to Massachusetts General Hospital).
This work was supported by NSF grant MCB-9723952 and USDA grant
97-35303-4520 to D.F.K. K.K.W. was supported by NSF Plant
Molecular Biology Fellowship BIR-9203814.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Waksman
Institute and Department of Molecular Biology and Biochemistry,
Rutgers, the State University of New Jersey, 190 Frelinghuysen Rd.,
Piscataway, NJ 08854-8020. Phone: (732) 445-3805. Fax: (732) 445-5735. E-mail: Klessig{at}mbcl.rutgers.edu.
| |
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J Virol, July 1998, p. 6247-6250, Vol. 72, No. 7
0022-538X/98/$04.00+0
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Vilar, M., Esteve, V., Pallas, V., Marcos, J. F., Perez-Paya, E.
(2001). Structural Properties of Carnation Mottle Virus p7 Movement Protein and Its RNA-binding Domain. J. Biol. Chem.
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