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Previous Article | Next Article 
Journal of Virology, September 2001, p. 8831-8836, Vol. 75, No. 18
0022-538X/01/$04.00+0 DOI: 10.1128/JVI.75.18.8831-8836.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Tobamovirus Replicase Coding Region Is Involved in
Cell-to-Cell Movement
Kyotaro
Hirashima and
Yuichiro
Watanabe*
Department of Life Sciences, Graduate School
of Arts and Sciences, University of Tokyo, Meguro-ku, Tokyo
153-8902, Japan
Received 29 January 2001/Accepted 29 May 2001
 |
ABSTRACT |
Tobacco mosaic virus (TMV) encodes a 30-kDa movement
protein (MP) which enables viral movement from cell to cell. It is,
however, unclear whether the 126- and 183-kDa replicase proteins are
involved in the cell-to-cell movement of TMV. In the course of our
studies into TMV-R, a strain with a host range different from that of TMV-U1, we have obtained an interesting chimeric virus, UR-hel. The
amino acid sequence differences between UR-hel and TMV-U1 are located
only in the helicase-like domain of the replicase. Interestingly,
UR-hel has a defect in its cell-to-cell movement. The replication of
UR-hel showed a level of replication of the genome, synthesis, and
accumulation of MP similar to that observed in TMV-U1-inoculated
protoplasts. Such observations support the hypothesis that the
replicase coding region may in some fashion be involved in cell-to-cell
movement of TMV.
| |
TEXT |
Tobacco mosaic
virus (TMV) has a positive-sense single-stranded RNA genome that
encodes four proteins (7). The 126- and 183-kDa replicases
are translated directly from the genomic RNA using the same first
initiation codon. The movement protein (MP) and the coat protein (CP)
are translated from their respective subgenomic mRNAs, which are
synthesized during the replication cycle. Functions have been assigned
to the genes mainly according to the phenotypic lesions of deletion or
substitution mutants of each protein. It has been shown that the 126- and 183-kDa replicases are involved in intracellular replication
(12), that the MP is involved in cell-to-cell movement
(5, 18), and that the CP is involved in long-distance
movement (9, 19). TMV requires MP but not CP for
cell-to-cell movement. It is as yet unclear whether or not replicase
directly takes part in cell-to-cell movement, since cell-to-cell
movement prior to replication has not been observed.
TMV-R, the rakkyo strain, which exhibits distinct host range
differences from the common strain of TMV-U1, was recently reported (14). TMV-R infects rakkyo (Allium chinense), a
monocot host that TMV-U1 is unable to infect. TMV-R causes only latent
infection of Nicotiana tabacum cv. Bright Yellow (BY)
in inoculated leaves, whereas TMV-U1 infects BY tobacco plants
systemically and induces mosaic virus symptoms (14). The
overall sequence homologies between TMV-U1 and TMV-R are 94% at the
nucleotide level and 96 to 98% at the amino acid sequence level of the
encoded proteins (3). Chen et al. constructed a series of
chimeric viruses between the two strains (4). When
chimeric viruses in which the replicase domain was derived from TMV-U1
were used, mosaic virus symptoms were observed on BY tobacco plants. In
contrast, infection using chimeric viruses in which the replicase
proteins had been derived from TMV-R resulted in only latent infection
in BY tobacco plants with inoculated leaves. The phenotypes of all the
chimeric viruses on BY tobacco plants were shown to be unaffected by
the mixed origins of MP or CP sequences, whether the sequence was
TMV-U1 or TMV-R derived. The difference in the pathogenicity of TMV-U1 and TMV-R for BY tobacco plants was determined by the replicase protein
(4).
The 126-kDa replicase protein contains two domains showing
similarities to the methyltransferase (1, 2) and
helicase (1, 6) domains commonly recognized in
replicases of various RNA viruses (Fig.
1). There is a relatively nonconserved
region between the two domains (Fig. 1). The 183-kDa replicase is
translated by read-through of the amber termination codon of the
126-kDa protein. The read-through region contains so-called polymerase domains (11), which can also be found in replicase
proteins of various RNA viruses (Fig. 1). To understand the involvement of each domain in host range determination, we constructed various viruses which would express chimeric replicases of TMV-U1 and TMV-R.
The chimeric viruses possess different combinations of such domains in
addition to the nonconserved regions from TMV-U1 or TMV-R.
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FIG. 1.
Schematic representation of the genomic organization of
the viruses studied. (A). TMV-U1 and TMV-R parental viruses and derived
chimeric viruses. (B) Viruses in which CPs were replaced with GFP. Gray
boxes in the chimeric viruses indicate portions of sequence derived
from the TMV-R genome. Vertical lines in the open reading frames
indicate the locations of amino acid differences between
TMV-U1 and TMV-R. Hatched boxes in panel B indicate inserted
GFP genes.
|
|
The genomic organization of the constructed chimeric viruses
(UR-met, UR-var, UR-hel, and UR-pol) is shown in Fig.
1. TMV-U1 and TMV-R were obtained from previously described sources
(3, 10). cDNA clones of chimeric viruses were constructed
by replacing the SmaI (nucleotide [nt]
258)-MluI (nt 811), MluI-NsiI (nt
2354), NsiI-BamHI (nt 3332), and
BamHI-HindIII (nt 5080) fragments of TMV-U1 with corresponding fragments from TMV-R. The sequences of the
fragments contain 5, 15, 12, and 7 amino acid differences in comparison
to those of TMV-U1, respectively. Transcription (10),
protoplast handling, and RNA inoculation into protoplasts (20,
23) or plants (12, 17) were performed essentially as described previously.
The infectivity of the four viruses was verified by sodium
dodecyl sulfate-12.5% polyacrylamide gel electrophoresis
detection of CP in inoculated BY-2 protoplasts (22) at
16 h postinoculation (hpi). Staining with Coomassie
brilliant blue revealed that these chimeric viruses accumulated CP to
levels similar to those of TMV-U1 (data not shown), demonstrating that
chimeric viruses did not lose infectivity in protoplasts.
Inability of cell-to-cell movement of UR-hel.
The infectivity
of chimeric viruses in plants was checked by noting the formation of
local lesions on N. tabacum cv. Xanthi-nc leaves. Xanthi-nc
has a dominant inherited gene, N, which confers resistance
against tobamoviruses by triggering a hypersensitive response, while
the virus retains viability. Analysis of many artificially constructed
MP mutants showed that the appearance of local lesions reflects
cell-to-cell movement of the virus (18). Contrary to
expectations, UR-hel caused no local lesions, whereas TMV-U1 did
cause local lesions (4 days postinoculation [dpi]) (Fig.
2A), as did UR-met, UR-var, and UR-pol
(data not shown). Our observations suggest that the cell-to-cell
movement of UR-hel was very low or defective.
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FIG. 2.
Assay of the ability for cell-to-cell movement of
viruses on Xanthi-nc leaves carrying the N gene (4 dpi). All
left halves of the leaves were inoculated with TMV-U1 (positive
control). (A) Right halves of each Xanthi-nc leaf were inoculated with
UR-hel or the TAD 16 mutant (13). TMV-U1 caused local
lesions on the left sides, but no local lesions appeared on the right
halves of both leaves. (B) The right half of a Xanthi-nc leaf was
inoculated with UR-lay. Local lesions appeared on both halves of the
leaf.
|
|
A detailed analysis, focusing on cell-to-cell movement, was carried out
on UR-hel. To monitor viral movement in planta, the green fluorescent
protein (GFP) gene was inserted in place of the CP gene, creating a
UR-hel
C-GFP construct (Fig. 1B). We already had a counterpart
construct, U1C-GFP (8), from the TMV-U1 genome in which
the CP gene had been replaced with the GFP gene. Tobamovirus can move
from one cell to another on inoculated leaves without CP; thus, these
viruses would express GFP and show the spread of fluorescent cells
following infection. GFP expression was observed on
U1C-GFP-inoculated Samsun-nn tobacco leaves (the systemic host) as
circles with diameters of approximately 1 mm (Fig. 3A and
B). Fluorescent areas
were seen to expand thereafter. In contrast, UR-helC-GFP did not
show any visible fluorescent circles or spots (4 and 7 dpi) (Fig. 3A
and B). Subsequently, we observed UR-hel-inoculated leaves using
fluorescence microscopy. Wright et al. reported that a mutant deficient
in cell-to-cell movement, TMV-GFPMP, in which the CP gene had been
replaced with a GFP gene, showed GFP expression only in initially
infected cells on inoculated leaves (23). GFP expression
of UR-helC-GFP was barely detected in a single cell (or in a couple
of cells at most) (Fig. 3C). The shapes and the areas of
fluorescence-positive parts were almost the same as those reported by
Wright et al. (23). Taken together with the available
experimental data (Fig. 2A), these results showed that UR-helC-GFP
can replicate in initially infected cells but cannot move out of the
cells. It is likely that UR-helC-GFP (and UR-hel) has little, if
any, cell-to-cell movement ability.
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FIG. 3.
Viral movement demonstrated by GFP expression on
systemic hosts. (A) Photos of the same inoculated leaf were taken at 4 and at 7 dpi. The left half of the Samsun-nn leaf was inoculated
with U1C-GFP, and the right half was inoculated with UR-helC-GFP.
(B) Detached leaf (treated as described for panel A) was observed at 4 dpi at a higher magnification. The left half of the Samsun-nn leaf was
inoculated with U1C-GFP, and the right half was inoculated with
UR-helC-GFP. Bar, 10 mm. (C) Visualization of each leaf half by
fluorescence microscopy at 4 dpi. GFP induced by UR-helC-GFP
challenge was observed only in a single cell (or in a couple of cells
at most). Bars, 200 µm.
|
|
We made as many as eight independent clones of UR-hel, none of which
caused any local lesions on Xanthi-nc tobacco leaves (data not shown).
In addition, we constructed UR-lay, the "true revertant" clone, by
replacing the NsiI-BamHI restriction fragment of
UR-hel with that of the corresponding fragment of TMV-U1. UR-lay caused
local lesions, as did TMV-U1, on Xanthi-nc tobacco leaves (Fig. 2B).
This result confirmed that UR-hel possessed no other substitutions
outside the NsiI-BamHI fragment. The novel
phenotype of UR-hel is not caused by a change in the MP sequence.
UR-hel and TMV-U1 have similar protoplast replication levels.
It is conceivable that UR-hel contains amino acid sequence changes in
the replicase that may cause low levels of replication and
inefficient cell-to-cell movement. We thus checked the replication level of UR-hel in protoplasts and compared it to that of TMV-U1 by
employing Northern analysis. Total RNA was extracted from protoplasts with the RNeasy plant minikit (Qiagen) at 0, 3, 6, 9, 12, 18, and 24 hpi. RNA blotting was performed with formaldehyde-agarose gels and
Hybond N+ (Amersham). For RNA detection, digoxigenin-labeled hybridization probes were employed for positive- and negative-strand RNA (nt 5713 to 6191), generated using the DIG-RNA labeling kit (Roche). Bands were detected by anti-digoxigenin-alkaline
phosphatase Fab fragments (Roche) and a BCIP-NBT
(5-bromo-4-chloro-3-indolyl-phosphate-nitroblue tetrazolium)
phosphatase substrate system (Kirkegaard & Perry Laboratories).
Northern analysis showed that UR-hel replicated to levels similar to
those of TMV-U1 during the time period studied (Fig.
4). We infer that the defect in
cell-to-cell movement of UR-hel was not caused by a low level of
replication.
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FIG. 4.
Comparison of replication efficiencies of TMV-U1 and
UR-hel. The total RNA (0.2 µg/lane) extracted from protoplasts was
separated, blotted, and analyzed. (A) Northern analysis of replication
of TMV-U1 and UR-hel in inoculated protoplasts using RNA probes for
positive- and negative-strand TMV RNA (nt 5713 to 6191). The
replication level of UR-hel was similar to that of TMV-U1. (B) rRNA
detected by ethidium bromide staining.
|
|
There are several reports which have shown that a low level of MP
synthesis reduces the cell-to-cell movement ability of TMV (15,
16, 21). Due to the low level of synthesis and accumulation, MP
mRNA of TMV-U1 and UR-hel was not detected by Northern analysis. Whether the synthesis of UR-hel MP differs from that of TMV-U1 needed
to be determined. Therefore, we analyzed the synthesis of MP and
CP in protoplasts and focused on the level of MP production. Protoplasts inoculated with TMV-U1 or UR-hel were pulse-labeled with a
[35S]methionine-[35S]cysteine
protein-labeling mixture (NEN) at 0.1 MBq/ml for 30 min at 3, 6, 9, 12, 18, and 24 hpi. Proteins were extracted from protoplasts and subjected
to sodium dodecyl sulfate-12.5% polyacrylamide gel electrophoresis.
35S-labeled MP and CP bands were detected and traced
quantitatively using a Fuji Image Analyzer. UR-hel synthesized both MP
and CP to levels similar to those of TMV-U1 at each of the times
investigated (Fig. 5). If the CP of each
virus accumulated to similar levels at the same times postinoculation,
then the data would further support the MP data suggesting that the
subgenomic RNAs were likely synthesized to similar levels by both
viruses during replication. We can exclude the possibility that defects
in the cell-to-cell movement of UR-hel were caused by the low
production of MP.
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FIG. 5.
Pulse-labeling analysis of the synthesis of MP and CP in
TMV-U1- and UR-hel-inoculated protoplasts over time. Inoculated
protoplasts were metabolically labeled with a
[35S]methionine-[35S]cysteine
protein-labeling mixture (NEN) at 0.1 MBq/ml for 30 min, starting from
the time indicated at the top of each lane. UR-hel synthesized MP and
CP at levels similar to those of TMV-U1.
|
|
UR-hel could not be rescued by MP supply in trans
We have investigated whether defects in cell-to-cell movement of UR-hel
can be complemented by MP supplied in trans. Since the
transgenic tobacco line 2005 expresses TMV-U1 MP from the transgene, we
attempted to complement in trans the defect in the cell-to-cell movement of mutants. For example, the TAD 16 mutant (13), a virus that has a three-amino-acid deletion in the
MP coding region, caused local lesions on tobacco line 2005 leaves but not on Xanthi-nc leaves (Fig. 2A and
6). On the other hand, UR-hel
caused local lesions neither on Xanthi-nc nor on tobacco line 2005 plants (Fig. 2A and 6). This result indicates that the defect of
cell-to-cell movement in UR-hel cannot be rescued by MP supplied in
trans.
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FIG. 6.
In trans supply of MP from tobacco line 2005 plant carrying the N gene cannot complement the UR-hel
defect in cell-to-cell movement (4 dpi). The left half of each leaf was
inoculated with TMV-U1. The right half of each leaf was inoculated with
UR-hel or the TAD 16 mutant (13). The transgenic line 2005 expresses TMV-U1 MP constitutively. Leaves inoculated with the TAD 16 mutant showed local lesions, but leaves inoculated with UR-hel showed
no local lesions.
|
|
Additionally, we found a unique virus, designated UR-hel, among these
chimeric viruses. We have confirmed that the MP sequence or production
of UR-hel is identical to that of TMV-U1. Also, UR-hel could replicate
to levels similar to those of U1 in protoplasts. Moreover, UR-hel did
not cause local lesions even on tobacco line 2005 leaves, which
constitutively expressed MP. The defect in cell-to-cell movement was
not caused by MP, but it is reasonable to suspect that TMV replicase is
involved in cell-to-cell movement. We plan to investigate how the
replicase acts in cell-to-cell movement.
| |
ACKNOWLEDGMENTS |
We thank S. Kawakami for critically reviewing and L. Knight for
reading the manuscript. We also thank R. N. Beachy for providing pU3/12-4, pU1C-GFP, the TAD mutant, and the tobacco line 2005 expressing a TMV MP.
This work was supported in part by "Molecular Mechanisms of
Plant-Pathogenic Microbe Interaction," a grant-in-aid for scientific research on priority area (A) from the Ministry of Education, Culture,
Sports, Science, and Technology of Japan (no. 08680733) to Y.W., and by
a grant from the Japan Society for the Promotion of Science
(RFTF96L00603) to Y.W.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Department of
Life Sciences, Graduate School of Arts and Sciences, University of
Tokyo, Komaba 3-8-1, Meguro-ku, Tokyo 153-8902, Japan. Phone:
81-3-5454-6776. Fax: 81-3-5454-6776. E-mail:
solan{at}bio.c.u-tokyo.ac.jp.
| |
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Journal of Virology, September 2001, p. 8831-8836, Vol. 75, No. 18
0022-538X/01/$04.00+0 DOI: 10.1128/JVI.75.18.8831-8836.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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