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Journal of Virology, March 1999, p. 2288-2297, Vol. 73, No. 3
0022-538X/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
Tomato Spotted Wilt Virus Particle Morphogenesis in
Plant Cells
Marjolein
Kikkert,
Jan
Van Lent,
Marc
Storms,
Pentcho
Bodegom,
Richard
Kormelink, and
Rob
Goldbach*
Laboratory of Virology, Wageningen
Agricultural University, Wageningen, The Netherlands
Received 11 May 1998/Accepted 30 November 1998
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ABSTRACT |
A model for the maturation of tomato spotted wilt virus (TSWV)
particles is proposed, mainly based on results with a protoplast infection system, in which the chronology of different maturation events could be determined. By using specific monoclonal and polyclonal antisera in immunofluorescence and electron microscopy, the site of
TSWV particle morphogenesis was determined to be the Golgi system. The
viral glycoproteins G1 and G2 accumulate in the Golgi prior to a
process of wrapping, by which the viral nucleocapsids obtain a double
membrane. In a later stage of the maturation, these doubly enveloped
particles fuse to each other and to the endoplasmic reticulum to form
singly enveloped particles clustered in membranes. Similarities and
differences between the maturation of animal-infecting (bunya)viruses
and plant-infecting tospoviruses are discussed.
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INTRODUCTION |
Increased knowledge about the
molecular biology of tomato spotted wilt virus (TSWV), type species of
the genus Tospovirus, has shed light on the replication and
gene-coding strategy of this plant-infecting bunyavirus (for reviews,
see references 6, 8, 9, 23, and
34). In contrast, a clear view of the TSWV particle
maturation pathway in plant cells has not yet been reported, mainly
because useful single-cell systems to study this process have been
lacking. Early electron microscopic studies by Milne (22)
and Ie (12) of infected leaf tissues summarized typical
structures associated with tospovirus infections that were observed,
such as the viroplasm (VP), nucleocapsid aggregates (NCA), paired
parallel membranes (PPM) thought to be involved in budding events,
doubly enveloped particles (DEV), and singly enveloped particles (SEV)
clustered within endoplasmic reticulum (ER) membranes. It was observed
that VP, NCA, PPM, and DEV were present mostly in early stages of
infection whereas clustered SEV seemed to be a late or even final state
in the maturation. Since TSWV is an enveloped bunyavirus, it is
anticipated that preexisting intracellular membranes are used for
enveloping, although it has been reported (22) that the PPM
may be produced de novo since they did not seem to resemble any of the
cellular membrane structures. More recently however, Kitajima et al.
(14) presented three possible models for the morphogenesis
of tospovirus particles, which included morphogenesis at the
intracellular membranes of the ER or the Golgi system, although no
conclusive choice could be made between the models proposed. While
studying defective and nondefective isolates of impatiens necrotic spot
virus, Lawson et al. (20) suggested that PPM, showing
budding structures, could be Golgi derived based on their morphology.
None of the above studies, however, presented extensive labeling data
that supported either of the different models of the maturation pathway of tospoviruses in plants.
Structures possibly associated with morphogenesis of TSWV have also
been observed in cells of the thrips vector Frankliniella occidentalis (32). Both N and G1/G2 proteins were
immunolocalized to intracellular membranes, which were suggested to be
Golgi derived (again based on their morphology), in cells of the midgut
epithelium. However, no intermediate structures associated with budding
virus were observed in these membranes, and no mature particles were observed in the midgut.
Since previous studies of nonsynchronous infections have hampered our
understanding of the morphogenesis process of TSWV and other
tospoviruses in plants, we now apply the recently developed protoplast
infection system (13) to study this topic. Both cowpea (Vigna unguiculata) and Nicotiana rustica
protoplast suspensions support TSWV multiplication, reaching at least
50% infection, provided that freshly prepared, highly infectious virus
preparations are used as the inoculum (13). The application
of a protoplast system not only has the advantage of a high level of
infected cells but also allows a temporal analysis of the maturation
pathway, since a high synchrony of infection is obtained. It has been
shown that in cowpea protoplasts the infection cycle leads to only
small numbers of enveloped particles whereas in N. rustica
protoplasts large numbers of mature particles accumulate and a complete
infection is produced (13). Therefore the system based on
N. rustica protoplasts was used in the present studies to
investigate the chronology of the TSWV maturation.
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MATERIALS AND METHODS |
Virus, plants, and protoplasts.
Throughout this study, a
Brazilian isolate of TSWV, BR01 (2), was used, and
maintained in N. rustica plants by mechanical inoculation
and transmission by thrips. For (cryo)electron microscopic analysis,
N. rustica plants were harvested 5 to 10 days after inoculation with TSWV and local lesions were isolated from petunia (cv.
Polo Blauw) 3 to 5 days after inoculation with TSWV. N. rustica protoplasts were inoculated with freshly isolated TSWV
particles as described previously (13) and harvested for
immunofluorescence microscopy, (immuno)electron microscopy, or Western
blotting between 0 and 40 h postinoculation (p.i.).
Antisera.
Polyclonal antisera against TSWV N protein and the
hydrophilic ectodomains of G1 and G2 were raised as described
previously (13). The rat monoclonal immunoglobulin M serum
against the plant Golgi system (JIM84) was described previously
(11), as were anti-
F1 (19) and
anti-RGP1 (3) sera against the plant Golgi system.
Immunofluorescence light microscopy.
Immunofluorescence of
protoplasts was performed as described previously (13).
Double-labeling experiments were performed with a combination of rabbit
polyclonal antiserum and rat monoclonal antiserum, with swine
anti-rabbit serum conjugated to tetramethylrhodamine isothiocyanate and
goat anti-rat serum conjugated to fluorescein isothiocyanate as the
respective second antibodies.
(Immuno)electron microscopy.
Immunoelectron microscopy of
protoplasts fixed with 3% glutaraldehyde-2% paraformaldehyde, as
well as ultrastructural analysis with osmium tetroxide fixation, was
performed as described previously (13).
Cryoelectron microscopy.
Aldehyde fixation, infiltration
with sucrose, cryosectioning, and negative staining of infected leaf
material were carried out as described by Van der Wel et al.
(33).
Western blotting.
Sodium dodecyl sulfate-polyacrylamide gel
electrophoresis and Western immunoblot analysis with alkaline
phosphatase detection were carried out as described by Kikkert et al.
(13).
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RESULTS |
Chronology of appearance, and labeling of structures associated
with maturation.
N. rustica protoplasts were inoculated with
TSWV particles by using polyethylene glycol, and samples were taken
between 0 and 40 h p.i. for immunofluorescence and electron
microscopy analyses. Table 1 shows the
times of appearance of different structures, which have previously been
reported to be associated with TSWV maturation (12, 14, 22),
during the infection in protoplasts. Table
2 summarizes the reactivity of these
maturation-associated structures with antisera used in electron
microscopy, as discussed further throughout Results and Discussion.
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TABLE 1.
Relative appearance of TSWV maturation-associated
structures and intracellular membranes during TSWV infection
in protoplastsa
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TABLE 2.
Reactivity of TSWV maturation-associated structures and
intracellular membranes with different antisera in immunogold electron
microscopy, in TSWV-infected protoplastsa
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Examples of the different structures are depicted in Fig.
1. VP (Fig.
1A), characterized as amorphous
medium-density material,
was seen throughout the infection, very often
in association with
NCA, which is much more dense (Fig.
1A) and which
often appears
as aggregated nodules of around 60 to 80 nm in diameter
embedded
in the VP (Fig.
1). Both structures are strongly labeled with
antiserum against the nucleocapsid protein, N (Fig.
1A and C and
Table
2), suggesting that both contain viral nucleocapsid protein.
They are
only weakly labeled with serum against the viral glycoproteins
G1 and
G2 (Table
2 and data not shown). In the early stages of
infection,
mostly small patches of VP and NCA dispersed throughout
the cytoplasm
were observed (Fig.
1A), whereas in later stages,
often only one or two
very large areas of NCA and VP were found
(Fig.
1B).
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FIG. 1.
Overview of TSWV maturation-associated structures found
in infected N. rustica protoplasts. (A) NCA embedded in VP,
immunogold labeled with antiserum against N at 26 h p.i. (B) Large
cluster of VP-NCA, as found in late stages of infection at 40 h
p.i. (C) Detail of panel B (the boxed area) showing DEV and ER on the
edge of the VP-NCA cluster labeled with antiserum against N. (D) SEV
clusters surrounded by membrane envelopes (membranes are indicated by
arrowheads) and NCA close to PPM structures at 30 h p.i. Bars, 200 nm.
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PPM are characterized as membrane cisternae that are often strongly
curved, and dense material is tightly associated with
them (Fig.
1D).
PPM were previously suggested to be derived from
Golgi stacks
(
20), and the modification of Golgi stacks that
was observed
in protoplast infections can indeed be interpreted
as the formation of
PPM (Fig.
2). In infected cells, the
cisternae
of a Golgi stack seem to drift apart and dense material
accumulates
between them (Fig.
2B). The cisternae become curved and
often
seem extended (Fig.
2C). The formation of PPM was quite obvious
in protoplast infections at several time points, but a clear peak
was
found in the early stages of infection around 18 to 22 h p.i.
(Table
1). PPM and their surroundings were labeled with antiserum
against G1 (Fig.
3A), G2 (Fig.
3B), and N (Fig.
3C) proteins (Table
2)
in infected protoplasts, while these antisera gave no background
on
healthy plant cells (data not shown). Often DEV were found
in the
vicinity, which appear to form at the PPM (Fig.
3C). To
confirm that these structures
found in protoplast infections were
not artifacts of the system, early
stages of systemic infections
in
N. rustica plants as well
as TSWV local lesions in petunia
were investigated. Particularly clear
examples of curving and
wrapping PPM were found in these plants as well
(Fig.
4). The
data suggest that DEV are
formed by curving and wrapping of modified
Golgi cisternae around dense
nucleocapsid material in the cytoplasm.
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FIG. 2.
Formation of PPM structures by modification of Golgi
stacks. (A) Apparently unmodified Golgi stack at 18 h p.i. (B)
Putative, modified Golgi stack with cisternae moving away from each
other and dense material, presumably nucleocapsids, accumulating
between them at 18 h p.i. (C) PPM structure showing extended and
curved Golgi cisternae presumably surrounded by nucleocapsid material
at 18 h p.i. Bars, 200 nm.
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FIG. 3.
Immunogold labeling of PPM structures with antiserum
against G1 (A), G2 (B), and N (C), all at 22 h p.i. Arrowheads
indicate DEV being formed. Bars, 200 nm.
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FIG. 4.
(A) PPM structures in local lesions in petunia at 4 days
p.i. (B to D) PPM structures in systemically infected N. rustica plants at 5 days p.i. Formation of DEV is shown clearly.
Bars, 200 nm.
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From Table
1 it becomes clear that PPM largely precedes the formation
of DEV and that SEV seem to represent a final stage
in the infection.
At late stages of infection (30 to 40 h p.i.),
PPM as well as DEV
were rarely found whereas SEV surrounded by
membranes were abundant and
were often found near the large NCA
clusters (Table
1 and Fig.
1D). ER
membranes were found throughout
the infection, often in the vicinity of
maturation-associated
structures (Fig.
1A to C). Apparently unmodified
Golgi stacks,
however, became more scarce during the infection process
and were
virtually absent at late
stages.
The Golgi system is the site of TSWV enveloped-particle
morphogenesis.
Since the morphology of PPM structures strongly
suggests that they are derived from Golgi stacks, three independent
plant Golgi markers were used to confirm this. JIM84, a rat monoclonal antiserum raised against carrot Golgi protein epitopes (11), anti-F1, a polyclonal antiserum raised in carrot against
complex glycans common to plant Golgi glycoproteins (19),
and anti-RGP1, a polyclonal antiserum against the peptide fraction of a
reversibly glycosylated trans-Golgi protein from pea
(3) were used. Since JIM84 is a monoclonal antiserum, it
could be used in double-label experiments together with polyclonal sera
against viral proteins in immunofluorescence microscopy. JIM84 was
raised against carrot Golgi epitopes, and so we verified whether it can
also recognize the Golgi system of N. rustica. Indeed, in
healthy N. rustica protoplasts or at 0 h p.i., JIM84
produced a typical pattern of small spots scattered throughout the
cytoplasm, representing individual Golgi stacks (Fig.
5A), as was also observed in carrot,
onion, and maize cells with JIM84 (11). As a result of
transport of the epitope-containing protein, parts of the plasma
membrane were usually labeled by JIM84 as well (Fig. 5A) (11,
27). During TSWV infection, the Golgi system did not appear
dramatically different, although larger clusters were increasingly
observed with JIM84, as well as the smaller ones (Fig. 5B and D). The
viral glycoproteins colocalized at least partly with these Golgi
structures at different time points during the protoplast infection
(Fig. 5B to E). Viral N protein also colocalized with the Golgi during
protoplast infections (data not shown).
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FIG. 5.
Immunofluorescence images of N. rustica
protoplasts. (A) Healthy protoplast labeled with JIM84 antiserum
against the plant Golgi system, showing individual Golgi stacks as
small clusters throughout the cytoplasm. The plasma membrane is also
labeled with JIM84 due to transport of the epitope-containing Golgi
proteins. (B and D) TSWV-infected protoplasts at 30 h p.i.,
labeled with JIM84 antiserum. (C and E) The same infected protoplasts
labeled with mixed antisera against G1 and G2. Areas of clear
colocalization of the viral glycoproteins with the Golgi system are
indicated with arrows. Cloudy areas within cells represent the
autofluorescence background. Bars, 5 µm.
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Both polyclonal anti-
F
1 and anti-RGP1 sera labeled Golgi
stacks in healthy
N. rustica protoplasts or in protoplasts
at 0
h p.i., as shown by immunogold electron microscopy (Fig.
6A and
D). In infected protoplasts,
anti-
F
1 labeled PPM structures (Fig.
6B) as well as
virus particles (Fig.
6C). Anti-RGP1 labeled PPM
very specifically
although not heavily (Fig.
6E and F), but it
did not tag virus
particles (Table
2). Figure
7 shows that
in
Western blots anti-
F
1 cross-reacts with G1 from virus
particles,
which most probably explains the labeling of virus
particles.
The serum, however, did not react with unglycosylated G1
expressed
in
Escherichia coli (data not shown), indicating
that the cross-reaction
is an interaction with the glycans of G1. Since
the anti-
F
1 serum
was raised against Golgi-specific
glycans (
19), the cross-reaction
may indicate that G1
contains epitopes for anti-
F
1, confirming
the Golgi
targeting of TSWV glycoproteins.
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FIG. 6.
Immunogold labeling of maturation-associated structures
with antisera against the plant Golgi system. (A) Unmodified Golgi
stack in a healthy cell, labeled with anti-F1 antiserum.
(B) PPM structure labeled with anti-F1 antiserum at
22 h p.i. (C) Virus particles labeled with anti-F1
antiserum at 40 h p.i. (D) Unmodified Golgi stack at 0 h
p.i., labeled with anti-RGP1 antiserum. (E and F) PPM structures
labeled with anti-RGP1 antiserum at 26 h p.i. White arrows
indicate gold particles; black arrowheads indicate PPM membranes. Bars,
200 nm.
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FIG. 7.
Western blot analysis with anti-F1
antiserum, showing cross-reaction of this serum with G1 protein from
purified TSWV particles. Lanes: TSWV, purified TSWV particles; MARKER,
low-molecular-mass marker proteins.
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These data together indicate that PPM are in fact derived from the
Golgi and form the site of particle
morphogenesis.
SEV are produced by fusion of DEV.
From osmium tetroxide-fixed
specimens of infected protoplasts, in which DEV and SEV can be clearly
distinguished, it was observed that at around 26 h p.i. SEV
started to accumulate in clusters surrounded by membranes (Table 1)
while DEV particles could also be observed in these areas (Fig.
8A). These kinds of structures were also
found in local lesions in petunia (results not shown), along with
structures suggesting the formation of these SEV accumulations in
membranes (Fig. 8B). Considering the chronology of the appearance of
DEV and SEV (Table 1), these images suggest that SEV is formed by
fusion of DEV. In this process, the outer membranes of DEV form a tight
collective smooth envelope around singly enveloped particles (Fig. 8B).
DEV seem also able, either individually or fused, to fuse to (rough) ER
membranes (Fig. 8B).
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FIG. 8.
Formation of SEV by fusion of DEV. (A) Clustered SEV
inside smooth and rough membranes, as found in late stages of TSWV
infections of N. rustica protoplasts at 40 h p.i. Note
the DEV at the bottom of the image (arrowhead). (B) Image from a TSWV
local lesion in petunia showing DEV particles fusing with each other
(triangles) and with ER membranes identified by ribosomes on the
surface (arrowheads). Bars, 200 nm.
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DISCUSSION |
By using the recently developed N. rustica protoplast
infection system, a time course of TSWV particle maturation could be produced. Analysis of the maturation intermediates in these protoplasts as well as in local lesions in petunia and systemically infected N. rustica plants leads to a TSWV particle maturation model
(Fig. 9).
The use of three independent plant-Golgi markers confirmed the
suggestion that PPM are derived from Golgi stacks and form the site of
doubly enveloped particle morphogenesis. The apparent retention of the
viral glycoproteins G1 and G2 in the Golgi system is in agreement with
the observations by immunofluorescence microscopy, which indicated that
these proteins are not found on the surface of the plasma membrane
(13) (Fig. 5) whereas they are assumed to enter the
secretory pathway due to their N-terminal signal peptide
(15). It is therefore likely that either one or both of the
TSWV glycoproteins contain a Golgi retention signal, as recently
documented for Uukuniemi virus (1).
In the proposed maturation model (Fig. 9), DEV is formed by wrapping of
modified Golgi membranes (PPM) around nucleocapsids in the cytoplasm,
and subsequently SEV is formed by fusion of DEV with each other or with
ER membranes. Whether this latter process is based on an existing
targeted membrane fusion mechanism in the cell or whether it is a
virally induced phenomenon remains to be investigated.
Apart from the structures that now have been identified as being
involved in particle morphogenesis, other virus-associated structures
were also observed but not clarified. VP in association with NCA,
consisting of nucleocapsid protein, does not seem to be directly
involved in particle morphogenesis. However, PPM and DEV are often
found in the vicinity of VP and NCA (Fig. 1B and C) or are even
embedded in them, as suggested by the labeling of NCA and VP with
anti-G1-G2 sera (Table 2). NCA and VP thus could be a source of
nucleocapsids meant to be wrapped with Golgi membranes containing viral glycoproteins.
Still, a large part of the nucleocapsid protein that is produced during
an infection is not used for producing particles but seems to be stored
in large NCA clusters (Fig. 1B and C). This is also evident from
Western blots of crude extracts of infected plants and purified TSWV
particles, where the ratio of nucleocapsid protein to glycoproteins is
much greater in crude extracts than in purified particles (data not
shown). It is thought that TSWV moves from cell to cell by the action
of NSm (nonstructural protein encoded by the M segment) which modifies
the plasmodesmata so that infectious nucleocapsid units can pass the
cell barrier (17, 31). This accounts for a part of the
overproduction of nucleocapsids but most probably not for all.
The production of TSWV-encoded nonstructural (NSs) protein has not been
investigated here but was observed in earlier studies (12, 14, 16,
22). So far, there is no evidence that this protein plays a role
in particle morphogenesis.
Although the TSWV maturation pathway as proposed here is very different
from that of the animal-infecting bunyaviruses (reviewed in 4,
10, 21, 24, 30), the assembly of particles in the Golgi
system appears to be a feature of both plant- and animal-infecting bunyaviruses. Modification of the Golgi system, as observed in TSWV
infections, has also been reported for Uukuniemi virus and Nairobi
sheep virus (5, 18, 26); however, instead of curling and
wrapping, the Golgi cisternae vacuolize extensively during these animal
bunyavirus infections, thus increasing the volume of the cisternae and
allowing the budding of singly enveloped particles into the lumen. The
formation of doubly enveloped particles by wrapping of cisternae has
never been reported for animal infecting bunyaviruses; however, it is
not unknown in enveloped animal-infecting double-stranded DNA viruses.
Vaccinia poxvirus is wrapped by membranes of the intermediate
compartment between the ER and the Golgi and in a later stage of the
maturation it is wrapped by trans-Golgi network membranes
(28, 29). Varicella-zoster herpesvirus makes use of the
trans-Golgi network membranes for wrapping its particles as
well (7, 35), and African swine fever virus is wrapped by ER
membranes (25). The wrapping phenomenon has not been
reported for any other plant-infecting virus, and it is not yet
precisely clear which part of the Golgi is involved in TSWV morphogenesis.
The final stages of the particle maturation also seem to be different.
Animal-infecting bunyaviruses produce groups of particles inside
vesicles pinched off from the Golgi (21), and the ER plays
no role in particle morphogenesis. TSWV singly enveloped particles end
up in large membrane envelopes as a result of self-fusion of DEV (which
have two Golgi-derived membranes), or fusion with ER membranes. These
envelopes surrounding SEV clusters must consequently consist of both
Golgi- and ER-derived membranes.
To infect new cells, animal-infecting bunyaviruses are transported to
the plasma membrane and released outside the cell via the vesicular
transport pathway of the cell, whereas TSWV particles retain and
accumulate in the plant cell until feeding thrips vectors ingest them
for transport to other host plants.
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ACKNOWLEDGMENTS |
We thank Chris Hawes, Oxford School of Biological and Molecular
Sciences, for kindly providing the rat monoclonal JIM84 antiserum and
Maarten Chrispeels, University of California, La Jolla, for kindly
providing polyclonal anti-F1 antiserum. We also thank Kanwarpal Dhugga, Stanford University, Stanford, Calif., for sending us
the anti-RGP1 antiserum. We are grateful to Wiesje Kassies for
excellent technical assistance and to Beatrice Satiat-Jeunemaitre and
Dick Peters for helpful discussions.
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FOOTNOTES |
*
Corresponding author. Mailing address: Laboratory of
Virology, WAU, Binnenhaven 11, 6709 PD Wageningen, The Netherlands.
Phone: 31-317-483090. Fax: 31-317-484820. E-mail:
Rob.Goldbach{at}medew.viro.wau.nl.
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REFERENCES |
| 1.
|
Andersson, A. M.,
L. Melin,
A. Bean, and R. F. Pettersson.
1997.
A retention signal necessary and sufficient for Golgi localization maps to the cytoplasmic tail of a Bunyaviridae (Uukuniemi virus) membrane glycoprotein.
J. Virol.
71:4717-4727[Abstract].
|
| 2.
|
De Ávila, A. C.,
P. de Haan,
M. L. L. Smeets,
R. de O. Resende,
R. Kormelink,
E. W. Kitajima,
R. W. Goldbach, and D. Peters.
1993.
Distinct levels of relationships between tospovirus isolates.
Arch. Virol.
128:211-227[Medline].
|
| 3.
|
Dhugga, K. S.,
S. C. Tiwari, and P. M. Ray.
1997.
A reversibly glycosylated polypeptide (RGP1) possibly involved in plant cell wall synthesis: purification, gene cloning, and trans-Golgi localization.
Proc. Natl. Acad. Sci. USA
94:7679-7684[Abstract/Free Full Text].
|
| 4.
|
Elliott, R. M.
1990.
Molecular biology of the Bunyaviridae.
J. Gen. Virol.
71:501-522[Abstract/Free Full Text].
|
| 5.
|
Gahmberg, N.,
E. Kuismanen,
S. Keränen, and R. F. Pettersson.
1986.
Uukuniemi virus glycoproteins accumulate in and cause morphological changes of the Golgi complex in the absence of virus maturation.
J. Virol.
57:899-906[Abstract/Free Full Text].
|
| 6.
|
German, T. L.,
D. E. Ullman, and J. W. Moyer.
1992.
Tospoviruses: diagnosis, molecular biology, phylogeny and vector relationships.
Annu. Rev. Phytopathol.
30:315-348.
|
| 7.
|
Gershon, A. A.,
D. L. Sherman,
Z. Zhu,
G. A. Gabel,
R. T. Ambron, and M. D. Gershon.
1994.
Intracellular transport of newly synthesized varicella-zoster virus: final envelopment in the trans-Golgi network.
J. Virol.
68:6372-6390[Abstract/Free Full Text].
|
| 8.
|
Goldbach, R., and D. Peters.
1996.
Molecular and biological aspects of tospoviruses, p. 129-157.
In
R. M. Elliott (ed.), The Bunyaviridae. Plenum Press, New York, N.Y.
|
| 9.
|
Goldbach, R.,
R. Kormelink,
P. de Haan,
R. de O. Resende,
A. de Ávila,
F. van Poelwijk,
J. van Lent,
I. Wijkamp,
M. Prins, and D. Peters.
1992.
Tomato spotted wilt virus: genome organization, transmission and symptom induction, p. 257-311.
In
D. Bills, and S.-D. Kung (ed.), Biotechnology and plant protection. World Scientific, Singapore.
|
| 10.
|
Griffiths, G., and P. Rottier.
1992.
Cell biology of viruses that assemble along the biosynthetic pathway.
Semin. Cell Biol.
3:367-381[Medline].
|
| 11.
| Horsley, D., J. Coleman, D. Evans, K. Crooks, J. Peart,
B. Satiat-Jeunemaitre, and C. Hawes. 1993. A monoclonal antibody,
JIM84, recognizes the Golgi apparatus and plasma membrane in plant
cells. J. Exp. Bot. 44(Suppl.):223-229.
|
| 12.
|
Ie, T. S.
1971.
Electron microscopy of developmental stages of tomato spotted wilt virus in plant cells.
Virology
2:468-479.
|
| 13.
|
Kikkert, M.,
F. Van Poelwijk,
M. Storms,
W. Kassies,
H. Bloksma,
J. van Lent,
R. Kormelink, and R. Goldbach.
1997.
A protoplast system for studying tomato spotted wilt virus infection.
J. Gen. Virol.
78:755-1763.
|
| 14.
|
Kitajima, E. W.,
A. C. de Ávila,
R. O. Resende,
R. W. Goldbach, and D. Peters.
1992.
Comparative cytological and immunological labeling studies on different isolates of tomato spotted wilt virus.
J. Submicrosc. Cytol. Pathol.
24:1-14.
|
| 15.
|
Kormelink, R.,
P. de Haan,
C. Meurs,
D. Peters, and R. Goldbach.
1992.
The nucleotide sequence of the M RNA segment of tomato spotted wilt virus, a bunyavirus with two ambisense RNA segments.
J. Gen. Virol.
73:2795-2804[Abstract/Free Full Text].
|
| 16.
|
Kormelink, R.,
E. W. Kitajima,
P. de Haan,
D. Zuidema,
D. Peters, and R. Goldbach.
1991.
The nonstructural protein (NSs) encoded by the ambisense S RNA segment of tomato spotted wilt virus is associated with fibrous structures in infected plants.
Virology
181:459-468[Medline].
|
| 17.
|
Kormelink, R.,
M. Storms,
J. van Lent,
D. Peters, and R. Goldbach.
1994.
Expression and subcellular location of the NSm protein of tomato spotted wilt virus (TSWV), a putative movement protein.
Virology
200:56-65[Medline].
|
| 18.
|
Kuismanen, E.,
K. Hedman,
J. Saraste, and R. F. Pettersson.
1982.
Uukuniemi virus maturation: accumulation of virus particles and viral antigens in the Golgi complex.
Mol. Cell. Biol.
2:1444-1458[Abstract/Free Full Text].
|
| 19.
|
Laurière, M.,
C. Laurière,
M. J. Chrispeels,
K. D. Johnson, and A. Sturm.
1989.
Characterization of a xylose-specific antiserum that reacts with the complex asparagine-linked glycans of extracellular and vacuolar glycoproteins.
Plant Physiol.
90:1182-1188[Abstract/Free Full Text].
|
| 20.
|
Lawson, R. H.,
M. M. Dienelt, and H. T. Hsu.
1996.
Ultrastructural comparisons of defective, partially defective, and non-defective isolates of impatiens necrotic spot virus.
Phytopathology
86:650-661.
|
| 21.
|
Matsouka, Y.,
S. Y. Chen, and R. W. Compans.
1991.
Bunyavirus protein transport and assembly.
Curr. Top. Microbiol. Immunol.
169:161-180[Medline].
|
| 22.
|
Milne, R. G.
1970.
An electron microscope study of tomato spotted wilt virus in sections of infected cells and in negative stain preparations.
J. Gen. Virol.
6:267-276.
|
| 23.
|
Mumford, R. A.,
I. Barker, and K. R. Wood.
1996.
The biology of the tospoviruses.
Ann. Appl. Biol.
128:159-183.
|
| 24.
|
Pettersson, R. F.
1991.
Protein localization and virus assembly at intracellular membranes.
Curr. Top. Microbiol. Immunol.
170:67-104[Medline].
|
| 25.
|
Rouiller, I.,
S. M. Brookes,
A. D. Hyatt,
M. Windsor, and T. Wileman.
1998.
African swine fever virus is wrapped by the endoplasmic reticulum.
J. Virol.
72:2373-2387[Abstract/Free Full Text].
|
| 26.
|
Rwambo, P. M.,
M. K. Shaw,
F. R. Rurangirwa, and J. C. DeMartini.
1996.
Ultrastructural studies on the replication and morphogenesis of Nairobi sheep disease virus, a Nairovirus.
Arch. Virol.
141:1479-1492[Medline].
|
| 27.
|
Satiat-Jeunemaitre, B., and C. Hawes.
1992.
Redistribution of a Golgi glycoprotein in plant cells treated with brefeldin A.
J. Cell Sci.
103:1153-1166[Abstract/Free Full Text].
|
| 28.
|
Schmelz, M.,
B. Sodeik,
M. Ericsson,
E. J. Wolffe,
H. Shida,
G. Hiller, and G. Griffiths.
1994.
Assembly of vaccinia virus: the second wrapping cisterna is derived from the trans-Golgi network.
J. Virol.
68:130-147[Abstract/Free Full Text].
|
| 29.
|
Sodeik, B.,
R. W. Doms,
M. Ericsson,
G. Hiller,
C. E. Machamer,
W. van't Hof,
G. van Meer, and G. Griffiths.
1993.
Assembly of vaccinia virus: role of the intermediate compartment between the endoplasmic reticulum and the Golgi stacks.
J. Cell Biol.
121:521-541[Abstract/Free Full Text].
|
| 30.
|
Stephens, E. B., and R. W. Compans.
1988.
Assembly of animal viruses at cellular membranes.
Annu. Rev. Microbiol.
42:489-516[Medline].
|
| 31.
|
Storms, M.,
R. Kormelink,
D. Peters,
J. van Lent, and R. Goldbach.
1995.
The non-structural protein NSm of tomato spotted wilt virus induces tubular structures in plant and insect cells.
Virology
214:485-493[Medline].
|
| 32.
|
Ullman, D. E.,
D. M. Westcot,
K. D. Chenault,
J. L. Sherwood,
T. L. German,
M. D. Bandla,
F. A. Cantone, and H. L. Duer.
1995.
Compartmentalization, intracellular transport, and autophagy of tomato spotted wilt tospovirus proteins in infected thrips cells.
Phytopathology
85:644-654.
|
| 33.
|
Van der Wel, N. N.,
R. W. Goldbach, and J. W. M. van Lent.
1998.
The movement protein and coat protein of alfalfa mosaic virus accumulate in structurally modified plasmodesmata.
Virology
244:322-329[Medline].
|
| 34.
|
Van Poelwijk, F.,
M. Kikkert,
M. Prins,
R. Kormelink,
M. Storms,
J. van Lent,
P. de Haan,
D. Peters, and R. Goldbach.
1996.
Replication and expression of the tospoviral genome. Proceedings of the International Symposium on tospoviruses and thrips of floral and vegetable crops.
Acta. Hortic.
431:201-208.
|
| 35.
|
Whealy, M. E.,
J. P. Card,
R. P. Meade,
A. K. Robbins, and L. W. Enquist.
1991.
Effect of brefeldin A on alphaherpesvirus membrane protein glycosylation and virus egress.
J. Virol.
65:1066-1081[Abstract/Free Full Text].
|
Journal of Virology, March 1999, p. 2288-2297, Vol. 73, No. 3
0022-538X/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
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Abstract
Introduction
