Review
TRENDS in Plant Science
Vol.10 No.8 August 2005
Plant virus transport: motions of
functional equivalence
Herman B. Scholthof
Department of Plant Pathology and Microbiology, and Intercollegiate Faculty of Virology, Texas A&M University, 2132 TAMU,
College Station, TX 77843, USA
Plant virus cell-to-cell movement and subsequent
systemic transport are governed by a series of mechanisms involving various virus and plant factors. Specialized virus encoded movement proteins (MPs) control the
cell-to-cell transport of viral nucleoprotein complexes
through plasmodesmata. MPs of different viruses have
diverse properties and each interacts with specific host
factors that also have a range of functions. Most viruses
are then transported via the phloem as either nucleoprotein complexes or virions, with contributions from
host and virus proteins. Some virus proteins contribute
to the establishment and maintenance of systemic
infection by inhibiting RNA silencing-mediated degradation of viral RNA. In spite of all the different movement
strategies and the viral and host components, there are
possible functional commonalities in virus–host interactions that govern viral spread through plants.
Plant virus movement
Plant viruses share many general features with animal
viruses – transmission by invertebrate vectors, particle
morphology and composition, and strategies for gene
expression and replication. However, plant viruses face a
unique challenge: to move from an infected cell to adjacent
healthy cells, they must traverse a substantial barrier
that surrounds every host cell – the plant cell wall. The
initial entry of viruses into plant cells occurs by physical
penetration of the cell wall, for example by mechanical
wounding of leaf hairs or epidermal cells, or by insects,
mites or nematodes that feed on the plant. Subsequent
transport of virus material from the initially infected cells
to adjacent cells occurs through the plasmodesmata.
The translocation capacity of the plasmodesmata
channels is controlled in a complex and developmentally
regulated fashion [1,2] but, in general, plasmodesmata
openings are too small for passive passage of whole virus
particles (10–200 nm). To circumvent this physical restriction, plant viruses encode specialized movement proteins
(MPs) that dilate the plasmodesmata openings to enable
the passage of viral nucleic-acid–protein complexes
(VNPs) or sometimes even whole virions [3,4]. Considering
that all plant viruses must travel between cells through
plasmodesmata (there are no known examples of plant
viruses with an ability to lyse cell walls), the range in type
and number of MPs produced by plant viruses, and of the
seemingly different movement strategies are striking [5].
In spite of their many differences, a primary objective of
all plant viruses is to transport infectious material.
Therefore, my intention in this article is first to compare
the composition of the transported materials (i.e. virions
or other complexes) and then to concentrate on functional
similarities between different MPs, their modes of action
and interactions with host proteins. Subsequent comparisons reveal commonalities with regards to vascular spread
and interactions that interfere with RNA silencingmediated defenses to establish and maintain a systemic
infection. The theme throughout is shared functional
principles.
Nature of the viral complex that moves from cell to cell
When comparing the composition of VNPs that spread the
infection, plant viruses can be categorized based on a
single criterion: is the coat protein (CP) required for cellto-cell movement? As shown in Table 1, plant viruses can
be separated into three major types: in type I viruses, the
CP is dispensable for movement and is, therefore, not a
component of the transported material; in type II viruses,
the CP acts as an (auxiliary) MP, either actively or by
protecting the genome; in type III viruses, the CP is
required because these viruses move as particles. Tobacco
mosaic virus (TMV) is the representative member for
type I. TMV encodes a specialized 30 kDa MP and does not
require CP for cell-to-cell movement. Two other examples
of plant viruses that use type I movement are the
taxonomically distinct icosahedral carmoviruses and
Table 1. Classification of plant viruses based on the requirement for coat protein for movement
Classification
Coat protein
Type I
Not Required
Type II
Required
Type III
Particles
a
Exampleb
Tobamovirus
Carmovirus
Hordeivirus
Cucumovirus
Potyvirus
Potexvirus
Geminivirusc
Tospovirus
Comovirus
Closterovirus
MP, cell-to-cell movement protein.
Virus genus designation.
This grouping represents the virus family, and CP requirement is virus species
dependent.
b
Corresponding author: Scholthof, H.B. ([email protected]).
Number of
MPsa
1
2
3
1
2
3
1–2
1 (and tubules)
1 (and tubules)
3–4 (and 2 CPs)
c
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Review
TRENDS in Plant Science
rod-shaped hordeiviruses, which encode two or three
specialized MPs, respectively, referred to as double and
triple gene block proteins (DGBps and TGBps) [5,6].
Type II viruses, exemplified by Cucumber mosaic virus
(CMV), encode an MP that shares many biochemical
characteristics with TMV MP, except the CMV CP is
required for cell-to-cell movement. Under experimental
conditions the CP dependence of CMV is not absolute
because deletion of a C-terminal portion of MP eliminates
the CP requirement for movement [7] (making the mutant
a type I virus). The type II viruses include several with
morphological features, genome organization and
expression strategies unrelated to CMV. As for type I
viruses, certain type II viruses have split their MP into
discrete parts [e.g. the TGBp of Potato virus X (PVX)] or, in
the case of members of the Potyvirus genus, the CP
appears to fulfill the role of MP, together with additional
viral proteins [8]. Another example of a type II representative is the monocot-infecting Panicum mosaic virus,
which uses a unique strategy for the coordinated
expression of four MPs (CP and TGBps) from a single
polycistronic subgenomic mRNA [9]. Geminiviruses not
only use MPs for cell-to-cell movement but also use
specialized proteins to move DNA out of the nucleus [3].
Upon nuclear exit, a VNP is formed that can involve one or
two MPs and the CP for plasmodesmata-mediated
transport. Tospoviruses such as Tomato spotted wilt virus
(TSWV) are normally considered to be a distinct group with
regards to movement because they form tubules [3,5] but,
because the nucleoprotein N (a CP analog) is required for
movement [10], they belong to type II.
Type III viruses also need the CP, but in the form of
virus particles, making them distinct from type II viruses
(Table 1). For example, the Comoviridae encode an MP
that induces the formation of tubules in which the
spherical virus particles assemble in single file. By
extending through the plasmodesmata, the tubules
transport the virus particles in a coordinated fashion to
the adjacent cell [11]. Other examples are Alfalfa mosaic
virus (AlMV) [12] and Brome mosaic virus (BMV) [13].
Members of the Closteroviridae do not form tubules, yet
they are also transported as particles. To achieve this,
these viruses encode several MPs and two different CPs,
and their coordinated action culminates in the deposition
of the (w10!2000 nm) flexuous particles at the plasmodesmatal opening. The concomitant enlargement of the
plasmodesmata opening allows the entry and, presumably, passage of the virus particles [14].
In addition, some viruses apparently have the ability to
make the requirement for CP or particle formation
optional because they can use more than one strategy.
For example, the pararetrovirus Cauliflower mosaic virus
(CaMV) has characteristics typical of both type I movement of VNPs and type III tubule formers. CaMV encodes
a prototypical nucleic acid binding MP that enlarges the
plasmodesmata opening, yet it also forms tubules through
plasmodesmata that contain queued virus particles [15].
Under certain circumstances, it is possible that the MP
transports an infectious VNP (containing pregenomic
RNA and requisite proteins), whereas, under other
conditions (e.g. in a different host), tubules are the
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Vol.10 No.8 August 2005
377
preferred mode of particle transportation, perhaps
through mediation of one or more virus proteins in
addition to the MP. Another example is CMV (type II,
Table 1), which is normally transported as an MP–VNP
(discussed above) but is also able to form tubules. Within
this context, it is also intriguing that Cowpea chlorotic
mottle virus, a species in the same family as CMV (type II)
and in the same genus as BMV (type III), does not require
CP for movement and is thus a type I virus. Likewise,
natural isolates of BMV have been identified that move
independently of CP [16].
In conclusion, when comparing the viral material that
is transported intracellularly and from cell-to-cell, it is
apparent that taxonomically different viruses can use
similar strategies, closely related viruses can use different
strategies and some viruses use more than one strategy.
This illustrates the inherent flexibility of viruses to adjust
the nature of the transported material to specific
circumstances, a property that is probably of key
importance for adaptation to new hosts.
Functional equivalence
When focusing on the mechanism of virus movement
rather than on the transported material, viruses are
typically divided into many separate movement classes:
for example, TMV-like, tubule formers, DGBp viruses,
TGBp viruses and Potyvirus-like. [5]. Recent results
suggest that, among this diverse set of descriptive
mechanisms there are important unifying functional
principles. As mentioned earlier, viruses grouped as
type I (Table 1) differ extensively in genome expression
strategies and in the number and amino acid sequence of
their MPs. However, their functional grouping in Table 1
agrees with the increasing body of evidence that smaller,
segmented MPs have structural and functional similarities
to specific portions of larger, single-unit MPs like that
encoded by TMV [5,6]. Likewise, molecular comparisons
suggest that the requirement for CP in conjunction with the
TGB proteins of PVX can be mimicked by an extra RNA
binding region on one of the hordeivirus TGBps, which
consequently eliminates the CP requirement [17].
The notion of functional equivalence is further supported by findings that the MP of one virus can
complement a movement deficiency of another, unrelated
virus. This has been demonstrated for different viruses
within type I, including the complementation of Barley
stripe mosaic virus movement by the TMV MP [18], and
the finding that a dianthovirus MP is functionally
competent to move TMV [19]. However, complementation
also can occur for viruses with seemingly different
movement strategies. For instance, the type II CMV MP
plus its cognate CP (or the C-terminal deletion MP mutant
in the absence of CP) complement the activity of the type I
TMV MP [20]. CMV also complemented PVX (both type II)
but was less efficient [20].
Another comparison that shows functional commonality relates to the biochemical properties of TMV MP
(type I) and the MP encoded by members of the
Comoviridae (type III, tubule formers). The comovirus
MP interacts with the CP [21] and is required for the
tubules to grow through the plasmodesmata to deposit
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Review
TRENDS in Plant Science
virions in the adjacent mesophyll cells [11]. This is
different from the type I movement of TMV, yet
biochemical analyses showed that, like TMV MP, the
comovirus MP is also a non-sequence-specific nucleic acid
binding protein [22]. Furthermore, a nepovirus (Comoviridae) MP is transported to the plasma membrane via a
secretory pathway that might, under certain circumstances, involve microtubules or microfilaments [23], and
such filaments can also interact with TMV MP [4].
Predicted structural core similarities for MPs of different viruses were also noted upon extensive sequence
comparisons [97].
Evidence is accumulating from genetic experiments
that viral replicases can also contribute to movement
[24,25] and a recent finding shows that translation
initiation factors might be involved in cell-to-cell trafficking [26]. These developments suggest that translation,
replication and movement are components of one continuous intra- and intercellular infection process. To explore a
component of this concept further, I will now compare in
some detail the movement properties of TSWV with those
recently reported for the seemingly entirely unrelated
TMV. TSWV is an enveloped spherical virus (w100 nm)
containing VNPs of three genomic segments of negative or
ambisense polarity whereby either the RNA strand
complementary to the genomic RNA is translated or both
strands serve as mRNA, respectively. The virus is
transmitted by thrips (Thysanoptera: Thripidae; small
insects with piercing mouthparts). TMV is a rigid rodshaped virus (w18!300 nm) containing a single-stranded
positive-sense RNA genome that is transmitted via
mechanical wounding of epidermal cells.
TMV forms an RNA–MP complex for translocation
through plasmodesmata [3,4]. The N protein (a CP) of
TSWV and its genomic RNAs form CP–RNA structures
that can be considered to be analogous to the TMV MP–
RNA complexes [10]. In the case of TSWV, this complex is
engulfed by a membrane enveloped structure (tubule) that
contains the replicase [3,5,10]. A recent study suggests
that the TMV RNA–MP complex also associates with
membrane structures whose formation is influenced by
the CP [27]. These VNP–membrane complexes contain the
viral replicase [28] (Figure 1) and are therefore functionally reminiscent of the membrane-enveloped vesicle-like
structures identified as replication complexes for BMV
[29]. The intriguing new notion in the context of this
article is the implication that the entire TMV VNP
replication complex is transported to [30] and through
[28] plasmodesmata to enable immediate replication once
deposited in the adjacent cell.
Therefore, it seems that for TSWV as well as for TMV,
and perhaps for plant viruses in general, not only is
replication associated with membranes but also transport
of the VNP–replicase complex might be mediated by
membranes for movement to and even through the
plasmodesmata into the neighboring cell (Figure 1). The
origin of membranes (e.g. endoplasmic reticulum or
plasma membrane) and the level of plasmodesmatal
destruction can be different, but the purpose here is to
offer the possibility that seemingly different movement
strategies represent divergent types of similar ancestral
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Vol.10 No.8 August 2005
transport archetypes. Experimental support for this idea
comes from a recent observation that TMV producing the
TSWV MP causes tubule formation as well as movement of
TMV [31].
Host proteins interacting with MPs
Biochemical studies have shown that the nucleic acid
binding associated with MPs is not amino acid sequence
specific [4]. The examples of complementation in the
previous section also illustrate that MPs lack specificity
for recognition of the transported genome. For cytoplasmic
viruses, MPs are probably translated close to the genome
(perhaps subcompartmentalized) and will bind promiscuously to any viral genomes (or host RNAs) in the vicinity.
Thus, the ability of a virus to move in any given host is
determined not so much by compatibility between the
genome and the MP as by crucial interactions between the
MP (binding any genome) and host proteins.
Based on a three-dimensional model for TMV MP [32]
and biochemical fractionation experiments [3], it is
thought that MPs are transmembrane proteins with
exposed hydrophilic portions that could potentially interact electrostatically with plant proteins. In agreement
with this, several host proteins have now been identified
that interact with MPs; these are categorized in Table 2
according to their (predicted) cellular function or biochemical activity. Many of these host factors have recently
been reviewed in the context of how plants exchange
macromolecular complexes [33] and are therefore only
briefly discussed here.
Table 2 shows that several type I MPs (Table 1) interact
with transcription factors. Possible working models are
that the MP–transcription-factor interaction either
induces the expression of genes that are important for
virus transport or interferes with the expression of
defense-related genes. In addition, some of these transcription factors are non-cell-autonomous proteins that
are transported together with their homologous mRNA
through plasmodesmata [34]. It is therefore conceivable
that they chaperone the VNP (perhaps in a complex as in
Figure 1) to and even through plasmodesmata.
Because MPs can be post-translationally modified, it is
perhaps not surprising that some regulatory enzymes
interact with viral MPs (Table 2). Other host proteins that
interact with MPs are surface-associated proteins, chaperone-like proteins and cytoskeletal proteins (Table 2).
The few known MP interacting proteins involved in vesicle
trafficking are limited to viruses that form tubules
(Table 2), although TGBps (type II) might also be involved
in promoting transport via vesicles through interaction
with a chaperone [35].
Thus, although it appears that a myriad of different
host factors interact with viral MPs, the concept of
functional equivalence suggests that most MP interacting
host proteins could provide direction for transport towards
the cell periphery or even directly to the plasmodesmata.
Evidence for a direct role in movement remains to be
provided for proteins listed in Table 2. However, irrespective of the underlying mechanism, the great variation in
host encoded proteins that interact with individual MPs of
different viruses agrees with the supposition that the
Review
TRENDS in Plant Science
Directed transport
of VRC to and perhaps
through PD
TMV
Directed transport
of VRC via tubules
TSWV
TRENDS in Plant Science
Figure 1. Cell-to-cell movement of Tobacco mosaic virus (TMV) and Tomato spotted
wilt virus (TSWV). TMV forms rod-shaped virions (green rod) and TSWV forms
membrane-enveloped particles (green sphere, with exposed glycoproteins represented as spikes). In spite of their morphological differences, during infection of
cells, each virus forms a membrane-associated complex that moves to or even
through plasmodesmata. Dark- and light-blue spheres represent coat protein (CP)
and movement protein (MP), respectively, associated with viral RNA. Yellow
spheres represent replicase protein and the red structures denote membranes.
Abbreviations: PD, plasmodesmata; VRC, viral replication complex.
precise MP–host-protein combination is decisive in
determining whether a plant can serve as a host.
Long-distance transport
The phase following cell-to-cell movement involves systemic virus spread from the local infection sites to other
plant parts. For this purpose, most viruses spread along
with the solutes through the phloem. The transport of
VNPs or virions from mesophyll cells into phloem tissue is
a major hurdle and this process is often compromised,
explaining the well known phenomenon that longdistance transport is a crucial host range determinant
[5]. Therefore, it is generally assumed that viruses also
use host factors to achieve a systemic infection. Experimental evidence has been obtained for a few protein
candidates [4] (Table 3). One example is a cadmiuminduced glycine-rich protein of Nicotiana tabacum that
might regulate TMV movement by controlling callose
deposits at specific symplastic connections [36].
Functional genomics studies with Arabidopsis have
revealed the importance of specific host genes in controlling vascular movement of a Tobamovirus or a Potyvirus
(Table 3), but the mechanism by which the gene products
operate remains to be resolved [37–39].
As for cell-to-cell movement (Table 1), the CP is often a
major factor for the long-distance transport of viruses [19].
However, the capacity in which the CP contributes
Table 2. Categories of host factors that interact with movement
proteins
Host factor
Transcription-related factors
KELP, MBF1, HFi22
Enzymes
Kinase, acetylase
Surface-associated proteins
pme, AtP8, TIPs
Cytoskeleton
e.g. Actin, tubulin
Chaperone
DNAJ-like
Vesicle trafficking
Knolle or Rab-like
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Movement protein type
Refs
I
[62–65]
I, II
[66,67]
I, II
[68–71]
I, III
[72–75]
II, III
[10,35]
(II) III
[23,76]
Vol.10 No.8 August 2005
379
remains to be clarified for most viruses, although a recent
study shows that this might be a general principle because
CPs of unrelated viruses can complement [40]. Studies
with CMV suggest that VNPs are deposited into the sieve
elements where virions are assembled for further transport [41]. Umbraviruses do not encode a typical CP but
instead another viral protein that covers the RNA, and the
formation of this flexuous VNP is required for longdistance spread [42]. For some viruses, such as Tomato
bushy stunty virus (TBSV), the CP is qualitatively
dispensable for long-distance transport in some experimental hosts [19]. But even for TBSV the most effective
systemic invasion occurs upon the formation of virions or
alternative CP–VNPs [43–45].
Except for phloem-limited viruses, the final phase of
the infection cycle for most viruses involves egress from
the vasculature [46]. This process is poorly understood but
recent results have shown that a host-encoded pectin
methylesterase can be involved in vascular exit of the
TMV virion or CP–VNP [47] (Table 3). Other virus and
host factors that are thought to be involved in longdistance movement are listed in Table 3. For most of the
proteins grouped in the top half of Table 3, their functional
roles are not yet clear but, in some cases, they could
involve protein–protein interactions that compromise the
induction of resistance responses [48,49].
Suppression of gene silencing
RNA silencing is an effective mechanism that plants use
for targeted degradation of viral genomes. To counteract
this defense, plant viruses encode suppressors of gene
silencing [50,51]. A 19 kDa protein (P19), unique to the
Tombusvirus genus of plant viruses, is a well characterized pathogenicity protein [45,52,53] that is now
renowned as a suppressor of gene silencing [50]. P19
forms dimers in vivo and in vitro [53], and this
homodimerization is essential for virus spread and
suppression of RNA silencing [45,52,53]. Furthermore,
full functional activity of P19 for suppression and virus
spread requires its production at relatively high levels
[54,55]. This is in agreement with the finding that P19
binds the double-stranded short interfering RNAs
(siRNAs) that are abundantly produced during virusinduced RNA silencing [56]. The X-ray crystallographic
structure of the P19–siRNA complex [57,58] revealed an
elegant structural basis for the binding of precisely
measured 21 nucleotide siRNAs by P19 dimers. It is
therefore likely that the appropriation of the prolifically
accumulating siRNAs by P19 renders these unavailable
for activation of the RNA-induced silencing complex.
Many of the virus encoded suppressors were previously
identified as pathogenicity factors involved in systemic
invasion (Table 3, bottom half). Thus, a likely common
objective of suppressors is to prevent RNA silencingmediated destruction of viral RNA to permit a
systemic infection to become established or to be
maintained. As for MPs, this shared goal again agrees
with the observation that suppressors of different
viruses can complement each other [59], even if their
precise biochemical roles and targets in the RNA silencing
pathway are different [60].
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Vol.10 No.8 August 2005
Table 3. Examples of virus factors other than typical movement proteins and coat proteins that are involved in systemic invasion,
and host proteins either known to have a role or that interact with viral factors
Virus(genus)
Caulimovirus
Closterovirus
Hordeivirus
Potyvirus
Umbravirus
Bromovirus
Geminivirus
Polerovirus
Potyvirus
Potyvirus
Tobamovirus
Tobamovirus
Comovirus
Cucumovirus
Closterovirus
Hordeivirus
Polerovirus
Pecluvirus
Tobamovirus
Carmovirus
Potexvirus
Potyvirus
Tombusvirus
Virus protein
Biochemical role in movement unclear
P6
L-Pro, P20 (CHsp70)
bb
6K2
P3
CPa
4b
AL2 L2
4b
P17
VPg
4b
?
?
MPa
4b
Suppressors of RNA silencing
CPa
2b
CPa, P20–21, P23
gb
P0
P15
Rep
CPa
4b
TGBp1a
4b
HC-Pro
4b
P19
4b
Host protein
Refs
HCP1
Kinases
PVIP
RTM1, RTM2
vsm1, ciGRP
Pme
[48,77]
[78,79]
[80]
[81]
[42]
[82]
[49]
[88]
[64]
[38,39]
[36,37]
[47]
TIPc
TIPp
Cmd, RING
REF
[83]
[50,84]
[85,86]
[59,87]
[89]
[90]
[24,91]
[92,93]
[6,70,94]
[8,50,95]
[50,53,96]
Abbreviations: CP, coat protein; MP, movement protein.
a
Only CPs or MPs are listed that either have an interactive partner that might assist in spread, or where the function involves an additional novel property associated with virus
invasion.
b
Interaction between the virus and host protein has been demonstrated.
Separate suppressors interact with a range of host
factors (Table 3). Although their functional role has yet to
be determined, this variation could involve host-dependent roles. In support of this notion is the observation that
P19 performs host-specific activities [45,52,53]. In this
context, the question that can be posed for P19 and most
other suppressors is whether their interference with RNA
silencing underlies all their pathogenic phenotypes or if
they can perform additional biochemical functions independent of suppressing RNA silencing that contribute to
virus spread in a host-dependent manner.
Concluding remarks
More than a century ago, Martinus Beijerinck introduced
the concept of a virus as a contagium vivum fluidum
(i.e. contagious living liquid) and, O70 years ago, Geoffrey
Samuel demonstrated that the movement pathway of
viruses through plants follows the transport of nutrients
[61]. These were major discoveries that formed the
beginning of modern research in virology and plant virus
movement. Over the years, viruses were placed in
taxonomic groups based on various properties, lately
predominantly influenced by their genomic composition. Recently, plant viruses have also increasingly
been distinguished according to their movement
strategy, and the latest studies illustrate the great
wealth and variety of virus and host components
involved in virus transport. However, when focusing
on general functional themes, there are commonalities
that suggest the co-evolution of modi operandi,
whereby differences in the biochemical details have
been adapted to accommodate particular host–environment situations.
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Throughout this review, several processes are described
for which the precise mechanism is unknown, therefore,
many fascinating challenges still lie ahead. For example,
studies of the functional role of identified host factors
should substantially improve our understanding of how
the contagium is vivum and fluidum.
Acknowledgements
I am grateful to the American Society for Virology for the invitation to
present a ‘State of the Art’ lecture (July 2004) on virus movement, which
formed the basis and impetus for this review. I appreciate the financial
support from the National Science Foundation (MCB 0131552) to study
virus movement. I thank Rick Nelson, Scott Adkins and Dennis
Lewandowski for sharing information that was in press for publication,
and Karen-Beth G. Scholthof for constructive comments during the
various stages of manuscript preparation.
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