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Parallels and distinctions in the direct cell-to-cell spread of the plant and animal viruses
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Parallels and distinctions in the direct cell-to-cell spread of the plant and animal viruses Christophe Ritzenthaler The paradigm that viruses can move directly, and in some cases covertly, between contacting target cells is now well established for several virus families. The underlying mechanisms of cell-to-cell spread, however, remain to be fully elucidated and may differ substantially depending on the viral exit/entry route and the cellular tropism. Here, two divergent cell-to-cell spread mechanisms are exemplified: firstly by human retroviruses, which rely upon transient adhesive structures that form between polarized immune cells termed virological synapses, and secondly by herpesviruses that depend predominantly on pre-existing stable cellular contacts, but may also form virological synapses. Plant viruses can also spread directly between contacting cells, but are obliged by the rigid host cell wall to move across pore structures termed plasmodesmata. This review will focus primarily on recent advances in our understanding of animal virus cell-to-cell spread using examples from these two virus families to highlight differences and similarities, and will conclude by comparing and contrasting the cell-to-cell spread of animal and plant viruses. Address Institut de Biologie Mole´culaire des Plantes (IBMP), CNRS and Universite´ de Strasbourg, 12, rue du Ge´ne´ral Zimmer, 67084 Strasbourg, France Corresponding author: Ritzenthaler, Christophe ([email protected])
Current Opinion in Virology 2011, 1:403–409 This review comes from a themed issue on Virus replication in animals and plants Edited by Anne Simon and Grant McFadden Available online 14th October 2011 1879-6257/$ – see front matter # 2011 Elsevier B.V. All rights reserved. DOI 10.1016/j.coviro.2011.09.006
Introduction Contrarily to mammalian cells, plant cells are surrounded by a cell wall that prevents direct contact between adjacent cells. This physical barrier is a major bottleneck that plant viruses have to overcome to able to spread from cellto-cell for the subsequent systemic invasion of their host. To do so, plant viruses exploit specific cell wallembedded pores, analogous to the gap junctions in animal cells, named plasmodesmata (PD) that provide symplastic continuity throughout most of the plant. Anatomically, the plasma membrane forms the outer limits of PD, and www.sciencedirect.com
the desmotubule, derived from the endoplasmic reticulum (ER), forms the central axial core of PD (Figure 1a). Longitudinal views reveal that PD are often narrowed at either end forming a so-called collar or neck constriction. This constriction is the result of callose deposition between the plasma membrane and the wall in response to stresses such as plasmolysis or physical wounding and is one point of regulation of molecular flow from cell-to-cell. The structure, ontogeny, composition, and functional diversity of PD have been reviewed extensively in recent years [1–6] and so will not be discussed here due to word limitation [1–6]. Regarding PD permeability, the space between the plasma membrane and the desmotubule provides the conduit for the diffusion of soluble molecules within the natural size exclusion limit (SEL) of the pore. Passive PD transport is exemplified by translocation of solutes, small RNAs, proteins including specific transcription factors, and marker molecules such as GFP or fluorescent dextrans [5,7–9]. Per se, PD are incompatible with the (passive) transport by diffusion of a whole set of macromolecules including endogenous noncell autonomous proteins and, of course, plant viruses and/or full-length viral genomes. In this latter case, an active transport mechanism involving specific interactions between viral components and the PD translocation machinery occurs, leading to the specific dilatation of PD. In this review, we will focus on the different active transport strategies developed by plant viruses to overcome the limitation in size imposed by PD with special emphasis on the parallels and distinction that exist between cell-to-cell movement of plant and animal viruses. It should be noted that the use of ‘transmission’ to refer to cell-to-cell movement of viruses [10] was carefully avoided here to prevent confusion as it corresponds to the commonly accepted definition of host-to-host propagation of plant viruses by mechanical means or via vectors [11,12].
Historical viewpoint: translocation of virion versus nucleoprotein complex The first hints toward understanding how viruses could move through PD came from early observations of infected plant tissues by electron microscopy reporting the accumulation of virus-like particles in the interior channel of PD. The presence of particles in PD was most frequent with nonenveloped icosahedral virus in particular the pararetrovirus Cauliflower mosaic virus (CaMV) or members of the picorna-like nepovirus and comovirus [13–16], but were also observed with rod-shaped virus Current Opinion in Virology 2011, 1:403–409
404 Virus replication in animals and plants
Figure 1
(a)
bunyaviridea, or the bacilliform rhabdovirus Pittosporum vein clearing virus has also been reported [21,22]. On the basis of these early observations, the concept emerged that cell-to-cell translocation of viruses through PD occurs in an encapsidated form, that is, as entire virions or nucleocapsids.
Cell 2 (b) ER
PM
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Cell 1 (c)
(d)
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Current Opinion in Virology
Modes of cell-to-cell spread of plant viruses. (a) A cartoon of a plasmodesma. The plasmodesma is seen as a plasma-membrane (PM)lined channel through the cell wall containing a central endoplasmic reticulum (ER)-derived rod-shaped desmotubule (DT). The location of actin filaments and PDLP in the symplastic channel and the PM components is illustrated. Callose (Cal) accumulates at the neck region of PD. (b) Model for PD modification by nontubule forming MP. In the presence of TMV MP, actin severing by MP and reduced accumulation of callose at the PD neck region lead to dilation of the PD pore. NPC consisting of viral RNA, MP and host factors can then move through PD by lateral diffusion along the desmotubule. (c) and (d) Model for PD modification by tubule forming MP. Assembly of tubule forming MP into tubules occurs upon interaction of the MP with PDLP and leads to the removal of the desmotubule inside PD. Virions may then be transported between cells through polar tubule assembly-driven and disassemblydriven treadmilling as indicated by the arrow (c). Alternatively, tubule may promote the passage of NPC consisting of vRNA and CP (d).
such as Tobacco mosaic virus (TMV) [17,18], Potato virus X (PVX), a potexvirus [19], Beet yellows virus (BYV), a closterovirus [20], and Potato virus Y (PVY), a potyvirus [18]. Although scarce, the presence in PD of enveloped viruses like Tomato spotted wilt virus (TSWV), a plant-adapted Current Opinion in Virology 2011, 1:403–409
The molecular characterization of virus translocation mechanisms through PD started with the groundbreaking discovery that TMV encodes a specific protein required for viral cell-to-cell movement, namely the 30K protein. This protein was given the name ‘movement protein’ or MP for its unique capacity to restore the cell-to-cell movement deficiency of TMV strains with mutated MP [23,24]. Thus, transgenic plants expressing the TMV 30K complement, in trans, mutated TMV strains lacking a functional MP [23,25]. Sensu stricto, MP defines virus-encoded proteins necessary for spreading viral infections, but which have little or no impact on replication in single cells. In TMV, the CP and MP are both optional for replication, but only the MP is needed for cell-to-cell movement [25]. It should be noted that the TMV replicase is also directly or indirectly involved in virus movement but cannot be considered as a bona fide MP, as it is required for viral replication and displays additional suppression of silencing activity [26–28]. It is now well established that TMV MP localizes to PD and increases the SEL without inducing obvious ultrastructural changes in PD architecture [29]. In addition, the 30K is able to bind, in a cooperative but sequence nonspecific manner, single stranded nucleic acids including fulllength TMV viral RNA (vRNA) [30,31]. Atomic force microscopy further revealed that the diameters of the MP–vRNA nucleoprotein complex are in the range of 1.5–3.5 nm [32,33], hence close to the dimensions of the dilated PD microchannels [7,29]. Consistent with these findings, the general consensus emerged that TMV traffics from cell-to-cell in the form of a nucleoprotein complex (NPC, Figure 1b).
The diversity of MP Nearly a quarter of a century after the characterization the TMV MP, it appears that most, and probably all plant viruses encode one or more MPs. Recognized MPs display considerable structural diversity and fall into at least four different phylogenetic groups, the largest and probably best characterized being the ‘30K’ superfamily named after its prototype member, the TMV 30K [34– 37]. The number of encoding genes per viral genome and size of MP is also highly variable. Thus, viruses with MP belonging to the 30K superfamily generally encode a single MP in the 30–40 kDa range [38], whereas the MP of tymovirus is nearly 70 kDa [39] and those of closterovirus only 6 kDa [40–42]. Cell-to-cell transport of carmovirus is aided by a set of two small virus-encoded polypeptides no larger than 12 kDa, referred to as the double gene block proteins (DGB) [43–45]. The family www.sciencedirect.com
Cell-to-cell movement of plant viruses Ritzenthaler 405
Potyviridae to which belong approximately 30% of known plant viruses, is thought to encode also two MPs, the cylindrical inclusion protein (CI) and the recently identified P3N-PIPO [46–50]. Finally, a complex of three MPs (7–25 kDa) is necessary for the movement of the triple gene block (TGB) group of viruses belonging to the Virgaviridae and Flexiviridae families that includes potexvirus and hordeivirus [51,52]. It should be noted that besides MP, structural proteins are often required for movement. An example of extreme involvement of structural proteins is provided by the closterovirus BYV in which four out of five proteins participating in the cell-tocell movement machinery are integral virion components [53]. It is now clear that during the course of plant virus evolution, a number of MPs evolved to allow the viral genome to cross the barrier of the host cell wall. This is in sharp contrast to animal viruses for which in the majority of cases proteins specifically dedicated to cell-to-cell movement have not been identified. An exception to this may be herpesviruses, which encode a heterodimer of glycoproteins (gE/gI), which are not required for cell-free viral entry but are essential for efficient cell-to-cell spread [54]. The role of this glycoprotein heterodimer appears to be to target the virus to intercellular basolateral junctions, allowing direct access to viral receptors on the opposing target cell membrane [55,56]. Other exceptions may include the few viruses that are able to replicate in both plants and animals. An excellent illustration of the unique adaptation of animal viruses to plants is provided by Tospovirus, the sole genus within the family Bunyaviridae with plant tropism [57]. In this virus, the nonstructural protein NSm produced by the ambisense M RNA is not encoded by any of the animal-infecting members of the Bunyaviridae. The NSm protein of TSWV possess typical features of plant MPs, including presence in cellular fractions enriched for cell walls and cytoplasmic membranes, intracellular localization close to PD and modification of PD structure via the formation of tubules (see below for more details), RNA binding properties and also interactions with a host trafficking protein [22,58–63]. Direct evidence for the function of TSWV NSm protein in virus movement was generated by complementation of a movement-deficient TMV vector by heterologous expression of NSm [60]. In sharp contrast to the vast diversity of MP, the present picture suggests the existence of only two main strategies for plant virus cell-to-cell movement, one in which the viral genome moves as intact virions and another where the viral nucleic acids are trafficked through PD in the form of a NPC (Figure 1). At the ultrastructural level, the two strategies are readily distinguishable. The former socalled tubule-guided mechanism is accompanied by profound modifications in PD architecture through the removal of the desmotubule and its replacement by www.sciencedirect.com
tubular structures containing viral particles or in some cases NPCs (Figure 1c,d). The second strategy applies to the majority of plant viruses including TMV and involves, at most only minor structural changes in PD architecture [64,65]. Viruses belonging to this group encode single or multiple MP generally with affinity for membranes, in particular for the ER that extends in PD to form the desmotubule. With the help of specific host factors that are still largely unknown, the movement of the NPC via PD is thought to occur by lateral movement along the membranes upon relaxation of the PD aperture. Recently, two such factors that facilitate TMV movement have been identified. Actin, which is suggested by a recent study shows that several viral MPs may sever actin filaments to relax the PD during their cell-to-cell movement [66], whereas ankyrin is thought to downregulate the deposition of callose [67]. Because of space limitation, the remaining part of this review will essentially focus on recent advance in our understanding of tubuleguided viral dissemination strategies. Extensive recent reviews on nontubule-guided movement have been published elsewhere [2,5,68,69].
Tubule-guided movement Tubule-guided mechanism applies to a whole set of plant viruses with RNA or DNA genomes sharing in common a single MP with tubule-forming capacity (for an extensive list of virus employing tubule-guided movement see Refs. [70,71]). This group typically includes viruses with icosahedral symmetry such as Cowpea mosaic virus (CPMV), Grapevine fanleaf virus (GFLV) or CaMV, but the situation of filamentous or enveloped virus is not always clearly defined. MPs with tubule-forming capacity have been classified in the 30K superfamily, although in groups that are phylogenetic distinct from nontubuleforming MP groups [36]. The ability of specific MP to form tubules was first observed with CPMV whose infection leads to the production of tubular structures containing a single row of virus-like particles extending from the entry of PD in one cell, into the cytoplasm of a neighboring cell. Early genetic and immunological studies revealed that the RNA2-encoded 48K protein is a structural component of the tubule and essential for cellto-cell movement of CPMV [72,73]. Further work showed that the 48K MP is the only viral protein needed for tubule formation and tubules produced upon ectopic expression of the MP are identical to those observed upon infection, except for the lack of virions in the tubule lumen [74–76]. Since then, the intrinsic property of MP to assemble into tubules in the absence of other viral proteins has been demonstrated not only with various icosahedral viruses even when fused to GFP [16,59,77– 83] but also with rod-shaped viruses [84,85]. A remarkable feature of these MP is their ability to assemble into tubules when expressed in protoplasts, hence in the absence of cell wall and consequently of PD. Amazingly, a number of these proteins, also maintain their capacity to Current Opinion in Virology 2011, 1:403–409
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form tubules when expressed in insect cells [59,77,80,86]. Although the functionality of such tubules cannot easily be probed, they appear to be structurally similar to those produced in plants. However, the NSm protein of TSWV that forms tubule on the surface of insect cells (Spodoptera frugiperda) is unable to do so in infected thrips tissue, the vector of TSWV, raising the question of whether NSm has a function at all during the insect life cycle of TSWV [87]. This contrasts with the reoviridae Rice dwarf virus (RDV), a phytoreovirus that multiplies also in plants and in invertebrate insect vectors. Infection of cultured leafhopper cells with RDV leads to the formation of tubules along actin-based filopodia composed of the nonstructural viral protein Pns10 and containing viral particles. In cultured cells, Pns10 has the intrinsic ability to form tubules extending out of the cells in a manner involving the actomyosin and secretion system but not microtubules [88,89]. Electron tomography revealed that the Pns10 tubules are uniform in size with an inner diameter of 75 6 nm resulting in direct contact between the RDV particles and the inner surface of the tubule [90]. All this suggests that one of the ways RDV could spread among cells of its insect vector is through virus-induced tubular structures. Sensu stricto, tubule-guided movement refers the transport of virus particles in the inner channel formed by the MP assembled into tubules. Mechanistically, two possibility exist for this type of transport, the first whereby virions would be able to transit autonomously in the lumen of the tubules similarly to cars inside a tunnel and a second, related to treadmilling, in which virions would be incorporated simultaneously to the MP at one end of growing tubules and released at the other end upon removal of the MP and/or depolymerization of the tubule. The latter, more likely mechanism, implies direct or indirect interactions between the MP and the virion/CP, which has been demonstrated for several viruses including CPMV, CaMV and Alfalfa mosaic virus (AMV). In all these cases, interactions were triggered by small C-terminal domains of MPs dispensable for tubule formation but generally required for movement [91–94]. Additionally, the C-terminus of the CPMV MP was shown to be necessary for the incorporation of virus particles in the tubule, suggesting that it is located inside the tubular structure [95]. Probably the best evidence in favor of treadmilling comes from a CPMV MP point mutant able to form tubules containing virus particles, but unable to support cell-tocell movement. It is likely that this mutant with increased tubules stability interferes with viral spread by preventing breakdown or disassembly of tubules and thereby release of virions in neighboring cells [94]. It also strongly supports the notion that CPMV, a virus with an ssRNA genome, exclusively moves as encapsidated particles Current Opinion in Virology 2011, 1:403–409
via tubules. The same rule seems to apply likely to GFLV, a close relative of CPMV [16,96], and also CaMV, a virus with dsDNA genome and whose MP allows only the transport of virus particles in a heterologous system adapted from AMV [97]. Paradoxically, using the same AMV-derived experimental system [98], noncognate tubule-forming MP from different genera including comovirus, nepovirus, and caulimovirus supported the transport from cell-to-cell of RNA3 of AMV, but only on the condition that specific interactions between the various MPs and AMV CP were maintained [93,97]. Preservation of such interactions was achieved through the addition of the CP-binding domain of the AMV MP (44 C-terminal residues) to the different MP [93]. Importantly, these experiments were performed in the presence of a mutated AMV CP defective in virion assembly [98]. Under such circumstances where cell-to-cell movement occurs and tubules are synthesized but no virions are produced, one can only conclude that the various tubuleforming MP can mediate the transports of AMV RNA/CP complexes through tubules as depicted in Figure 1d. To date the molecular mechanism leading to the physical remodeling of the PD, in particular the displacement of the desmotubule, remains elusive. Perhaps a first step in this direction has recently been achieved through the identification of a family of host proteins, conserved throughout higher plants and located in the plasmamembrane lining the interior of PD that promote the spread of viruses employing tubule-guided movement but not of TMV [99]. These type I membrane proteins named PDLP [100] provide a receptor-like function for anchoring MP at PD [99]. It is possible that the specific interaction between PDLP and tubule forming MP at PD may nucleate tubule self-assembly that would then lead to the removal of the desmotubule (Figure 1c). A future challenge will be to identify novel host proteins with agonist function in virus movement and determine the atomic structure of the moving complexes in situ.
Acknowledgement CR is supported by the ANR the region Alsace and is a CNRS fellow.
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61. Storms MMH, Va C, De N, Schoot R, Prins M, Kormelink R, Va JWM, Lent N, Goldbach RW: A comparison of two methods of microinjection for assessing altered plasmodesmal gating in tissues expressing viral movement proteins. Plant J 1998, 13:131-140.
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62. Soellick T, Uhrig JF, Bucher GL, Kellmann JW, Schreier PH: The movement protein NSm of tomato spotted wilt tospovirus (TSWV): RNA binding, interaction with the TSWV N protein, and identification of interacting plant proteins. Proc Natl Acad Sci U S A 2000, 97:2373-2378. 63. Paape M, Solovyev AG, Erokhina TN, Minina EA, Schepetilnikov MV, Lesemann DE, Schiemann J, Morozov SY, Kellmann JW: At-4/1, an interactor of the tomato spotted wilt virus movement protein, belongs to a new family of plant Current Opinion in Virology 2011, 1:403–409
79. Canto T, Palukaitis P: Subcellular distribution of mutant movement proteins of cucumber mosaic virus fused to green fluorescent proteins. J Gen Virol 2005, 86:1223-1228. 80. Liu C, Ye L, Lang G, Zhang C, Hong J, Zhou X: The VP37 protein of broad bean wilt virus 2 induces tubule-like structures in both plant and insect cells. Virus Res 2011, 155:42-47. 81. Zheng H, Wang G, Zhang L: Alfalfa mosaic virus movement protein induces tubules in plant protoplasts. Mol Plant Microbe Interact 1997, 8:1010-1014. www.sciencedirect.com
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Current Opinion in Virology 2011, 1:403–409
Parallels and distinctions in the direct cell-to-cell spread of the plant and animal viruses Christophe Ritzenthaler The paradigm that viruses can move directly, and in some cases covertly, between contacting target cells is now well established for several virus families. The underlying mechanisms of cell-to-cell spread, however, remain to be fully elucidated and may differ substantially depending on the viral exit/entry route and the cellular tropism. Here, two divergent cell-to-cell spread mechanisms are exemplified: firstly by human retroviruses, which rely upon transient adhesive structures that form between polarized immune cells termed virological synapses, and secondly by herpesviruses that depend predominantly on pre-existing stable cellular contacts, but may also form virological synapses. Plant viruses can also spread directly between contacting cells, but are obliged by the rigid host cell wall to move across pore structures termed plasmodesmata. This review will focus primarily on recent advances in our understanding of animal virus cell-to-cell spread using examples from these two virus families to highlight differences and similarities, and will conclude by comparing and contrasting the cell-to-cell spread of animal and plant viruses. Address Institut de Biologie Mole´culaire des Plantes (IBMP), CNRS and Universite´ de Strasbourg, 12, rue du Ge´ne´ral Zimmer, 67084 Strasbourg, France Corresponding author: Ritzenthaler, Christophe ([email protected])
Current Opinion in Virology 2011, 1:403–409 This review comes from a themed issue on Virus replication in animals and plants Edited by Anne Simon and Grant McFadden Available online 14th October 2011 1879-6257/$ – see front matter # 2011 Elsevier B.V. All rights reserved. DOI 10.1016/j.coviro.2011.09.006
Introduction Contrarily to mammalian cells, plant cells are surrounded by a cell wall that prevents direct contact between adjacent cells. This physical barrier is a major bottleneck that plant viruses have to overcome to able to spread from cellto-cell for the subsequent systemic invasion of their host. To do so, plant viruses exploit specific cell wallembedded pores, analogous to the gap junctions in animal cells, named plasmodesmata (PD) that provide symplastic continuity throughout most of the plant. Anatomically, the plasma membrane forms the outer limits of PD, and www.sciencedirect.com
the desmotubule, derived from the endoplasmic reticulum (ER), forms the central axial core of PD (Figure 1a). Longitudinal views reveal that PD are often narrowed at either end forming a so-called collar or neck constriction. This constriction is the result of callose deposition between the plasma membrane and the wall in response to stresses such as plasmolysis or physical wounding and is one point of regulation of molecular flow from cell-to-cell. The structure, ontogeny, composition, and functional diversity of PD have been reviewed extensively in recent years [1–6] and so will not be discussed here due to word limitation [1–6]. Regarding PD permeability, the space between the plasma membrane and the desmotubule provides the conduit for the diffusion of soluble molecules within the natural size exclusion limit (SEL) of the pore. Passive PD transport is exemplified by translocation of solutes, small RNAs, proteins including specific transcription factors, and marker molecules such as GFP or fluorescent dextrans [5,7–9]. Per se, PD are incompatible with the (passive) transport by diffusion of a whole set of macromolecules including endogenous noncell autonomous proteins and, of course, plant viruses and/or full-length viral genomes. In this latter case, an active transport mechanism involving specific interactions between viral components and the PD translocation machinery occurs, leading to the specific dilatation of PD. In this review, we will focus on the different active transport strategies developed by plant viruses to overcome the limitation in size imposed by PD with special emphasis on the parallels and distinction that exist between cell-to-cell movement of plant and animal viruses. It should be noted that the use of ‘transmission’ to refer to cell-to-cell movement of viruses [10] was carefully avoided here to prevent confusion as it corresponds to the commonly accepted definition of host-to-host propagation of plant viruses by mechanical means or via vectors [11,12].
Historical viewpoint: translocation of virion versus nucleoprotein complex The first hints toward understanding how viruses could move through PD came from early observations of infected plant tissues by electron microscopy reporting the accumulation of virus-like particles in the interior channel of PD. The presence of particles in PD was most frequent with nonenveloped icosahedral virus in particular the pararetrovirus Cauliflower mosaic virus (CaMV) or members of the picorna-like nepovirus and comovirus [13–16], but were also observed with rod-shaped virus Current Opinion in Virology 2011, 1:403–409
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Figure 1
(a)
bunyaviridea, or the bacilliform rhabdovirus Pittosporum vein clearing virus has also been reported [21,22]. On the basis of these early observations, the concept emerged that cell-to-cell translocation of viruses through PD occurs in an encapsidated form, that is, as entire virions or nucleocapsids.
Cell 2 (b) ER
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Current Opinion in Virology
Modes of cell-to-cell spread of plant viruses. (a) A cartoon of a plasmodesma. The plasmodesma is seen as a plasma-membrane (PM)lined channel through the cell wall containing a central endoplasmic reticulum (ER)-derived rod-shaped desmotubule (DT). The location of actin filaments and PDLP in the symplastic channel and the PM components is illustrated. Callose (Cal) accumulates at the neck region of PD. (b) Model for PD modification by nontubule forming MP. In the presence of TMV MP, actin severing by MP and reduced accumulation of callose at the PD neck region lead to dilation of the PD pore. NPC consisting of viral RNA, MP and host factors can then move through PD by lateral diffusion along the desmotubule. (c) and (d) Model for PD modification by tubule forming MP. Assembly of tubule forming MP into tubules occurs upon interaction of the MP with PDLP and leads to the removal of the desmotubule inside PD. Virions may then be transported between cells through polar tubule assembly-driven and disassemblydriven treadmilling as indicated by the arrow (c). Alternatively, tubule may promote the passage of NPC consisting of vRNA and CP (d).
such as Tobacco mosaic virus (TMV) [17,18], Potato virus X (PVX), a potexvirus [19], Beet yellows virus (BYV), a closterovirus [20], and Potato virus Y (PVY), a potyvirus [18]. Although scarce, the presence in PD of enveloped viruses like Tomato spotted wilt virus (TSWV), a plant-adapted Current Opinion in Virology 2011, 1:403–409
The molecular characterization of virus translocation mechanisms through PD started with the groundbreaking discovery that TMV encodes a specific protein required for viral cell-to-cell movement, namely the 30K protein. This protein was given the name ‘movement protein’ or MP for its unique capacity to restore the cell-to-cell movement deficiency of TMV strains with mutated MP [23,24]. Thus, transgenic plants expressing the TMV 30K complement, in trans, mutated TMV strains lacking a functional MP [23,25]. Sensu stricto, MP defines virus-encoded proteins necessary for spreading viral infections, but which have little or no impact on replication in single cells. In TMV, the CP and MP are both optional for replication, but only the MP is needed for cell-to-cell movement [25]. It should be noted that the TMV replicase is also directly or indirectly involved in virus movement but cannot be considered as a bona fide MP, as it is required for viral replication and displays additional suppression of silencing activity [26–28]. It is now well established that TMV MP localizes to PD and increases the SEL without inducing obvious ultrastructural changes in PD architecture [29]. In addition, the 30K is able to bind, in a cooperative but sequence nonspecific manner, single stranded nucleic acids including fulllength TMV viral RNA (vRNA) [30,31]. Atomic force microscopy further revealed that the diameters of the MP–vRNA nucleoprotein complex are in the range of 1.5–3.5 nm [32,33], hence close to the dimensions of the dilated PD microchannels [7,29]. Consistent with these findings, the general consensus emerged that TMV traffics from cell-to-cell in the form of a nucleoprotein complex (NPC, Figure 1b).
The diversity of MP Nearly a quarter of a century after the characterization the TMV MP, it appears that most, and probably all plant viruses encode one or more MPs. Recognized MPs display considerable structural diversity and fall into at least four different phylogenetic groups, the largest and probably best characterized being the ‘30K’ superfamily named after its prototype member, the TMV 30K [34– 37]. The number of encoding genes per viral genome and size of MP is also highly variable. Thus, viruses with MP belonging to the 30K superfamily generally encode a single MP in the 30–40 kDa range [38], whereas the MP of tymovirus is nearly 70 kDa [39] and those of closterovirus only 6 kDa [40–42]. Cell-to-cell transport of carmovirus is aided by a set of two small virus-encoded polypeptides no larger than 12 kDa, referred to as the double gene block proteins (DGB) [43–45]. The family www.sciencedirect.com
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Potyviridae to which belong approximately 30% of known plant viruses, is thought to encode also two MPs, the cylindrical inclusion protein (CI) and the recently identified P3N-PIPO [46–50]. Finally, a complex of three MPs (7–25 kDa) is necessary for the movement of the triple gene block (TGB) group of viruses belonging to the Virgaviridae and Flexiviridae families that includes potexvirus and hordeivirus [51,52]. It should be noted that besides MP, structural proteins are often required for movement. An example of extreme involvement of structural proteins is provided by the closterovirus BYV in which four out of five proteins participating in the cell-tocell movement machinery are integral virion components [53]. It is now clear that during the course of plant virus evolution, a number of MPs evolved to allow the viral genome to cross the barrier of the host cell wall. This is in sharp contrast to animal viruses for which in the majority of cases proteins specifically dedicated to cell-to-cell movement have not been identified. An exception to this may be herpesviruses, which encode a heterodimer of glycoproteins (gE/gI), which are not required for cell-free viral entry but are essential for efficient cell-to-cell spread [54]. The role of this glycoprotein heterodimer appears to be to target the virus to intercellular basolateral junctions, allowing direct access to viral receptors on the opposing target cell membrane [55,56]. Other exceptions may include the few viruses that are able to replicate in both plants and animals. An excellent illustration of the unique adaptation of animal viruses to plants is provided by Tospovirus, the sole genus within the family Bunyaviridae with plant tropism [57]. In this virus, the nonstructural protein NSm produced by the ambisense M RNA is not encoded by any of the animal-infecting members of the Bunyaviridae. The NSm protein of TSWV possess typical features of plant MPs, including presence in cellular fractions enriched for cell walls and cytoplasmic membranes, intracellular localization close to PD and modification of PD structure via the formation of tubules (see below for more details), RNA binding properties and also interactions with a host trafficking protein [22,58–63]. Direct evidence for the function of TSWV NSm protein in virus movement was generated by complementation of a movement-deficient TMV vector by heterologous expression of NSm [60]. In sharp contrast to the vast diversity of MP, the present picture suggests the existence of only two main strategies for plant virus cell-to-cell movement, one in which the viral genome moves as intact virions and another where the viral nucleic acids are trafficked through PD in the form of a NPC (Figure 1). At the ultrastructural level, the two strategies are readily distinguishable. The former socalled tubule-guided mechanism is accompanied by profound modifications in PD architecture through the removal of the desmotubule and its replacement by www.sciencedirect.com
tubular structures containing viral particles or in some cases NPCs (Figure 1c,d). The second strategy applies to the majority of plant viruses including TMV and involves, at most only minor structural changes in PD architecture [64,65]. Viruses belonging to this group encode single or multiple MP generally with affinity for membranes, in particular for the ER that extends in PD to form the desmotubule. With the help of specific host factors that are still largely unknown, the movement of the NPC via PD is thought to occur by lateral movement along the membranes upon relaxation of the PD aperture. Recently, two such factors that facilitate TMV movement have been identified. Actin, which is suggested by a recent study shows that several viral MPs may sever actin filaments to relax the PD during their cell-to-cell movement [66], whereas ankyrin is thought to downregulate the deposition of callose [67]. Because of space limitation, the remaining part of this review will essentially focus on recent advance in our understanding of tubuleguided viral dissemination strategies. Extensive recent reviews on nontubule-guided movement have been published elsewhere [2,5,68,69].
Tubule-guided movement Tubule-guided mechanism applies to a whole set of plant viruses with RNA or DNA genomes sharing in common a single MP with tubule-forming capacity (for an extensive list of virus employing tubule-guided movement see Refs. [70,71]). This group typically includes viruses with icosahedral symmetry such as Cowpea mosaic virus (CPMV), Grapevine fanleaf virus (GFLV) or CaMV, but the situation of filamentous or enveloped virus is not always clearly defined. MPs with tubule-forming capacity have been classified in the 30K superfamily, although in groups that are phylogenetic distinct from nontubuleforming MP groups [36]. The ability of specific MP to form tubules was first observed with CPMV whose infection leads to the production of tubular structures containing a single row of virus-like particles extending from the entry of PD in one cell, into the cytoplasm of a neighboring cell. Early genetic and immunological studies revealed that the RNA2-encoded 48K protein is a structural component of the tubule and essential for cellto-cell movement of CPMV [72,73]. Further work showed that the 48K MP is the only viral protein needed for tubule formation and tubules produced upon ectopic expression of the MP are identical to those observed upon infection, except for the lack of virions in the tubule lumen [74–76]. Since then, the intrinsic property of MP to assemble into tubules in the absence of other viral proteins has been demonstrated not only with various icosahedral viruses even when fused to GFP [16,59,77– 83] but also with rod-shaped viruses [84,85]. A remarkable feature of these MP is their ability to assemble into tubules when expressed in protoplasts, hence in the absence of cell wall and consequently of PD. Amazingly, a number of these proteins, also maintain their capacity to Current Opinion in Virology 2011, 1:403–409
406 Virus replication in animals and plants
form tubules when expressed in insect cells [59,77,80,86]. Although the functionality of such tubules cannot easily be probed, they appear to be structurally similar to those produced in plants. However, the NSm protein of TSWV that forms tubule on the surface of insect cells (Spodoptera frugiperda) is unable to do so in infected thrips tissue, the vector of TSWV, raising the question of whether NSm has a function at all during the insect life cycle of TSWV [87]. This contrasts with the reoviridae Rice dwarf virus (RDV), a phytoreovirus that multiplies also in plants and in invertebrate insect vectors. Infection of cultured leafhopper cells with RDV leads to the formation of tubules along actin-based filopodia composed of the nonstructural viral protein Pns10 and containing viral particles. In cultured cells, Pns10 has the intrinsic ability to form tubules extending out of the cells in a manner involving the actomyosin and secretion system but not microtubules [88,89]. Electron tomography revealed that the Pns10 tubules are uniform in size with an inner diameter of 75 6 nm resulting in direct contact between the RDV particles and the inner surface of the tubule [90]. All this suggests that one of the ways RDV could spread among cells of its insect vector is through virus-induced tubular structures. Sensu stricto, tubule-guided movement refers the transport of virus particles in the inner channel formed by the MP assembled into tubules. Mechanistically, two possibility exist for this type of transport, the first whereby virions would be able to transit autonomously in the lumen of the tubules similarly to cars inside a tunnel and a second, related to treadmilling, in which virions would be incorporated simultaneously to the MP at one end of growing tubules and released at the other end upon removal of the MP and/or depolymerization of the tubule. The latter, more likely mechanism, implies direct or indirect interactions between the MP and the virion/CP, which has been demonstrated for several viruses including CPMV, CaMV and Alfalfa mosaic virus (AMV). In all these cases, interactions were triggered by small C-terminal domains of MPs dispensable for tubule formation but generally required for movement [91–94]. Additionally, the C-terminus of the CPMV MP was shown to be necessary for the incorporation of virus particles in the tubule, suggesting that it is located inside the tubular structure [95]. Probably the best evidence in favor of treadmilling comes from a CPMV MP point mutant able to form tubules containing virus particles, but unable to support cell-tocell movement. It is likely that this mutant with increased tubules stability interferes with viral spread by preventing breakdown or disassembly of tubules and thereby release of virions in neighboring cells [94]. It also strongly supports the notion that CPMV, a virus with an ssRNA genome, exclusively moves as encapsidated particles Current Opinion in Virology 2011, 1:403–409
via tubules. The same rule seems to apply likely to GFLV, a close relative of CPMV [16,96], and also CaMV, a virus with dsDNA genome and whose MP allows only the transport of virus particles in a heterologous system adapted from AMV [97]. Paradoxically, using the same AMV-derived experimental system [98], noncognate tubule-forming MP from different genera including comovirus, nepovirus, and caulimovirus supported the transport from cell-to-cell of RNA3 of AMV, but only on the condition that specific interactions between the various MPs and AMV CP were maintained [93,97]. Preservation of such interactions was achieved through the addition of the CP-binding domain of the AMV MP (44 C-terminal residues) to the different MP [93]. Importantly, these experiments were performed in the presence of a mutated AMV CP defective in virion assembly [98]. Under such circumstances where cell-to-cell movement occurs and tubules are synthesized but no virions are produced, one can only conclude that the various tubuleforming MP can mediate the transports of AMV RNA/CP complexes through tubules as depicted in Figure 1d. To date the molecular mechanism leading to the physical remodeling of the PD, in particular the displacement of the desmotubule, remains elusive. Perhaps a first step in this direction has recently been achieved through the identification of a family of host proteins, conserved throughout higher plants and located in the plasmamembrane lining the interior of PD that promote the spread of viruses employing tubule-guided movement but not of TMV [99]. These type I membrane proteins named PDLP [100] provide a receptor-like function for anchoring MP at PD [99]. It is possible that the specific interaction between PDLP and tubule forming MP at PD may nucleate tubule self-assembly that would then lead to the removal of the desmotubule (Figure 1c). A future challenge will be to identify novel host proteins with agonist function in virus movement and determine the atomic structure of the moving complexes in situ.
Acknowledgement CR is supported by the ANR the region Alsace and is a CNRS fellow.
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