Probing Plasmodesmal Transport With Plant Viruses

8/12/2019 Probing Plasmodesmal Transport With Plant Viruses

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Plant Physiol. (1993) 102: 1071-1076

Probing Plasmodesmal Transport wi th Plant VirusesVi ta ly Ci tovsky

Department of Biochemistry and Cell Biology, State

Plant intercellular connections, the plasmodesmata, effec-tively link individual cells into one symplastic continuum andfunction as conduits for transport and cell-to-cell communi-cation processes. Although plasmodesmal ultrastructure hasbeen extensively studied (see below), very little is knownabout the biochemistry, molecular biology, and regulation ofthese intercellular channels. This lack of knowledge stemsmainly from technical difficulties in isolation and purificationof plasmodesmata structures that are embedded in the plantcell-wall matrix. Thus, plasmodesmata remain essentially abiological black box. Recently, however, a potentially pow-erful approach with which to study plasmodesmal functionhas been developed. This approach is based on the generalobservation that complex biological pathways can be func-tionally dissected using specific biologically active com-pounds (e.g. inhibitors or inducers) or mutations that perturbthe pathway. In the case of plasmodesmata, a unique classof biological molecules is known to specifically and dramat-ically alter plasmodesmal function: the cell-to-cell movementproteins of plant viruses.

In this review, I focus on the use of plant virus cell-to-cellmovement proteins as molecular tools to study plasmodes-mata. For detailed descriptions of the role of movementproteins in cell-to-cell spread of plant viruses, the reader isreferred to recent comprehensive reviews (Atabekov andTaliansky, 1990; Citovsky and Zambryski, 1991; Hull, 1991;Maule, 1991; Deom et al., 1992; Citovsky and Zambryski,1993; McLean et al., 1993).

PL SMODESM TStructure

A simple plasmodesma is a pore that is lined with plasmamembranes of the connecting cells (Fig. 1A). The center ofthis pore is occupied by an appressed strand of ER connectedto the ER of the adjacent cells. In the center of the appressedER is a vertical row of globular proteinaceous particles (3 nmin diameter) associated with the inner leaflet of the appressedER membrane (Fig. 2). Most of the space between the plasmamembrane surface of the pore and the appressed ER is alsothought to be occluded by 3-nm protein particles. One layerof particles is embedded in the inner leaflet of the plasmamembrane; a second layer is embedded in the outer leafletof the appressed ER and is connected by filamentous struc-tures to protein particles in the central part of the appressedER structure (Fig. 2). The small (2.5 nm in diameter) space

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between the two layers of protein particles (Fig. 2) formsaqueous microchannels (usually 7-10 per single plasmo-desma) through which plasmodesmal transport occurs (Dinget al., 1992b). The function of these protein particles isunknown; possibly they regulate the size of permeable mi-crochannels by changing their positions within the plasmo-desmal pore (see below).

Structurally and developmentally, plasmodesmata can bedivided into two groups. (a) Single plasmodesmata are foundpredominantly in young immature tissue; they are thoughtto represent the primary plasmodesmata, i.e. the connectionsformed between cells during cell division (Fig. 1A). (b)Branched plasmodesmata consist of severa1 single plasmo-desmata interconnected by a central cavity (Fig. 1B). Theseplasmodesmata are found only in mature tissue and areconsidered to represent the secondary connections insertedinto the existing cell walls after cell division (Ding et al.,1992a). Both primary and secondary plasmodesmata exhibitsimilar size exclusion limits (Ding et al., 1992a), implying thatthese two types of connections are physiologically similar.Recently, however, a specific protein kinase activity wassuggested to associate with secondary but not primary plas-modesmata (Citovsky et al., 1993) (see below). This findingmay reflect differences in mechanisms by which these twoclasses of plasmodesmata are regulated.Permeability

In higher plants, permeability of plasmodesmata has beenextensively studied by microinjecting dyes of increasing mo-lecular mass. These studies defined the size exclusion limit ofplasmodesmal microchannels as 1.5 to 2 nm in diameter(800-1000 D) depending on the plant species (Terry andRobards, 1987; Wolf et al., 1989). Considering the physicaldimensions of plasmodesmal channels (2.5 nm as estimatedfrom electron micrographs [Ding et al., 1992b]), it appearsthat, for efficient transport, the transported molecule must besmaller than the actual diameter of the channel.

Control of plasmodesmal permeability is largely an unex-plored subject. Severa1 factors (eg. Ca2+and phosphoinosi-tides) have been shown to reduce plasmodesmal flow (Baron-Eppel et al., 1988; Tucker, 1988), but these regulatory factorsdo not specifically affect plasmodesmata, but instead act assecond messengers for many cellular processes. Although

Abbreviations: NBP, nuclear localization signal binding protein;NLS, nuclear localization signal; SSB, single-strand DNA bindingprotein; TMV, tobacco mosaic virus.


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1072 Citovsky Plant Physiol.Vol. 102 1993

Figure 1. Ultrastructure of primary single) A) and secondary branched) B)plasmodesm ata. Electron m icrographs ofplasmodesmata between tobacco m esophyl l cel ls magnif icat ion x131,500) are from Dinget al. 1992a) an d they wereprovided by B.Ding and W. Lucas Universi tyof California, Davis).ER , Cel lular endoplasmic ret iculum; aER, appressedER;C C, central cavi ty.

cell

cell2

permeablespace(closed)

filamentsprotein particles InInner leafletof ER

protein particles Inouter leafletof ERappressedER

proteinparticlesIn CrOSS-SCCtJOn (ClOSBd)Inner leafletofplasmamem brane ^ F S gS permeable space (open) m m~ mmplasmamem brane

cellular ER

longitudinal section cross-section(open)Figure2 . Schem atic struc ture of a simple plasmo desm a. Diagrams oflongitudinalviewand of transverseviewof a closedplasmodesmaare adapted fromDinget al . 199 2b). Amodel for plasmodesmalopening transverseview) is explained inthe text.


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Probing Plasmodesmal Transport with Plant Viruses 1 73

these secondary messengers can decrease plasmodesmalpermeability, no known plant factors increase the permeabil-ity. Still, recent evidence suggests that the plasmodesmal sizeexclusion limit can increase significantly to allow transport ofproteins and even larger nucleic acid molecules. For example,cellular proteins appear to be transported through the plas-modesmata linking companion and sieve cells in the vascularbundle (Fisher et al., 1992). A striking example of plasmo-desmal expansion is transport of plant virus nucleic acidsfrom infected into healthy adjacent cells, a process causednot by plant proteins but by viral proteins (Wolf et al., 1989;Derrick et al., 1992).

Specifically, the virus-encoded movement proteins mediatecell-to-cell spread of plant viruses through plasmodesmata(reviewed by Atabekov and Taliansky, 1990; Citovsky andZambryski, 1991; Hull, 1991; Maule, 1991; Deom et a]., 1992;Citovsky and Zambryski, 1993; McLean et al., 1993). Al-though these proteins originally were studied in the contextof plant virus pathology and plant protection, they are nowreceiving attention as molecular tools to probe plasmodesmaltransport.

PROTEIN MACHINERY OF PLASMODESMALTRANSPORMovement Proteins

Movement proteins specifically alter plasmodesmal func-tion and thus can be used to characterize transport pathwaysthrough plasmodesmata. A11 cell-to-cell movement proteinsknown to date are virus encoded. Evolutionary studies sug-gest that invading viruses insinuate into the existing cellularprocesses and adapt them for their own life cycle. It ispossible, then, that viral movement proteins are functionallyanalogous to unidentified plant cellular proteins that mediatetransport of macromolecules through plasmodesmata. In-deed, recent amino acid sequence analyses indicate that mostviral cell-to-cell movement proteins appear to have evolvedfrom a single ancestor (Melcher, 1990), possibly a capturedcellular protein (Koonin et al., 1991). Thus, study of viralmovement proteins may directly reflect mechanisms of plas-modesmal transport in normal, uninfected plants rather thana plant virus-specific phenomenon.

One of the best-studied cell-to-cell movement proteins isthe P30 protein of TMV. Two lines of evidence implicate P30in cell-to-cell movement of TMV: (a) P30 mutations specifi-cally restrict the cell-to-cell spread of TMV (Jockusch, 1968;Peters and Murphy, 1975; Nishiguchi et al., 1978; Meshi etal., 1987); and (b) P30 expressed in transgenic plants restorescell-to-cell spread of movement-deficient TMV strains (Deomet al., 1987). How does P30 mediate plasmodesmal transport?Recent evidence suggests that P30 (as well as movementproteins of many other plant viruses [Citovsky et al., 1991;Osman et al., 1992; Schoumacher et al., 19921) may associatewith the transported viral nucleic acid molecule and functionas its molecular chaperone during transport (Citovsky et al.,1990; Citovsky and Zambryski, 1991). P30 is a single-strandnucleic acid binding protein with two independently activebinding domains at its carboxyl terminus (Citovsky et al.,1992a). Similar to a11 known SSBs (Chase and Williams,

1986), P30 binding to single-strand nucleic acids is coopera-tive and sequence nonspecific; unlike most SSBs, however,P30 binds single-strand DNA and RNA with equal affinity(Citovsky et al., 1990).

Cooperative binding of P30 to TMV RNA was proposed tounfold the nucleic acid and convert it into a form that canpenetrate through plasmodesmal microchannels (Fig. 3) (Ci-tovsky et al., 1990). Typically, free single-strand nucleic acidsexist as bulky and collapsed structures (Citovsky et al., 1989,1992a); for example, calculations indicate that free-foldedTMV genomic RNA molecule has an average diameter of 10nm (Gibbs, 1976). EM observations demonstrated that bind-ing of P30 to single-strand nucleic acid molecules producesapproximately 2-nm-wide unfolded P30-RNA and P30-single-strand DNA complexes (Citovsky et al., 1992a). Asdiscussed below, the dimensions of P30-nucleic acid com-plexes 2 nm) are compatible with the size of plasmodesmatafound in plants transgenic for or microinjected with P30(Wolf et al., 1989; E. Waigmann, W. Lucas, V. Citovsky, P.Zambryski, unpublished data) and , by implication, modifiedduring viral infection. Along with unfolding the transportednucleic acid molecule, P30 binding may protect it from cel-lular nucleases. Indeed, SSB binding is known to preventnucleic acid degradation by extemally added exo- and en-donucleases (Citovsky et al., 1989).

Although P30 is the only viral protein required for cell-to-cell spread of TMV, it may interact with at least two cellularprotein components of the transport pathway. First, P30potentially interacts with plant cell cytoplasmic receptors thatmay shuttle the movement complex from the site of itsassembly in the cytoplasm to plasmodesmata (Fig. 3). Thepresence of these receptors, however, has not been proven.Second, P30 likely interacts with plasmodesmal componentsto increase permeability and promote transport (Fig. 3).Putative Cytoplasmic Receptors

Because P3O-nucleic acid movement complexes are pre-sumably formed in the cell cytoplasm where TMV RNA isreplicated and translated (reviewed by Palikaitis and Zaitlin,1986), cell-to-cell movement of the newly formed complexesrequires that they first trave1 to plasmodesmal orifices. Howdoes this cytoplasm-to-plasmodesmata transfer of protein-nucleic acid complexes occur? Much of our knowledge ofnucleic acid transport through membrane channels derivesfrom studies of nuclear export and import. Although plas-modesmata and nuclear pores are obviously structurally dif -ferent, both are the only known complex proteinaceous poresinvolved in active bidirectional traffic of macromolecules(Robards and Lucas, 1990; Forbes, 1992; Citovsky and Zam-bryski, 1993). Furthermore, transport of viral nucleic acidsthrough plasmodesmata (Citovsky et al., 1992a), as well asnuclear transport of grobacterium T-DNA (Citovsky et al.,1989, 1992b) and pre-mRNAs (Mehlin et al., 1992), presum-ably involves unfolded nucleic acid-protein complexes. Thus,it is possible that nucleic acid transport through plasmodes-mata may functionally resemble nuclear import.

Nuclear import initiates in the cytoplasm with binding ofNLSs to specific cytoplasmic receptors, the NBPs, which thendirect the transported molecule to the nuclear pore (reviewed


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1074 C itovsky Plant Physiol. Vol. 102, 1993

TRANSLOCATIONMOVEMENTPROTEIN

BINDING MTENDED TARGETING INCREASEINoPLASMODESMATA F IASIKIDESMALPERMEABILITYUNFOLDINGFOLDEDNUCLEICACID CYMPLASMICSHVITLE RECEFTORS ?)INACTIVATION OFMOVEM ENT PROTEINBY A PLANT CELLwALLAssocIAmPROTEIN KINASE (?)

Figure 3. Plant virus cell-to-cell movement protein chaperons a single-strand nucleic acid molecule through plasmodesmalchannel.This is a model for P30-mediated cell-to-cell spread of TMV RNA (adapted from Citovskyand Zambryski, 1993).

by Nigg et al., 1991; Forbes, 1992). By analogy, specificcytoplasmic receptors may also be involved in plasmodesmaltransport; these receptors would bind and transport P30-TMV RNA complexes to plasmodesmata. Currently, severa1laboratories are searching for the putative cytoplasmic recep-tors that bind plant virus movement proteins.Movement Protein-Plasmodesmata lnteractionP30-lnduced lncrease n Plasmodesmal Permeability

Experiments show that P30 (and movement proteins ofother plant viruses) interact with plasmodesmata to increasetheir size exclusion limit (Wolf et al., 1989; Derrick et al.,1992; E. Waigmann, W. Lucas, V. Citovsky, P. Zambryski,unpublished data). Originally, this increase in plasmodesmalpermeability was assessed by microinjection of fluorescentlylabeled dextrans of increasing molecular mass into leaf me-sophyll cells of transgenic tobacco plants that constitutivelyexpress P30 (Wolf et al., 1989). This study showed that theplasmodesmal size exclusion limit in these transgenic plantsis higher (5-6 nm) than that in wild-type tobacco plants (1.5nm). In a different system, microinjection of tobacco rattlevirus into leaf trichomes also caused an increase in plasmo-desmal permeability (Derrick et al., 1992).

Recently, P30 interaction with plasmodesmata was furtherexamined by co-injection of purified P30 and fluorescentdextrans into leaf mesophyll of wild-type tobacco plants E.Waigmann, W. Lucas, V. Citovsky, P. Zambryski, unpub-lished data). Microinjected P30 increased plasmodesmalpermeability to 6 to 9 nm, higher than that observed in P30transgenic plants (5-6 nm). More importantly, the large flu-orescent dextrans appeared as far as 10 to 20 cells away fromthe site of injection E. Waigmann, W. Lucas, V. Citovsky, P.Zambryski, unpublished data). This result has two potentialexplanations. (a) Microinjected P30 itself may move betweencells to affect plasmodesmal permeability in noninjected cells.(b) Alternatively, microinjected P30 may trigger a putativeintercellular signal transduction pathway that increases theplasmodesmal size exclusion limit in numerous interconnect-ing cells.

The mechanism by which P30 increases plasmodesmalpermeability is unknown. Previous models proposed asym-metrical redistribution of plasmodesmal protein particles Lu-t s et al., 1990; Deom et al., 1992) and/or change in their

shape (Robards and Lucas, 1990). Recent observations sug-gest a third possibility. Filaments were shown to connectplasmodesmal protein particles of the outer leaflet of theappressed ER to the particles in the center of the ER (Fig. 2)(Ding et al., 1992b). It is tempting to speculate that theseprotein particles can slide in and out of the membrane toincrease or decrease the size of the permeable microchannelbetween the particles (Fig. 2); this movement may be modu-lated by the filamentous structures attached to the particles.

The P3O-induced increase in the size of plasmodesmalchannels (5-9 nm). (Wolf et al., 1989; E. Waigmann, W.Lucas, V. Citovsky, P Zambryski, unpublished data) i.; con-sistent with transport of 2-nm-wide P30-nucleic acid com-plexes (Citovsky et al., 1992a). Thus, these data support thecurrent view that P3O-induced modification of plasmodes-mata is a prerequisite for virus movement. However, theincrease in plasmodesmal permeability as revealed by cell-to-cell movement of fluorescent dextrans may be only partof the story. As mentioned, transport through the nuclearpore may be functionally similar to transport through plas-modesmata. Early experiments measuring diffusion of mi-croinjected dextrans determined the size exclusion lirnit ofthe nuclear pore as 40 kD (Paine, 1988). Recent studies,however, suggest that even smaller endogenous nuclear pro-teins, such as 21-kD H1 histones, do not diffuse throug;h thenuclear pore but are imported by an active NLS-dependentmechanism (Breeuwer and Goldfarb, 1990). By this analogy,endogenous macromolecules (as opposed to microinjecteddextrans) may not diffuse through the enlarged plasrriodes-mata. Instead, cell-to-cell transport is an active process me-diated by specific plasmodesma localization signals.P30 Phosphorylation by a Cell Wall-AssociatedProtein Kinase

Because plasmodesmal transport of P30-TMV RNA com-plexes probably involves an increase in the size exclusionlimit of plasmodesmata, P30 most likely interacts withl plas-modesmal components. Although interaction of P301 withspecific plasmodesmal proteins has not yet been proven, acell wall-associated protein kinase from tobacco, a po lentialplasmodesmal component, directly interacts with P30. ThisSer/Thr-specific protein kinase phosphorylates P30 at itscarboxyl terminal Ser258, hrZ6',and Ser265esidues. In terest-ingly, these P30 phosphorylation sites do not correspond to


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Probing Plasmodesmal Transport with Plant Viruses 1 75

any known consensus phosphorylation sites for proteinkinases (Citovsky et al., 1993).

The cell wall-associated protein kinase activity is organspecific, is present mainly in leaves but only marginally instems, and is absent in roots and apical buds. In addition,this enzymic activity is developmentally expressed, closelyparalleling basipetal (tip-to-base) leaf maturation (Citovskyet al., 1993). This basipetal pattem of development also hasbeen described for formation of secondary (branched) plas-modesmata in tobacco leaves (Ding et al., 1992b). Becausethe protein kinase activity correlates with secondary plas-modesmata development, this cell wall-associated proteinkinase may represent a functional component of secondaryplasmodesmata. Possible association of the protein kinaseactivity with secondary plasmodesmata is further supportedby the recent observation that P30, a substrate for this cellwall-associated protein kinase (Citovsky et al., 1993), isspecifically and irreversibly accumulated in secondary plas-modesmata in P30 transgenic plants (Ding et al., 1992a).Potentially, P30 phosphorylation is involved in its specificdeposition in secondary plasmodesmata.

What biological role, then, does P30 phosphorylation havefor the virus and/or for the host plant? To address thisquestion, one should consider the adverse effects of P30 onthe physiology of the host plant. For example, the P30-induced increase in plasmodesmal permeability may alterintercellular communication, an important biological process.Thus, inactivation or attenuation of P30 activity may becritical for survivalof the host plant and, in turn, of the virus;to this end, phosphorylation may function to deactivate P30by sequestering it to plant cell walls (Fig. 3). The followingobservations support this hypothesis. (a) Young apical leaveslack the protein kinase activity responsible for P30 phos-phorylation (Citovsky et al., 1993). In P30 transgenic plants,these young leaves were found to accumulate P30 in thesoluble fraction (Deom et al., 1990). (b) In contrast, matureleaves with the highest levels of P30 phosphorylation (Citov-sky et al., 1993) efficiently accumulate P30 in their cell walls(Deom et al., 1990). (c) In wild-type plants, young apicalleaves, potentially unable to sequester P30 by phosphoryla-tion, are more susceptible to virus infection (reviewed byCulver et al., 1991). Thus, the confinement of P30 to second-ary plasmodesmata may be mediated by a protein kinase thatspecifically associates with these intercellular connections.

LOOKINC A H E A DOver the next few years, the use of plant virus movement

proteins will hopefully enrich our knowledge of plasmodes-mal transport. As research continues, cellular proteins poten-tially involved in this transport pathway will be identifiedand characterized. The elucidation of the cell-to-cell transportmechanisms will allow us to address many critical questionsin plant biology. For example, analogous to animal systems,changes in plasmodesmal transport may create compartmentsin which cells communicate with each other but not withcells from other compartments within the same tissue; suchcommunication compartments may function during plant

development and morphogenesis. On the applied level,knowledge of plasmodesmal transport may lead to nove1

approaches for production of agronomically important virus-resistant plants. Thus, the multifaceted attack now in progresson the structure of plasmodesmata and plasmodesmal trans-port pathways will provide new and exciting answers for thequestion of how plant cells communicate with each other.

ACKNOWLEDCMENTSI thank Patricia Zambryski, my friend and mentor, for her contin-

u o u ~ elp and support. I am grateful to Bill Lucas, Gail McLean,Elisabeth Waigmann, Patricia Zambryski, and John Zupan for criticalreading of the manuscript. I am especially indebted to Gail McLeanfor a11 her patience and help. I also thank Bill Lucas and Biao Dingfor micrographs of plasmodesmata.

Received April 27, 1993; accepted May 4, 1993.Copyright Clearance Center: 0032-0889/93/102/1071/06

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movement locus of CaMV, encodes an RNA binding protein. ProcNatl Acad Sci USA 88: 2476-2480Citovsky V, McLean BG, Zupan J Zambryski P (1993) Phosphoryl-ation of tobacco mosaic virus cell-to-cell movement protein bya developmentally-regulated plant cell wall-associated proteinkinase. Genes Dev 7: 904-910Citovsky V, Wong ML, Sha w A, Prasad BVV, Zamb ryski P (1992a)Visualization and characterization of tobacco mosaic virus move-ment protein binding to single-stranded nucleic acids. Plant CellCitovsky V, Wong ML, Zambryski P (1989) Cooperative interactionof grobacterium VirE2 protein with single stranded DNA: impli-cations for the T-DNA transfer process. Proc Natl Acad Sci USACitovsky V, Zambryski P (1991) How do plant virus nucleic acidsmove through intercellular connections? BioEssays 1 3 373-379Citovsky V, Zambryski P (1993) Transport of nucleic acids through

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