Many plant virus genera encode a ‘triple gene block’ (TGB), a specialized evolutionarily conserved gene module involved in the cell-to-cell and long-distance movement of viruses. The TGB-based transport system exploits the co-ordinated action of three polypeptides to deliver viral genomes to plasmodesmata and to accomplish virus entry into neighbouring cells. Although data obtained on both the TGB and well-studied single protein transport systems clearly demonstrate that plant viruses employ host cell pathways for intra- and intercellular trafficking of genomic nucleic acids and proteins, there is no integral picture of the details of molecular events during TGB-mediated virus movement. Undoubtedly, understanding the molecular basis of the concerted action of TGB-encoded proteins in transporting viral genomes from cell to cell should provide new insights into the general principles of movement protein function. This review describes the structure, phylogeny and expression of TGB proteins, their roles in virus cell-to-cell movement and potential influence on host antiviral defences.
AgranovskyA. A.,
MorozovS. Yu.1999; Gene expression in positive strand RNA viruses: conventional and aberrant strategies. In Molecular Biology of Plant Viruses pp 99–119 Edited by
MandaharC. L.
Boston/Dordrecht/London: Kluwer;
AgranovskyA. A.,
BoykoV. P.,
KarasevA. V.,
KooninE. V.,
DoljaV. V.1991; Putative 65 kDa protein of beet yellows closterovirus is a homologue of HSP70 heat shock proteins. J Mol Biol 217:603–610
AgranovskyA. A.,
FolimonovaS. Yu.,
FolimonovA. S.,
DenisenkoO. N.,
ZinovkinR. A.1997; The beet yellows closterovirus p65 homologue of HSP70 chaperones has ATPase activity associated with its conserved N-terminal domain but does not interact with unfolded protein chains. J Gen Virol 78:535–542
AgranovskyA. A.,
FolimonovA. S.,
FolimonovaS. Yu.,
MorozovS. Yu.,
SchiemannJ.,
LesemannD.,
AtabekovJ. G.1998; Beet yellows closterovirus HSP70-like protein mediates the cell-to-cell movement of a potexvirus transport-deficient mutant and a hordeivirus-based chimeric virus. J Gen Virol 79:889–895
AllisonA. V.,
ShallaT. A.1974; The ultrastructure of local lesions induced by potato virus X: a sequence of cytological events in the course of infection. Phytopathology 64:784–793
AlzhanovaD. V.,
HagiwaraY.,
PeremyslovV. V.,
DoljaV. V.2000; Genetic analysis of the cell-to-cell movement of beet yellows closterovirus. Virology 268:192–200
AlzhanovaD. V.,
NapuliA. J.,
CreamerR.,
DoljaV. V.2001; Cell-to-cell movement and assembly of a plant closterovirus: roles for the capsid proteins and Hsp70 homolog. EMBO J 20:6997–7007
AngellS. M.,
DaviesC.,
BaulcombeD. C.1996; Cell-to-cell movement of potato virus X is associated with a change in the size-exclusion limit of plasmodesmata in trichome cells of Nicotiana clevelandii
. Virology 216:197–201
AokiK.,
KraglerF.,
Xoconostle-CázaresB.,
LucasW. J.2002; A subclass of plant heat shock cognate 70 chaperones carries a motif that facilitates trafficking through plasmodesmata. Proc Natl Acad Sci U S A 99:16342–16347
AtabekovJ. G.,
RodionovaN. P.,
KarpovaO. V.,
KozlovskyS. V.,
PoljakovV. Y.2000; The movement protein-triggered in situ conversion of potato virus X virion RNA from a nontranslatable into a translatable form. Virology 271:259–263
BeckD. L.,
GuilfordP. J.,
VootD. M.,
AndersenM. T.,
ForsterR. L.1991; Triple gene block proteins of white clover mosaic potexvirus are required for transport. Virology 183:695–702
BeckD. L.,
Van DolleweerdC. J.,
LoughT. J.,
BalmoriE.,
VootD. M.,
AndersenM. T.,
O'BrienI. E.,
ForsterR. L.1994; Disruption of virus movement confers broad-spectrum resistance against systemic infection by plant viruses with a triple gene block. Proc Natl Acad Sci U S A 91:10310–10314
Bleykasten-GrosshansC.,
GuilleyH.,
BouzoubaaS.,
RichardsK. E.,
JonardG.1997; Independent expression of the first two triple gene block proteins of beet necrotic yellow vein virus complements virus defective in the corresponding gene but expression of the third protein inhibits viral cell-to-cell movement. Mol Plant–Microbe Interact 10:240–246
BrakkeM. K.,
BallE. M.,
LangenbergW. G.1988; A non-capsid protein associated with unencapsidated virus RNA in barley infected with barley stripe mosaic virus. J Gen Virol 69:481–491
BrandizziF.,
SnappE. L.,
RobertsA. G.,
Lippincott-SchwartzJ.,
HawesC.2002b; Membrane protein transport between the endoplasmic reticulum and the Golgi in tobacco leaves is energy dependent but cytoskeleton independent: evidence from selective photobleaching. Plant Cell 14:1293–1309
BucherG. L.,
TarinaC.,
HeinleinM.,
Di SerioF.,
MeinsF.Jr,
IglesiasV. A.2001; Local expression of enzymatically active class I β -1,3-glucanase enhances symptoms of TMV infection in tobacco. Plant J 28:361–369
CarringtonJ. C.,
JensenP. E.,
SchaadM. C.1998; Genetic evidence for an essential role for potyvirus CI protein in cell-to-cell movement. Plant J 14:393–400
ChapmanS.,
HillsG.,
WattsJ.,
BaulcombeD.1992; Mutational analysis of the coat protein gene of potato virus X: effects on virion morphology and viral pathogenicity. Virology 191:223–230
ChengW.,
BrendzaK. M.,
GaussG. H.,
KorolevS.,
WaksmanG.,
LohmanT. M.2002; The 2B domain of the Escherichia coli Rep protein is not required for DNA helicase activity. Proc Natl Acad Sci U S A 99:16006–16011
CrawfordK. M.,
ZambryskiP. C.2000; Subcellular localization determines the availability of non-targeted proteins to plasmodesmatal transport. Curr Biol 10:1032–1040
CrawfordK. M.,
ZambryskiP. C.2001; Non-targeted and targeted protein movement through plasmodesmata in leaves in different developmental and physiological states. Plant Physiol 125:1802–1812
DonaldR. G. K.,
PettyI. T. D.,
ZhouH.,
JacksonA. O.1995; Properties of genes influencing barley stripe mosaic virus movement phenotypes. In Fifth International Symposium on Biotechnology and Plant Protection: Viral Pathogenesis and Disease Resistance pp 135–147 Singapore: World Scientific;
DonaldR. G.,
LawrenceD. M.,
JacksonA. O.1997; The barley stripe mosaic virus 58-kilodalton β b protein is a multifunctional RNA binding protein. J Virol 71:1538–1546
DuM. X.,
JohnsonR. B.,
SunX. L.,
StaschkeK. A.,
ColacinoJ.,
WangQ. M.2002; Comparative characterization of two DEAD-box RNA helicases in superfamily II: human translation-initiation factor 4A and hepatitis C virus non-structural protein 3 (NS3) helicase. Biochem J 363:147–155
DunoyerP.,
PfefferS.,
FritschC.,
HemmerO.,
VoinnetO.,
RichardsK. E.2002a; Identification, subcellular localization and some properties of a cysteine-rich suppressor of gene silencing encoded by peanut clump virus. Plant J 29:555–567
ErhardtM.,
HerzogE.,
LauberE.,
FritschC.,
GuilleyH.,
JonardG.,
RichardsK.,
BouzoubaaS.1999a; Transgenic plants expressing the TGB1 protein of peanut clump virus complement movement of TGB1-defective peanut clump virus but not of TGB1-defective beet necrotic yellow vein virus. Plant Cell Rep 18:614–619
ErhardtM.,
Stussi-GaraudC.,
GuilleyH.,
RichardsK. E.,
JonardG.,
BouzoubaaS.1999b; The first triple gene block protein of peanut clump virus localizes to the plasmodesmata during virus infection. Virology 264:220–229
ErhardtM.,
MorantM.,
RitzenthalerC.,
Stussi-GaraudC.,
GuilleyH.,
RichardsK. E.,
JonardG.,
BouzoubaaS.,
GilmerD.2000; P42 movement protein of beet necrotic yellow vein virus is targeted by the movement proteins p13 and p15 to punctate bodies associated with plasmodesmata. Mol Plant–Microbe Interact 13:520–528
ForsterR. L.,
BevanM. W.,
HarbisonS. A.,
GardnerR. C.1988; The complete nucleotide sequence of the potexvirus white clover mosaic virus. Nucleic Acids Res 16:291–303
ForsterR. L.,
BeckD. L.,
GuilfordP. J.,
VootD. M.,
Van DolleweerdC. J.,
AndersenM. T.1992; The coat protein of white clover mosaic potexvirus has a role in facilitating cell-to-cell transport in plants. Virology 191:480–484
FosterT. M.,
LoughT. J.,
EmersonS. J.,
LeeR. H.,
BowmanJ. L.,
ForsterR. L. S.,
LucasW. J.2002; A surveillance system regulates selective entry of RNA into the shoot apex. Plant Cell 14:1497–1508
FridborgI.,
GraingerJ.,
PageA.,
ColemanM.,
FindlayK.,
AngellS.2003; TIP, a novel host factor linking callose degradation with the cell-to-cell movement of Potato virus X
. Mol Plant–Microbe Interact 16:132–140
GafvelinG.,
SakaguchiM.,
AnderssonH.,
von HeijneG.1997; Topological rules for membrane protein assembly for eukaryotic cells. J Biol Chem 272:6119–6127
GhoshroyS.,
LarteyR.,
ShengJ.,
CitovskyV.1997; Transport of proteins and nucleic acids through plasmodesmata. Annu Rev Plant Physiol Plant Mol Biol 48:27–49
GorbalenyaA. E.,
KooninE. V.,
DonchenkoA. P.,
BlinovV. M.1989; Two related superfamilies of putative helicases involved in replication, recombination, repair and expression of DNA and RNA genomes. Nucleic Acids Res 17:4713–4730
GorshkovaE. N.,
ErokhinaT. N.,
StroganovaT. A.,
YelinaN. E.,
ZamyatninA. A.Jr,
KalininaN. O.,
SchiemannJ.,
SolovyevA. G.,
MorozovS. Yu.2003; Immunodetection and fluorescent microscopy of transgenically expressed hordeivirus TGBp3 movement protein reveals its association with endoplasmic reticulum elements in close proximity to plasmodesmata. J Gen Virol 84:985–994
HefferonK. L.,
DoyleS.,
AbouhaidarM. G.1997; Immunological detection of the 8K protein of potato virus X (PVX) in cell walls of PVX-infected tobacco and transgenic potato. Arch Virol 142:425–433
HerzogE.,
HemmerO.,
HauserS.,
MeyerG.,
BouzoubaaS.,
FritschC.1998; Identification of genes involved in replication and movement of peanut clump virus. Virology 248:312–322
HuismanM. J.,
LinthorstH. J.,
BolJ. F.,
CornelissenJ. C.1988; The complete nucleotide sequence of potato virus X and its homologies at the amino acid level with various plus-stranded RNA viruses. J Gen Virol 69:1789–1798
IglesiasV. A.,
MeinsF.Jr2000; Movement of plant viruses is delayed in a β -1,3-glucanase-deficient mutant showing a reduced plasmodesmatal size exclusion limit and enhanced callose deposition. Plant J 21:157–166
JuutiJ. T.,
BamfordD. H.,
TumaR.,
ThomasG. J.Jr1998; Structure and NTPase activity of the RNA-translocating protein (P4) of bacteriophage ϕ 6. J Mol Biol 279:347–359
KalininaN. O.,
FedorkinO. N.,
SamuilovaO. V.,
MaissE.,
KorpelaT.,
MorozovS. Yu.,
AtabekovJ. G.1996; Expression and biochemical analyses of the recombinant potato virus X 25K movement protein. FEBS Lett 397:75–78
KalininaN. O.,
SamuilovaO. V.,
FedorkinO. N.,
ZeleninaD. A.,
MorozovS. Yu.1998; Biochemical characterization and subcellular localization of a 25K transport protein of potato virus X. Molekulyarnaya Biologiya (Moscow) 32:569–573 (in Russian
KalininaN. O.,
RakitinaD. A.,
YelinaN. E.9 other authors2001; RNA-binding properties of the 63 kDa protein encoded by the triple gene block of poa semilatent hordeivirus. J Gen Virol 82:2569–2578
KalininaN. O.,
RakitinaD. V.,
SolovyevA. G.,
SchiemannJ.,
MorozovS. Yu.2002; RNA helicase activity of the plant virus movement proteins encoded by the first gene of the triple gene block. Virology 296:321–329
KarpovaO. V.,
KozlovskyS. V.,
ArkhipenkoM. V.,
RodionovaN. P.,
AtabekovJ. G.1999; Complexes of tobacco mosaic virus RNA with a hordeivirus movement protein are infectious in plants susceptible to both viruses. Doklady RAN (Moscow) 368:406–409 (in Russian
KobayashiK.,
CabralS.,
CalamanteG.,
MaldonadoS.,
MentaberryA.2001; Transgenic tobacco plants expressing the potato virus X open reading frame 3 gene develop specific resistance and necrotic ring symptoms after infection with the homologous virus. Mol Plant–Microbe Interact 14:1274–1285
KoenigR.,
PleijC. W.,
BeierC.,
CommandeurU.1998; Genome properties of beet virus Q, a new furo-like virus from sugarbeet, determined from unpurified virus. J Gen Virol 79:2027–2036
KotlizkyG.,
BoultonM. I.,
PitaksutheepongC.,
DaviesJ. W.,
EpelB. L.2000; Intracellular and intercellular movement of maize streak geminivirus V1 and V2 proteins transiently expressed as green fluorescent protein fusions. Virology 274:32–38
KraglerF.,
MonzerJ.,
ShashK.,
Xoconostle-CazaresB.,
LucasW. J.1998; Cell-to-cell transport of proteins: requirement for unfolding and characterization of binding to a putative plasmodesmal receptor. Plant J 15:367–381
KrishnamurthyK.,
MitraR.,
PaytonM. E.,
Verchot-LubiczJ.2002; Cell-to-cell movement of the PVX 12K, 8K, or coat proteins may depend on the host, leaf developmental stage, and the PVX 25K protein. Virology 300:269–281
LauberE.,
Bleykasten-GrosshansC.,
ErhardtM.,
BouzoubaaS.,
JonardG.,
RichardsK. E.,
GuilleyH.1998; Cell-to-cell movement of beet necrotic yellow vein virus. I. Heterologous complementation experiments provide evidence for specific interactions among the triple gene block proteins. Mol Plant–Microbe Interact 11:618–625
LauberE.,
JanssensL.,
WeyensG.,
JonardG.,
RichardsK. E.,
LefebvreM.,
GuilleyH.2001; Rapid screening for dominant negative mutations in the beet necrotic yellow vein virus triple gene block proteins P13 and P15 using a viral replicon. Transgenic Res 10:293–302
LawrenceD. M.,
JacksonA. O.2001b; Requirements for cell-to-cell movement of barley stripe mosaic virus in monocot and dicot hosts. Mol Plant Pathol 2:65–75
LeeJ.-Y.,
YooB.-C.,
RojasM. R.,
Gomez-OspinaN.,
StaehelinL. A.,
LucasW. J.2003; Selective trafficking of non-cell-autonomous proteins mediated by NtNCAPP1. Science 299:392–396
LeisnerS. M.1999; Molecular basis of virus transport in plants. In Molecular Biology of Plant Viruses pp 161–182 Edited by
MandaharC. L.
Boston/Dordrecht/London: Kluwer;
LeonardD. A.,
ZaitlinM.1982; A temperature-sensitive strain of tobacco mosaic virus defective in cell-to-cell movement generate an altered virus-coded protein. Virology 117:416–424
LiouD.-Y.,
HsuY.-H.,
WungC.-H.,
WangW.-H.,
LinN.-S.,
ChangB.-Y.2000; Functional analyses and identification of two arginine residues essential to the ATP-utilizing activity of the triple gene block protein 1 of bamboo mosaic potexvirus. Virology 277:336–344
LoughT. J.,
ShashK.,
Xoconostle-CazaresB.,
HofstraK. R.,
BeckD. L.,
BalmoriE.,
ForsterR. L.,
LucasW. J.1998; Molecular dissection of the mechanism by which potexvirus triple gene block proteins mediate cell-to-cell transport of infectious RNA. Mol Plant–Microbe Interact 11:801–814
LoughT. J.,
NetzlerN. E.,
EmersonS. J.,
SutherlandP.,
CarrF.,
BeckD. L.,
LucasW. J.,
ForsterR. L.2000; Cell-to-cell movement of potexviruses: evidence for a ribonucleic protein complex involving the coat protein and first triple gene block protein. Mol Plant–Microbe Interact 13:962–974
LoughT. J.,
EmersonS. J.,
LucasW. J.,
ForsterR. L.2001; Trans-complementation of long-distance movement of white clover mosaic virus triple gene block (TGB) mutants: phloem-associated movement of TGBp1. Virology 288:18–28
MalcuitI.,
MaranoM. R.,
KavanaghT. A.,
De JongW.,
ForsythA.,
BaulcombeD. C.1999; The 25-kDa movement protein of PVX elicits Nb -mediated hypersensitive cell death in potato. Mol Plant–Microbe Interact 12:536–543
MarcosJ. F.,
VilarM.,
Perez-PayaE.,
PallasV.1999; In vivo detection, RNA-binding properties and characterization of the RNA-binding domain of the p7 putative movement protein from carnation mottle carmovirus (CarMV). Virology 255:354–365
McGeachyK. D.,
BarkerH.2000; Potato mop-top virus RNA can move long distance in the absence of coat protein: evidence from resistant, transgenic plants. Mol Plant–Microbe Interact 13:125–128
MitsuhashiN.,
HayashiY.,
KoumotoY.,
ShimadaT.,
Fukasawa-AkadaT.,
NishimuraM.,
Hara-NishimuraI.2001; A novel membrane protein that is transported to protein storage vacuoles via precursor-accumulating vesicles. Plant Cell 13:2361–2372
MorozovS. Yu.,
SolovyevA. G.1999; Genome organization in RNA viruses. In Molecular Biology of Plant Viruses pp 47–98 Edited by
MandaharC. L.
Boston/Dordrecht/London: Kluwer;
MorozovS. Yu.,
LukashevaL. I.,
ChernovB. K.,
SkryabinK. G.,
AtabekovJ. G.1987; Nucleotide sequence of the open reading frames adjacent to the coat protein cistron in potato virus X genome. FEBS Lett 213:438–442
MorozovS. Yu.,
MiroshnichenkoN. A.,
ZeleninaD. A.,
FedorkinO. N.,
SolovijevA. G.,
LukashevaL. I.,
AtabekovJ. C.1990; Expression of RNA transcripts of potato virus X full-length and subgenomic cDNAs. Biochimie 72:677–684
MorozovS. Yu.,
MiroshnichenkoN. A.,
SolovyevA. G.,
ZeleninaD. A.,
FedorkinO. N.,
LukashevaL. I.,
GrachevS. A.,
ChernovB. K.1991a; In vitro membrane binding of the translation products of the carlavirus 7-kDa protein genes. Virology 183:782–785
MorozovS. Yu.,
MiroshnichenkoN. A.,
SolovyevA. G.,
FedorkinO. N.,
ZeleninaD. A.,
LukashevaL. I.,
KarasevA. V.,
DoljaV. V.,
AtabekovJ. G.1991b; Expression strategy of the potato virus X triple gene block. J Gen Virol 72:2039–2042
MorozovS. Yu.,
FedorkinO. N.,
JuttnerG.,
SchiemannJ.,
BaulcombeD. C.,
AtabekovJ. G.1997; Complementation of a potato virus X mutant mediated by bombardment of plant tissues with cloned viral movement protein genes. J Gen Virol 78:2077–2083
MorozovS. Yu.,
SolovyevA. G.,
KalininaN. O.,
FedorkinO. N.,
SamuilovaO. V.,
SchiemannJ.,
AtabekovJ. G.1999; Evidence for two nonoverlapping functional domains in the potato virus X 25K movement protein. Virology 260:55–63
MushegianA. R.,
KooninE. V.1993; Cell-to-cell movement of plant viruses. Insights from amino acid sequence comparisons of movement proteins and from analogies with cellular transport systems. Arch Virol 133:239–257
NapuliA. J.,
AlzhanovaD. V.,
DoneanuC. E.,
BarofskyD. F.,
KooninE. V.,
DoljaV. V.2003; The 64-Kilodalton capsid protein homolog of Beet yellows virus is required for assembly of virion tails. J Virol 77:2377–2384
OhnoT.,
TakamatsuN.,
MeshiT.,
OkadaY.,
NishiguchiM.,
KihoY.1983; Single amino acid substitution in 30K protein of TMV defective in virus transport function. Virology 131:255–258
PengC. W.,
PeremyslovV. V.,
MushegianA. R.,
DawsonW. O.,
DoljaV. V.2001; Functional specialization and evolution of leader proteinases in the family Closteroviridae
. J Virol 75:12153–12160
PeremyslovV. V.,
HagiwaraY.,
DoljaV. V.1999; HSP70 homolog functions in cell-to-cell movement of a plant virus. Proc Natl Acad Sci U S A 96:14771–14776
PlanteC. A.,
KimK. H.,
Pillai-NairN.,
OsmanT. A.,
BuckK. W.,
HemenwayC. L.2000; Soluble, template-dependent extracts from Nicotiana benthamiana plants infected with potato virus X transcribe both plus- and minus-strand RNA templates. Virology 275:444–451
ProkhnevskyA. I.,
PeremyslovV. V.,
NapuliA. J.,
DoljaV. V.2002; Interaction between long-distance transport factor and Hsp70-related movement protein of beet yellows virus. J Virol 76:11003–11011
RadfordJ. E.,
WhiteR. G.2001; Effects of tissue preparation-induced callose synthesis on estimates of plasmodesmata size exclusion limits. Protoplasma 216:47–55
RajamakiM. L.,
ValkonenJ. P.1999; The 6K2 protein and the VPg of potato virus A are determinants of systemic infection in Nicandra physaloides
. Mol Plant–Microbe Interact 12:1074–1081
ReversF.,
Le GallO.,
CandresseT.,
MauleA. J.1999; New advances in understanding the molecular biology of plant/potyvirus interactions. Mol Plant–Microbe Interact 12:367–376
RobertsI. M.,
WangD.,
FindlayK.,
MauleA. J.1998; Ultrastructural and temporal observations of the potyvirus cylindrical inclusions (CIs) show that the CI protein acts transiently in aiding virus movement. Virology 245:173–181
Rodriguez-CerezoE.,
FindlayK.,
ShawJ. G.,
LomonossoffG. P.,
QiuS. G.,
LinsteadP.,
ShanksM.,
RiscoC.1997; The coat and cylindrical inclusion proteins of a potyvirus are associated with connections between plant cells. Virology 236:296–306
RojasM. R.,
ZerbiniF. M.,
AllisonR. F.,
GilbertsonR. L.,
LucasW. J.1997; Capsid protein and helper component-proteinase function as potyvirus cell-to-cell movement proteins. Virology 237:283–295
RupasovV. V.,
MorozovS. Yu.,
KanyukaK. V.,
ZavrievS. K.1989; Partial nucleotide sequence of potato virus M RNA shows similarities to potexviruses in gene arrangement and the encoded amino acid sequences. J Gen Virol 70:1861–1869
SaenzP.,
SalvadorB.,
Simon-MateoC.,
KasschauK. D.,
CarringtonJ. C.,
GarciaJ. A.2002; Host-specific involvement of the HC protein in the long-distance movement of potyviruses. J Virol 76:1922–1931
Santa CruzS.,
RobertsA. G.,
PriorD. A. M.,
ChapmanS.,
OparkaK. J.1998; Cell-to-cell and phloem-mediated transport of potato virus X: the role of virions. Plant Cell 10:495–510
SatoK.,
UedaT.,
NakanoA.1999; The Arabidopsis thaliana RER1 gene family: its potential role in the endoplasmic reticulum localization of membrane proteins. Plant Mol Biol 41:815–824
SatoK.,
SatoM.,
NakanoA.2001; Rer1p, a retrieval receptor for endoplasmic reticulum membrane proteins, is dynamically localized to the Golgi apparatus by coatomer. J Cell Biol 152:935–944
SchmittC.,
BalmoriE.,
JonardG.,
RichardsK. E.,
GuilleyH.1992; In vitro mutagenesis of biologically active transcripts of beet necrotic yellow vein virus RNA 2: evidence that a domain of the 75-kDa readthrough protein is important for efficient virus assembly. Proc Natl Acad Sci U S A 89:5715–5719
ScholzeP.,
FreissmuthM.,
SitteH. H.2002; Mutations within an intramembrane leucine heptad repeat disrupt oligomer formation of the rat GABA transporter 1. J Biol Chem 277:43682–43690
SchwartzM.,
ChenJ.,
JandaM.,
SullivanM.,
den BoonJ.,
AhlquistP.2002; A positive-strand RNA virus replication complex parallels form and function of retrovirus capsids. Mol Cell 9:505–514
SitT. L.,
AbouhaidarM. G.1993; Infectious RNA transcripts derived from cloned cDNA of papaya mosaic virus: effect of mutations to the capsid and polymerase proteins. J Gen Virol 74:1133–1140
SivaguruM.,
FujiwaraT.,
SamajJ.7 other authors2000; Aluminium-induced β -1,3-glucan inhibits cell-to-cell trafficking of molecules through plasmodesmata. A new mechanism of aluminium toxicity in plants. Plant Physiol 124:991–1005
SjöbergM.,
GaroffH.2003; Interactions between the transmembrane segments of the alphavirus E1 and E2 proteins play a role in virus budding and fusion. J Virol 77:3441–3450
SkryabinK. G.,
MorozovS. Yu.,
KraevA. S.,
RozanovM. N.,
ChernovB. K.,
LukashevaL. I.,
AtabekovJ. G.1988; Conserved and variable elements in RNA genomes of potexviruses. FEBS Lett 240:33–40
SolovyevA. G.,
SavenkovE. I.,
AgranovskyA. A.,
MorozovS. Yu.1996; Comparisons of the genomic cis -elements and coding regions in RNA β components of the hordeiviruses barley stripe mosaic virus, lychnis ringspot virus, and poa semilatent virus. Virology 219:9–18
SolovyevA. G.,
SavenkovE. I.,
GrdzelishviliV. Z.,
KalininaN. O.,
MorozovS. Yu.,
SchiemannJ.,
AtabekovJ. G.1999; Movement of hordeivirus hybrids with exchanges in the triple gene block. Virology 253:278–287
TamaiA.,
MeshiT.2001; Cell-to-cell movement of potato virus X: the role of p12 and p8 encoded by the second and third open reading frames of the triple gene block. Mol Plant–Microbe Interact 14:1158–1167
ThomasC. L.,
MauleA. J.2000; Limitations on the use of fused green fluorescent protein to investigate structure–function relationships for the cauliflower mosaic virus movement protein. J Gen Virol 81:1851–1855
TzfiraT.,
RheeY.,
ChenM. H.,
KunikT.,
CitovskyV.2000; Nucleic acid transport in plant–microbe interactions: the molecules that walk through the walls. Annu Rev Microbiol 54:187–219
VerchotJ.,
AngellS. M.,
BaulcombeD. C.1998; In vivo translation of the triple gene block of potato virus X requires two subgenomic mRNAs. J Virol 728316–8320
VilarM.,
SauriA.,
MonneM.,
MarcosJ. F.,
von HeijneG.,
Perez-PayaE.,
MingarroI.2002; Insertion and topology of a plant viral movement protein in the endoplasmic reticulum membrane. J Biol Chem 277:23447–23452
VoinnetO.,
LedererC.,
BaulcombeD. C.2000; A viral movement protein prevents spread of the gene silencing signal in Nicotiana benthamiana
. Cell 103:157–167
von BargenS.,
SalchertK.,
PaapeM.,
PiechullaB.,
KellmannJ.-W.2001; Interactions between the tomato spotted wilt virus movement protein and plant proteins showing homologies to myosin, kinesin and DNAJ-like chaperones. Plant Physiol Biochem 39:1083–1093
WongS. M.,
LeeK. C.,
YuH. H.,
LeongW. F.1998; Phylogenetic analysis of triple gene block viruses based on the TGB 1 homolog gene indicates a convergent evolution. Virus Genes 16:295–302
WungC. H.,
HsuY. H.,
LiouD. Y.,
HuangW. C.,
LinN. S.,
ChangB. Y.1999; Identification of the RNA-binding sites of the triple gene block protein 1 of bamboo mosaic potexvirus. J Gen Virol 80:1119–1126
YangY.,
DingB.,
BaulcombeD. C.,
VerchotJ.2000; Cell-to-cell movement of the 25K protein of potato virus X is regulated by three other viral proteins. Mol Plant–Microbe Interact 13:599–605
YelinaN. E.,
SavenkovE. I.,
SolovyevA. G.,
MorozovS. Yu.,
ValkonenJ. P. T.2002; Long-distance movement, virulence, and RNA silencing suppression controlled by a single protein in hordei- and potyviruses: complementary functions between virus families. J Virol 76:12981–12991
ZamyatninA. A.Jr,
SolovyevA. G.,
SablinaA. A.7 other authors2002; Dual-colour imaging of membrane protein targeting directed by poa semilatent virus movement protein TGBp3 in plant and mammalian cells. J Gen Virol 83:651–662
ZamyatninA. A.Jr,
SolovyevA. G.,
SavenkovE. I.,
MorozovS. Yu.,
ValkonenJ. P. T.2003; Intracellular trafficking of the proteins encoded by the triple gene block of Potato mop-top virus
. VIIIth International Congress of Plant Pathology (Christchurch, New Zealand, 2–7 February, 2003):