A Family of Plasmodesmal Proteins with Receptor-Like Properties for Plant Viral Movement Proteins

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Plasmodesmata (PD) are essential but poorly understood structures in plant cell walls that provide symplastic continuity and intercellular communication pathways between adjacent cells and thus play fundamental roles in development and pathogenesis. Viruses encode movement proteins (MPs) that modify these tightly regulated pores to facilitate their spread from cell to cell. The most striking of these modifications is observed for groups of viruses whose MPs form tubules that assemble in PDs and through which virions are transported to neighbouring cells. The nature of the molecular interactions between viral MPs and PD components and their role in viral movement has remained essentially unknown. Here, we show that the family of PD-located proteins (PDLPs) promotes the movement of viruses that use tubule-guided movement by interacting redundantly with tubule-forming MPs within PDs. Genetic disruption of this interaction leads to reduced tubule formation, delayed infection and attenuated symptoms. Our results implicate PDLPs as PD proteins with receptor-like properties involved the assembly of viral MPs into tubules to promote viral movement.

Vyšlo v časopise: A Family of Plasmodesmal Proteins with Receptor-Like Properties for Plant Viral Movement Proteins. PLoS Pathog 6(9): e32767. doi:10.1371/journal.ppat.1001119
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1001119

Souhrn

Zdroje

1. EugeninEA

GaskillPJ

BermanJW

2009 Tunneling nanotubes (TNT) are induced by HIV-infection of macrophages: A potential mechanism for intercellular HIV trafficking. Cellular Immunol 254 142 148

2. GerdesH-H

CarvalhoRN

2008 Intercellular transfer mediated by tunneling nanotubes. Curr Opin Cell Biol 20 470 475

3. SowinskiS

JollyC

BerninghausenO

PurbhooMA

ChauveauA

2008 Membrane nanotubes physically connect T cells over long distances presenting a novel route for HIV-1 transmission. Nat Cell Biol 10 211 219

4. BrandenburgB

ZhuangX

2007 Virus trafficking - learning from single-virus tracking. Nat Rev Micro 5 197 208

5. LucasWJ

HamB-K

KimJ-Y

2009 Plasmodesmata - bridging the gap between neighboring plant cells. Trends Cell Biol 19 495 503

6. MauleAJ

2008 Plasmodesmata: structure, function and biogenesis. Curr Opin Plant Biol 11 680 686

7. AlfonsoYB

CantrillL

JacksonD

2006 Plasmodesmata: Cell-cell channels in plants.

BaluskaF

VolkmannD

BarlowPW

Cell-cell channels Austin, TX Landes Biosciences 340

8. LucasWJ

LeeJY

2004 Plasmodesmata as a supracellular control network in plants. Nat Rev Mol Cell Biol 5 712 726

9. HeinleinM

EpelBL

2004 Macromolecular transport and signaling through plasmodesmata. Internat Rev Cytol 235 93 164

10. MelcherU

2000 The ‘30K’ superfamily of viral movement proteins. J Gen Virol 81 257 266

11. TalianskyM

TorranceL

KalininaNO

2008 Role of plant virus movement proteins. Methods Mol Biol 451 33 54

12. DingB

HaudenshieldJS

HullRJ

WolfS

BeachyRN

1992 Secondary plasmodesmata are specific sites of localization of the Tobacco mosaic virus movement protein in transgenic tobacco plants. Plant Cell 4 915 928

13. RitzenthalerC

HofmannC

2007 Tubule-guided movement of plant viruses.

WaigmannE

HeinleinM

Plant Cell Monogr Berlin-Heidelberg Springer-Verlag 63 83

14. van LentJWM

Schmitt-KeichingerC

2006 Viral movement proteins induce tubule formation in plant and insect cells.

BaluskaF

VolkmannD

BarlowPW

Cell-cell channels Austin, TX Landes Bioscience 160 174

15. LazarowitzSG

BeachyRN

1999 Viral movement proteins as probes for intracellular and intercellular trafficking in plants. Plant Cell 11 535 548

16. Sanchez-NavarroJ

FajardoT

ZiccaS

PallasV

StavoloneL

2010 Caulimoviridae tubule-guided transport is dictated by movement protein properties. J Virol: 84 4109 4112

17. PouwelsJ

KornetN

van BersN

GuighelaarT

van LentJ

2003 Identification of distinct steps during tubule formation by the movement protein of Cowpea mosaic virus. J Gen Virol 84 3485 3494

18. PouwelsJ

van der VeldenT

WillemseJ

BorstJW

van LentJ

2004 Studies on the origin and structure of tubules made by the movement protein of Cowpea mosaic virus. J Gen Virol 85 3787 3796

19. PouwelsJ

Van Der KrogtGN

Van LentJ

BisselingT

WellinkJ

2002 The cytoskeleton and the secretory pathway are not involved in targeting the Cowpea mosaic virus movement protein to the cell periphery. Virology 297 48 56

20. HuangZ

AndrianovV

HanY

HowellS

2001 Identification of arabidopsis proteins that interact with the Cauliflower mosaic virus (CaMV) movement protein. Plant Mol Biol 47 663 675

21. LaporteC

VetterG

LoudesAM

RobinsonDG

HillmerS

2003 Involvement of the secretory pathway and the cytoskeleton in intracellular targeting and tubule assembly of Grapevine fanleaf virus movement protein in tobacco BY-2 cells. Plant Cell 15 2058 2075

22. SoellickT

UhrigJF

BucherGL

KellmannJW

SchreierPH

2000 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 USA 97 2373 2378

23. PaapeM

SolovyevAG

ErokhinaTN

MininaEA

SchepetilnikovMV

2006 At-4/1, an interactor of the Tomato spotted wilt virus movement protein, belongs to a new family of plant proteins capable of directed intra- and intercellular trafficking. Mol Plant-Microbe Interact 19 874 883

24. ThomasCL

BayerE

RitzenthalerC

Fernandez-CalvinoL

MauleAJ

2008 Specific targeting of a plasmodesmal protein affecting cell-to-cell communication. PLoS Biol 6 e7

25. ElangovanM

DayRN

PeriasamyA

2002 Nanosecond fluorescence resonance energy transfer-fluorescence lifetime imaging microscopy to localize the protein interactions in a single living cell. J Microsc 205 3 14

26. EpelBL

2009 Plant viruses spread by diffusion on ER-associated movement-protein-rafts through plasmodesmata gated by viral induced host [beta]-1,3-glucanases. Semin Cell Dev Biol doi:10.1016/j.semcdb.2009.1005.1010

27. BoevinkP

OparkaKJ

2005 Virus-host interactions during movement processes. Plant Physiol 138 1815 1821

28. LucasWJ

2006 Plant viral movement proteins: agents for cell-to-cell trafficking of viral genomes. Virology 344 169 184

29. PhillipsonBA

PimplP

daSilvaLL

CroftsAJ

TaylorJP

2001 Secretory bulk flow of soluble proteins is efficient and COPII dependent. Plant Cell 13 2005 2020

30. RuggenthalerP

FichtenbauerD

KrasenskyJ

JonakC

WaigmannE

2009 Microtubule-associated protein AtMPB2C plays a role in organization of cortical microtubules, stomata patterning, and tobamovirus infectivity. Plant Physiol 149 1354 1365

31. MansillaC

AguilarI

Martinez-HerreraD

SanchezF

PonzF

2006 Physiological effects of constitutive expression of Oilseed Rape Mosaic Tobamovirus (ORMV) movement protein in Arabidopsis thaliana. Transgenic Res 15 761 770

32. StavoloneL

VillaniME

LeclercD

HohnT

2005 A coiled-coil interaction mediates Cauliflower mosaic virus cell-to-cell movement. Proc Natl Acad Sci U S A 102 6219 6224

33. PerbalMC

ThomasCL

MauleAJ

1993 Cauliflower mosaic virus gene I product (P1) forms tubular structures which extend from the surface of infected protoplasts. Virology 195 281 285

34. ThomasCL

MauleAJ

1999 Identification of inhibitory mutants of Cauliflower mosaic virus movement protein function after expression in insect cells. J Virol 73 7886 7890

35. ThomasCL

MauleAJ

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

36. BassiM

FavaliMA

ContiGG

1974 Cell wall protrusions induced by cauliflower mosaic virus in Chinese cabbage leaves: a cytochemical and autoradiographic study. Virology 60 353 358

37. LinsteadPJ

HillsGJ

PlaskittKA

WilsonIG

HarkerCL

1988 The subcellular location of the gene I product of cauliflower mosaic virus is consistent with a function associated with virus spread. J Gen Virol 69 1809 1818

38. HuangZ

HanY

HowellS

2000 Formation of surface tubules and fluorescent foci in Arabidopsis thaliana protoplasts expressing a fusion between the green fluorescent protein and the Cauliflower mosaic virus movement protein. Virology 271 58 64

39. RaffaeleS

BayerE

LafargeD

CluzetS

German RetanaS

2009 Remorin, a solanaceae protein resident in membrane rafts and plasmodesmata, impairs Potato virus X movement. Plant Cell 21 1541 1555

40. ChenMH

TianGW

GafniY

CitovskyV

2005 Effects of calreticulin on viral cell-to-cell movement. Plant Physiol 138 1866 1876

41. ZavalievR

SagiG

GeraA

EpelBL

2009 The constitutive expression of Arabidopsis plasmodesmal-associated class 1 reversibly glycosylated polypeptide impairs plant development and virus spread. J Exp Bot 61 131 142

42. KarimiM

InzeD

DepickerA

2002 GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci 7 193 195

43. ViryM

SerghiniMA

HansF

RitzenthalerC

PinckM

1993 Biologically active transcripts from cloned cDNA of genomic Grapevine fanleaf nepovirus RNAs. J Gen Virol 74 169 174

44. GaireF

SchmittC

Stussi-GaraudC

PinckL

RitzenthalerC

1999 Protein 2A of Grapevine fanleaf nepovirus is implicated in RNA2 replication and colocalizes to the replication site. Virology 264 25 36

45. MerzlyakEM

GoedhartJ

ShcherboD

BulinaME

ShcheglovAS

2007 Bright monomeric red fluorescent protein with an extended fluorescence lifetime. Nat Methods 4 555 557

46. BrandnerK

SambadeA

BoutantE

DidierP

MelyY

2008 Tobacco mosaic virus movement protein interacts with green fluorescent protein-tagged microtubule end-binding protein 1. Plant Physiol 147 611 623

47. van der FitsL

DeakinEA

HogeJH

MemelinkJ

2000 The ternary transformation system: constitutive virG on a compatible plasmid dramatically increases Agrobacterium-mediated plant transformation. Plant Mol Biol 43 495 502

48. PinckL

FuchsM

PinckM

RavelonandroM

WalterB

1988 A satellite RNA in Grapevine fanleaf virus strain F13. J Gen Virol 69 233 239

49. WalterB

EtienneL

1987 Detection of the Grapevine fanleaf viruses away from the period of vegetation. J Phytopathol 120 355 364

50. KhelifaM

MasseD

BlancS

DruckerM

2010 Evaluation of the minimal replication time of Cauliflower mosaic virus in different hosts. Virology 396 238 245

51. KobayashiK

TsugeS

StavoloneL

HohnT

2002 The Cauliflower mosaic virus virion-associated protein is dispensable for viral replication in single cells. J Virol 76 9457 9464

52. WrightKM

WoodNT

RobertsAG

ChapmanS

BoevinkP

2007 Targeting of TMV movement protein to plasmodesmata requires the actin/ER network; evidence from FRAP. Traffic 8 21 31

53. RitzenthalerC

PinckM

PinckL

1995 Grapevine fanleaf nepovirus P38 putative movement protein is not transiently expressed and is a stable final maturation product in vivo. J Gen Virol 76 907 915

54. BoykoV

FerralliJ

AshbyJ

SchellenbaumP

HeinleinM

2000 Function of microtubules in intercellular transport of plant virus RNA. Nat Cell Biol 2 826 832

55. YooSD

ChoYH

SheenJ

2007 Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2 1565 1572

56. BelinC

SchmittC

GaireF

WalterB

DemangeatG

1999 The nine C-terminal residues of the Grapevine fanleaf nepovirus movement protein are critical for systemic virus spread. J Gen Virol 80 1347 1356

57. BrodersenP

Sakvarelidze-AchardL

Bruun-RasmussenM

DunoyerP

YamamotoYY

2008 Widespread translational inhibition by plant miRNAs and siRNAs. Science 320 1185 1190

58. HurkmanWJ

TanakaCK

1986 Solubilization of plant membrane proteins for analysis by two-dimensional gel electrophoresis. Plant Physiol 81 802 806