#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Tubule-Guided Cell-to-Cell Movement of a Plant Virus Requires Class XI Myosin Motors


Cell-to-cell movement of plant viruses occurs via plasmodesmata (PD), organelles that evolved to facilitate intercellular communications. Viral movement proteins (MP) modify PD to allow passage of the virus particles or nucleoproteins. This passage occurs via several distinct mechanisms one of which is MP-dependent formation of the tubules that traverse PD and provide a conduit for virion translocation. The MP of tubule-forming viruses including Grapevine fanleaf virus (GFLV) recruit the plant PD receptors called Plasmodesmata Located Proteins (PDLP) to mediate tubule assembly and virus movement. Here we show that PDLP1 is transported to PD through a specific route within the secretory pathway in a myosin-dependent manner. This transport relies primarily on the class XI myosins XI-K and XI-2. Inactivation of these myosins using dominant negative inhibition results in mislocalization of PDLP and MP and suppression of GFLV movement. We also found that the proper targeting of specific markers of the Golgi apparatus, the plasma membrane, PD, lipid raft subdomains within the plasma membrane, and the tonoplast was not affected by myosin XI-K inhibition. However, the normal tonoplast dynamics required myosin XI-K activity. These results reveal a new pathway of the myosin-dependent protein trafficking to PD that is hijacked by GFLV to promote tubule-guided transport of this virus between plant cells.


Vyšlo v časopise: Tubule-Guided Cell-to-Cell Movement of a Plant Virus Requires Class XI Myosin Motors. PLoS Pathog 7(10): e32767. doi:10.1371/journal.ppat.1002327
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002327

Souhrn

Cell-to-cell movement of plant viruses occurs via plasmodesmata (PD), organelles that evolved to facilitate intercellular communications. Viral movement proteins (MP) modify PD to allow passage of the virus particles or nucleoproteins. This passage occurs via several distinct mechanisms one of which is MP-dependent formation of the tubules that traverse PD and provide a conduit for virion translocation. The MP of tubule-forming viruses including Grapevine fanleaf virus (GFLV) recruit the plant PD receptors called Plasmodesmata Located Proteins (PDLP) to mediate tubule assembly and virus movement. Here we show that PDLP1 is transported to PD through a specific route within the secretory pathway in a myosin-dependent manner. This transport relies primarily on the class XI myosins XI-K and XI-2. Inactivation of these myosins using dominant negative inhibition results in mislocalization of PDLP and MP and suppression of GFLV movement. We also found that the proper targeting of specific markers of the Golgi apparatus, the plasma membrane, PD, lipid raft subdomains within the plasma membrane, and the tonoplast was not affected by myosin XI-K inhibition. However, the normal tonoplast dynamics required myosin XI-K activity. These results reveal a new pathway of the myosin-dependent protein trafficking to PD that is hijacked by GFLV to promote tubule-guided transport of this virus between plant cells.


Zdroje

1. Benitez-AlfonsoYFaulknerCRitzenthalerCMauleAJ 2010 Plasmodesmata: gateways to local and systemic virus infection. Mol Plant Microbe Interact 23 1403 1412

2. TzfiraTRheeYChenMHKunikTCitovskyV 2000 Nucleic acid transport in plant-microbe interactions: the molecules that walk through the walls. Annu Rev Microbiol 54 187 219

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

4. HeinleinM 2002 Plasmodesmata: dynamic regulation and role in macromolecular cell-to-cell signaling. Curr Opin Plant Biol 5 543 552

5. RitzenthalerCHofmannC 2007 Tubule-guided movement of plant viruses. WaigmannEHeinleinM Plant Cell Monogr 7 Berlin-Heidelberg Springer-Verlag 63 83

6. NiehlAHeinleinM 2010 Cellular pathways for viral transport through plasmodesmata. Protoplasma 248 75 99

7. Verchot-LubiczJTorranceLSolovyevAGMorozovSYJacksonAO 2010 Varied movement strategies employed by triple gene block-encoding viruses. Mol Plant Microbe Interact 23 1231 1247

8. DoljaVVKreuzeJFValkonenJP 2006 Comparative and functional genomics of closteroviruses. Virus Res 117 38 51

9. OparkaKJ 2004 Getting the message across: how do plant cells exchange macromolecular complexes? Trends Plant Sci 9 33 41

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

11. AmariKBoutantEHofmannCSchmitt-KeichingerCFernandez- CalvinoL 2010 A family of plasmodesmal proteins with receptor-like properties for plant viral movement proteins. PLoS Pathog 6 e1001119

12. SattentauQ 2008 Avoiding the void: cell-to-cell spread of human viruses. Nat Rev Microbiol 6 815 826

13. FacklerOTKräusslichHG 2006 Interactions of human retroviruses with the host cell cytoskeleton. Curr Opin Microbiol 9 409 415

14. GreberUFWayM 2006 A superhighway to virus infection. Cell 124 741 54

15. BoykoVFerralliJHeinleinM 2000 Cell-to-cell movement of TMV RNA is temperature-dependent and corresponds to the association of movement protein with microtubules. Plant J 22 315 325

16. BoykoVHuQSeemanpillaiMAshbyJHeinleinM 2007 Validation of microtubule-associated Tobacco mosaic virus RNA movement and involvement of microtubule-aligned particle trafficking. Plant J 51 589 603

17. WrightKMWoodNTRobertsAGChapmanSBoevinkP 2007 Targeting of TMV movement protein to plasmodesmata requires the actin/ER network: Evidence from FRAP. Traffic 8 21 31

18. HarriesPAParkJWSasakiNBallardKDMauleAJ 2009 Differing requirements for actin and myosin by plant viruses for sustained intercellular movement. Proc Natl Acad Sci U S A 106 17594 17599

19. Guenoune-GelbartDElbaumMSagiGLevyAEpelBL 2008 Tobacco mosaic virus (TMV) replicase and movement proteinfunction synergistically in facilitating TMV spread by lateral diffusion in the plasmodesmal desmotubule of Nicotiana benthamiana. Mol Plant-Microbe Interact 21 335 345

20. HarriesPASchoelzJENelsonRS 2010 Intracellular transport of viruses and their components: utilizing the cytoskeleton and membrane highways. Mol Plant Microbe Interact 23 1381 1393

21. PeremyslovVVMocklerTCFilichkinSAFoxSEJaiswalP 2011 Expression, splicing, and evolution of the myosin gene family in plants. Plant Phys 155 1191 1204

22. ReddyASDayIS 2001 Analysis of the myosins encoded in the recently completed Arabidopsis thaliana genome sequence. Genome Biol 2 1 17

23. AvisarDProkhnevskyAIMakarovaKSKooninEVDoljaVV 2008a Myosin XI-K is required for rapid trafficking of Golgi stacks, peroxisomes, and mitochondria in leaf cells of Nicotiana benthamiana. Plant Physiol 146 1098 1108

24. PeremyslovVVProkhnevskyAIAvisarDDoljaVV 2008 Two class XI myosins function in organelle trafficking and root hair development in Arabidopsis. Plant Physiol 146 1109 1116

25. UedaHYokotaEKutsunaNShimadaTTamuraK 2010 Myosin- dependent endoplasmic reticulum motility and F-actin organization in plant cells. Proc Natl Acad Sci U S A 107 6894 6899

26. ProkhnevskyAIPeremyslovVVDoljaVV 2008 Overlapping functions of the four class XI myosins in Arabidopsis growth, root hair elongation, and organelle motility. Proc Natl Acad Sci U S A 105 19744 19749

27. PeremyslovVVProkhnevskyAIDoljaVV 2010 Class XI myosins are required for development, cell expansion, and F-actin organization in Arabidopsis. Plant Cell 22 1883 1897

28. ReicheltSKnightAEHodgeTPBaluskaFSamajJ 1999 Characterization of the unconventional myosin VIII in plant cells and its localization at the post-cytokinetic cell wall. Plant J 19 555 567

29. GolombLAbu-AbiedMBelausovESadotE 2008 Different subcellular localizations and functions of Arabidopsis myosin VIII. BMC Plant Biol 8 3

30. SattarzadehAFranzenRSchmelzerE 2008 The Arabidopsis class VIII myosin ATM2 is involved in endocytosis. Cell Motil Cytoskeleton 65 457 468

31. AlzhanovaDVNapuliAJCreamerRDoljaVV 2001 Cell-to-cell movement and assembly of a plant closterovirus: Roles for the capsid proteins and Hsp70 homolog. EMBO J 20 6997 7007

32. ProkhnevskyAIPeremyslovVVDoljaVV 2005 Actin cytoskeleton is involved in targeting of a viral Hsp70 homolog to the cell periphery. J Virol 79 14421 14428

33. AvisarDProkhnevskyAIDoljaVV 2008b Class VIII myosins are required for plasmodesmatal localization of a closterovirus Hsp70 homolog. J Virol 82 2836 2843

34. YuanZChenHChenQOmuraTXieL 2011 The early secretory pathway and an actin-myosin VIII motility system are required for plasmodesmatal localization of the NSvc4 protein of Rice stripe virus. Virus Res 159 62 68

35. MortonWMAyscoughKRMcLaughlinPJ 2000 Latrunculin alters the actin monomer subunit interface to prevent polymerization. Nat Cell Biol 2 376 378

36. KrementsovDNKrementsovaEBTrybusKM 2004 Myosin V: regulation by calcium, calmodulin, and the tail domain. J Cell Biol 164 877 886

37. PashkovaNJinYRamaswamySWeismanLS 2006 Structural basis for myosin V discrimination between distinct cargoes. EMBO J 25 693 700

38. LaporteCVetterGLoudesAMRobinsonDGHillmerS 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

39. NebenführAGallagherLADunahayTGFrohlickJAMazurkiewiczAM 1999 Stop-and-go movements of plant Golgi stacks are mediated by the actomyosin system. Plant Physiol 121 1127 1142

40. TominagaMYokotaESonobeSShimmenT 2000 Mechanism of inhibition of cytoplasmic streaming by a myosin inhibitor, 2,3-butanedione monoxime. Protoplasma 213 46 54

41. BrandizziFFrangneNMarc-MartinSHawesCNeuhausJM 2002 The destination for single-pass membrane proteins is influenced markedly by the length of the hydrophobic domain. Plant Cell 14 1077 92

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

43. SimpsonCThomasCFindlayKBayerEMauleAJ 2009 An arabidopsis GPI-anchor plasmodesmal neck protein with callose binding activity and potential to regulate cell-to-cell trafficking. Plant Cell 21 581 594

44. NelsonBKCaiXNebenführA 2007 A multi-color set of in vivo organelle markers for colocalization studies in Arabidopsis and other plants. Plant J 51 1126 1136

45. MartyF 1999 Plant Vacuoles. Plant Cell 11 587 599

46. SaitoCUedaTAbeHWadaYKuroiwaT 2002 A complex and mobile structure forms a distinct subregion within the continuous vacuolar membrane in young cotyledons of Arabidopsis. Plant J 29 245 255

47. SuzukiYCraigieR 2007 The road to chromatin - nuclear entry of retroviruses. Nature Rev Microbiol 5 187 196

48. LymanMGEnquistLW 2009 Herpesvirus interactions with the host cytoskeleton. J Virol 83 2058 2066

49. HallerCFacklerOT 2008 HIV-1 at the immunological and T-lymphocytic virological synapse. Biol Chem 389 1253 1260

50. DoddingMPWayM 2009 Nck- and N-WASP-dependent actin-based motility is conserved in divergent vertebrate poxviruses. Cell Host Microbe 6 536 550

51. den BoonJADiazAAhlquistP 2010 Cytoplasmic viral replication complexes. Cell Host Microbe 8 77 85

52. NagyPDWangRYPoganyJHafrenAMakinenK 2011 Emerging picture of host chaperone and cyclophilin roles in RNA virus replication. Virology 411 374 82

53. XuXMJacksonD 2010 Lights at the end of the tunnel: new views of plasmodesmal structure and function. Curr Opin Plant Biol 13 684 692

54. GillespieTBoevinkPHauptSRobertsAGTothR 2002 Functional analysis of a DNA shuffled movement protein reveals that microtubules are dispensable for the cell-to-cell movement of Tobacco mosaic virus. Plant Cell 14 1207 1222

55. KawakamiSWatanabeYBeachyRN 2004 Tobacco mosaic virus infection spreads cell to cell as intact replication complexes. Proc Natl Acad Sci U S A 101 6291 6296

56. LiuJ-ZBlancaflorEBNelsonRS 2005 The Tobacco mosaic virus 126-kilodalton protein, a constituent of the virus replication complex, alone or within the complex aligns with and traffics along microfilaments. Plant Physiol 138 1853 1865

57. RitzenthalerCPinckMPinckL 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

Štítky
Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

Článok vyšiel v časopise

PLOS Pathogens


2011 Číslo 10
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#