Similarities in intracellular transport of plant viral movement proteins BMB2 and TGB3 Free

Abstract

The cell-to-cell transport of many plant viruses through plasmodesmata requires viral movement proteins (MPs) encoded by a ‘triple gene block’ (TGB) and termed TGB1, TGB2 and TGB3. TGB3 is a small integral membrane protein that contains subcellular targeting signals and directs both TGB2 and the helicase domain-containing TGB1 protein to plasmodesmata-associated structures. Recently, we described a ‘binary movement block’ (BMB) coding for two MPs, BMB1 and BMB2. The BMB2 protein associates with endoplasmic reticulum (ER) membranes, accumulates at plasmodesmata-associated membrane bodies and directs the BMB1 helicase to these structures. TGB3 transport to cell peripheral bodies was previously shown to bypass the secretory pathway and involve a non-conventional mechanism. Here, we provide evidence that the intracellular transport of both poa semilatent virus TGB3 and hibiscus green spot virus BMB2 to plasmodesmata-associated sites can occur via lateral translocation along the ER membranes. Agrobacterium-mediated transient co-expression in leaves revealed that green fluorescent protein (GFP)-fused actin-binding domains of fimbrin (ABD2–GFP) and mouse talin (TAL–GFP) inhibited the subcellular targeting of TGB3 and BMB2 to plasmodesmata-associated bodies, which resulted in TGB3 and BMB2 accumulation in the cytoplasm in association with aberrant ER structures. Inhibition of COPII budding complex formation by the expression of a dominant-negative mutant of the small GTPase Sar1 had no detectable effect on BMB2 subcellular targeting, which therefore could occur without exit from the ER in COPII transport vesicles. Collectively, the presented data support the current view that plant viral MPs exploit the ER:actin network for their intracellular transport.

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2017-09-01
2024-03-29
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References

  1. Heinlein M. Plasmodesmata: channels for viruses on the move. Methods Mol Biol 2015; 1217:25–52 [View Article][PubMed]
    [Google Scholar]
  2. Lucas WJ. Plant viral movement proteins: agents for cell-to-cell trafficking of viral genomes. Virology 2006; 344:169–184 [View Article][PubMed]
    [Google Scholar]
  3. Heinlein M. Viral Transport and Interaction with the Host Cytoskeleton. In Kleinow T. (editor) Plant-Virus Interact Cham: Springer International Publishing; 2016 pp. 39–66 [CrossRef]
    [Google Scholar]
  4. Boyko V, Hu Q, Seemanpillai M, Ashby J, Heinlein M. Validation of microtubule-associated Tobacco mosaic virus RNA movement and involvement of microtubule-aligned particle trafficking. Plant J 2007; 51:589–603 [View Article][PubMed]
    [Google Scholar]
  5. Sambade A, Brandner K, Hofmann C, Seemanpillai M, Mutterer J et al. Transport of TMV movement protein particles associated with the targeting of RNA to plasmodesmata. Traffic 2008; 9:2073–2088 [View Article][PubMed]
    [Google Scholar]
  6. Reichel C, Beachy RN. Tobacco mosaic virus infection induces severe morphological changes of the endoplasmic reticulum. Proc Natl Acad Sci USA 1998; 95:11169–11174 [View Article][PubMed]
    [Google Scholar]
  7. Fujiki M, Kawakami S, Kim RW, Beachy RN. Domains of tobacco mosaic virus movement protein essential for its membrane association. J Gen Virol 2006; 87:2699–2707 [View Article][PubMed]
    [Google Scholar]
  8. Ashby J, Boutant E, Seemanpillai M, Groner A, Sambade A et al. Tobacco mosaic virus movement protein functions as a structural microtubule-associated protein. J Virol 2006; 80:8329–8344 [View Article][PubMed]
    [Google Scholar]
  9. Ferralli J, Ashby J, Fasler M, Boyko V, Heinlein M. Disruption of microtubule organization and centrosome function by expression of tobacco mosaic virus movement protein. J Virol 2006; 80:5807–5821 [View Article][PubMed]
    [Google Scholar]
  10. Ueda H, Yokota E, Kutsuna N, Shimada T, Tamura K et al. Myosin-dependent endoplasmic reticulum motility and F-actin organization in plant cells. Proc Natl Acad Sci USA 2010; 107:6894–6899 [View Article][PubMed]
    [Google Scholar]
  11. Hamada T, Tominaga M, Fukaya T, Nakamura M, Nakano A et al. RNA processing bodies, peroxisomes, Golgi bodies, mitochondria, and endoplasmic reticulum tubule junctions frequently pause at cortical microtubules. Plant Cell Physiol 2012; 53:699–708 [View Article][PubMed]
    [Google Scholar]
  12. Hamada T, Ueda H, Kawase T, Hara-Nishimura I. Microtubules contribute to tubule elongation and anchoring of endoplasmic reticulum, resulting in high network complexity in Arabidopsis. Plant Physiol 2014; 166:1869–1876 [View Article][PubMed]
    [Google Scholar]
  13. Peña EJ, Heinlein M. Cortical microtubule-associated ER sites: organization centers of cell polarity and communication. Curr Opin Plant Biol 2013; 16:764–773 [View Article][PubMed]
    [Google Scholar]
  14. Wang P, Hawkins TJ, Richardson C, Cummins I, Deeks MJ et al. The plant cytoskeleton, NET3C, and VAP27 mediate the link between the plasma membrane and endoplasmic reticulum. Curr Biol 2014; 24:1397–1405 [View Article][PubMed]
    [Google Scholar]
  15. Niehl A, Peña EJ, Amari K, Heinlein M. Microtubules in viral replication and transport. Plant J 2013; 75:290–308 [View Article][PubMed]
    [Google Scholar]
  16. Epel BL. 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 2009; 20:1074–1081 [View Article][PubMed]
    [Google Scholar]
  17. Dolja VV. Beet yellows virus: the importance of being different. Mol Plant Pathol 2003; 4:91–98 [View Article][PubMed]
    [Google Scholar]
  18. Solovyev AG, Makarov VV. Helical capsids of plant viruses: architecture with structural lability. J Gen Virol 2016; 97:1739–1754 [View Article][PubMed]
    [Google Scholar]
  19. Dolja VV, Kreuze JF, Valkonen JP. Comparative and functional genomics of closteroviruses. Virus Res 2006; 117:38–51 [View Article][PubMed]
    [Google Scholar]
  20. Medina V, Peremyslov VV, Hagiwara Y, Dolja VV. Subcellular localization of the HSP70-homolog encoded by beet yellows closterovirus. Virology 1999; 260:173–181 [View Article][PubMed]
    [Google Scholar]
  21. Prokhnevsky AI, Peremyslov VV, Dolja VV. Actin cytoskeleton is involved in targeting of a viral Hsp70 homolog to the cell periphery. J Virol 2005; 79:14421–14428 [View Article][PubMed]
    [Google Scholar]
  22. Avisar D, Prokhnevsky AI, Dolja VV. Class VIII myosins are required for plasmodesmatal localization of a closterovirus Hsp70 homolog. J Virol 2008; 82:2836–2843 [View Article][PubMed]
    [Google Scholar]
  23. Morozov SY, Solovyev AG. Triple gene block: modular design of a multifunctional machine for plant virus movement. J Gen Virol 2003; 84:1351–1366 [View Article][PubMed]
    [Google Scholar]
  24. Verchot-Lubicz J, Torrance L, Solovyev AG, Morozov SY, Jackson AO et al. Varied movement strategies employed by triple gene block-encoding viruses. Mol Plant Microbe Interact 2010; 23:1231–1247 [View Article][PubMed]
    [Google Scholar]
  25. Lim HS, Bragg JN, Ganesan U, Ruzin S, Schichnes D et al. Subcellular localization of the barley stripe mosaic virus triple gene block proteins. J Virol 2009; 83:9432–9448 [View Article][PubMed]
    [Google Scholar]
  26. Shemyakina EA, Erokhina TN, Gorshkova EN, Schiemann J, Solovyev AG et al. Formation of protein complexes containing plant virus movement protein TGBp3 is necessary for its intracellular trafficking. Biochimie 2011; 93:742–748 [View Article][PubMed]
    [Google Scholar]
  27. Zamyatnin AA, Solovyev AG, Sablina AA, Agranovsky AA, Katul L et al. Dual-colour imaging of membrane protein targeting directed by poa semilatent virus movement protein TGBp3 in plant and mammalian cells. J Gen Virol 2002; 83:651–662 [View Article][PubMed]
    [Google Scholar]
  28. Haupt S, Cowan GH, Ziegler A, Roberts AG, Oparka KJ et al. Two plant-viral movement proteins traffic in the endocytic recycling pathway. Plant Cell 2005; 17:164–181 [View Article][PubMed]
    [Google Scholar]
  29. Tilsner J, Cowan GH, Roberts AG, Chapman SN, Ziegler A et al. Plasmodesmal targeting and intercellular movement of potato mop-top pomovirus is mediated by a membrane anchored tyrosine-based motif on the lumenal side of the endoplasmic reticulum and the C-terminal transmembrane domain in the TGB3 movement protein. Virology 2010; 402:41–51 [View Article][PubMed]
    [Google Scholar]
  30. Zamyatnin AA, Solovyev AG, Savenkov EI, Germundsson A, Sandgren M et al. Transient coexpression of individual genes encoded by the triple gene block of potato mop-top virus reveals requirements for TGBp1 trafficking. Mol Plant Microbe Interact 2004; 17:921–930 [View Article][PubMed]
    [Google Scholar]
  31. Ho TL, Lee HC, Chou YL, Tseng YH, Huang WC et al. The cysteine residues at the C-terminal tail of Bamboo mosaic virus triple gene block protein 2 are critical for efficient plasmodesmata localization of protein 1 in the same block. Virology 2017; 501:47–53 [View Article][PubMed]
    [Google Scholar]
  32. Lee SC, Wu CH, Wang CW. Traffic of a viral movement protein complex to the highly curved tubules of the cortical endoplasmic reticulum. Traffic 2010; 11:912–930 [View Article][PubMed]
    [Google Scholar]
  33. Wu CH, Lee SC, Wang CW. Viral protein targeting to the cortical endoplasmic reticulum is required for cell-cell spreading in plants. J Cell Biol 2011; 193:521–535 [View Article][PubMed]
    [Google Scholar]
  34. Schepetilnikov MV, Solovyev AG, Gorshkova EN, Schiemann J, Prokhnevsky AI et al. Intracellular targeting of a hordeiviral membrane-spanning movement protein: sequence requirements and involvement of an unconventional mechanism. J Virol 2008; 82:1284–1293 [View Article][PubMed]
    [Google Scholar]
  35. Lim HS, Lee MY, Moon JS, Moon JK, Yu YM et al. Actin cytoskeleton and Golgi Involvement in Barley stripe mosaic virus Movement and cell wall localization of triple gene block proteins. Plant Pathol J 2013; 29:17–30 [View Article][PubMed]
    [Google Scholar]
  36. Cowan GH, Lioliopoulou F, Ziegler A, Torrance L. Subcellular localisation, protein interactions, and RNA binding of Potato mop-top virus triple gene block proteins. Virology 2002; 298:106–115 [View Article][PubMed]
    [Google Scholar]
  37. Lazareva EA, Lezzhov AA, Komarova TV, Morozov SY, Heinlein M et al. A novel block of plant virus movement genes. Mol Plant Pathol 2017; 18:611–624 [View Article][PubMed]
    [Google Scholar]
  38. Morozov SY, Solovyev AG. Did silencing suppression counter-defensive strategy contribute to origin and evolution of the triple gene block coding for plant virus movement proteins?. Front Plant Sci 2012; 3:136 [View Article][PubMed]
    [Google Scholar]
  39. Morozov SY, Solovyev AG. Phylogenetic relationship of some "accessory" helicases of plant positive-stranded RNA viruses: toward understanding the evolution of triple gene block. Front Microbiol 2015; 6:1–8 [View Article][PubMed]
    [Google Scholar]
  40. Baird GS, Zacharias DA, Tsien RY. Biochemistry, mutagenesis, and oligomerization of DsRed, a red fluorescent protein from coral. Proc Natl Acad Sci USA 2000; 97:11984–11989 [View Article][PubMed]
    [Google Scholar]
  41. Sacchetti A, Subramaniam V, Jovin TM, Alberti S. Oligomerization of DsRed is required for the generation of a functional red fluorescent chromophore. FEBS Lett 2002; 525:13–19 [View Article][PubMed]
    [Google Scholar]
  42. Kost B, Spielhofer P, Chua NH. A GFP-mouse talin fusion protein labels plant actin filaments in vivo and visualizes the actin cytoskeleton in growing pollen tubes. Plant J 1998; 16:393–401 [View Article][PubMed]
    [Google Scholar]
  43. Du F, Ren H. Development and application of probes for labeling the actin cytoskeleton in living plant cells. Protoplasma 2011; 248:239–250 [View Article][PubMed]
    [Google Scholar]
  44. Dyachok J, Sparks JA, Liao F, Wang YS, Blancaflor EB. Fluorescent protein-based reporters of the actin cytoskeleton in living plant cells: fluorophore variant, actin binding domain, and promoter considerations. Cytoskeleton 2014; 71:311–327 [View Article][PubMed]
    [Google Scholar]
  45. Hofmann C, Niehl A, Sambade A, Steinmetz A, Heinlein M. Inhibition of Tobacco mosaic virus movement by expression of an actin-binding protein. Plant Physiol 2009; 149:1810–1823 [View Article][PubMed]
    [Google Scholar]
  46. Barlowe C. Signals for COPII-dependent export from the ER: what's the ticket out?. Trends Cell Biol 2003; 13:295–300 [View Article][PubMed]
    [Google Scholar]
  47. Nebenführ A. Vesicle traffic in the endomembrane system: a tale of COPs, Rabs and SNAREs. Curr Opin Plant Biol 2002; 5:507–512 [View Article][PubMed]
    [Google Scholar]
  48. Andreeva AV, Zheng H, Saint-Jore CM, Kutuzov MA, Evans DE et al. Organization of transport from endoplasmic reticulum to Golgi in higher plants. Biochem Soc Trans 2000; 28:505–512 [View Article][PubMed]
    [Google Scholar]
  49. Schepetilnikov MV, Manske U, Solovyev AG, Zamyatnin AA, Schiemann J et al. The hydrophobic segment of Potato virus X TGBp3 is a major determinant of the protein intracellular trafficking. J Gen Virol 2005; 86:2379–2391 [View Article][PubMed]
    [Google Scholar]
  50. Griffing LR. Networking in the endoplasmic reticulum. Biochem Soc Trans 2010; 38:747–753 [View Article][PubMed]
    [Google Scholar]
  51. Runions J, Brach T, Kühner S, Hawes C. Photoactivation of GFP reveals protein dynamics within the endoplasmic reticulum membrane. J Exp Bot 2006; 57:43–50 [View Article][PubMed]
    [Google Scholar]
  52. Sparkes I, Runions J, Hawes C, Griffing L. Movement and remodeling of the endoplasmic reticulum in nondividing cells of Tobacco leaves. Plant Cell 2009; 21:3937–3949 [View Article][PubMed]
    [Google Scholar]
  53. Griffing LR, Lin C, Perico C, White RR, Sparkes I. Plant ER geometry and dynamics: biophysical and cytoskeletal control during growth and biotic response. Protoplasma 2017; 254:43–56 [View Article][PubMed]
    [Google Scholar]
  54. Peremyslov VV, Prokhnevsky AI, Avisar D, Dolja VV. Two class XI myosins function in organelle trafficking and root hair development in Arabidopsis. Plant Physiol 2008; 146:1109–1116 [View Article][PubMed]
    [Google Scholar]
  55. Solovyev AG, Schiemann J, Morozov SY. Microscopic analysis of severe structural rearrangements of the plant endoplasmic reticulum and Golgi caused by overexpression of Poa semilatent virus movement protein. ScientificWorldJournal 2012; 2012:1–6 [View Article][PubMed]
    [Google Scholar]
  56. Avisar D, Prokhnevsky AI, Makarova KS, Koonin EV, Dolja VV. Myosin XI-K Is required for rapid trafficking of Golgi stacks, peroxisomes, and mitochondria in leaf cells of Nicotiana benthamiana. Plant Physiol 2008; 146:1098–1108 [View Article][PubMed]
    [Google Scholar]
  57. Stefano G, Hawes C, Brandizzi F. ER - the key to the highway. Curr Opin Plant Biol 2014; 22:30–38 [View Article][PubMed]
    [Google Scholar]
  58. Shemyakina EA, Solovyev AG, Leonova OG, Popenko VI, Schiemann J et al. The Role of Microtubule Association in Plasmodesmal Targeting of Potato mop-top virus Movement Protein TGBp1. Open Virol J 2011; 5:1–11 [View Article][PubMed]
    [Google Scholar]
  59. Solovyev AG, Minina EA, Makarova SS, Erokhina TN, Makarov VV et al. Subcellular localization and self-interaction of plant-specific Nt-4/1 protein. Biochimie 2013; 95:1360–1370 [View Article][PubMed]
    [Google Scholar]
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