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Actin Cytoskeleton and Golgi Involvement in Barley stripe mosaic virus Movement and Cell Wall Localization of Triple Gene Block Proteins

  • Lim, Hyoun-Sub (Department of Applied Biology, Chungnam National University) ;
  • Lee, Mi Yeon (Department of Plant and Microbial Biology, University of California) ;
  • Moon, Jae Sun (Green Bio Research Center, Korea Research Institute of Bioscience & Biotechnology) ;
  • Moon, Jung-Kyung (National Institute of Crop Science, Suwon, Rural Development Administration) ;
  • Yu, Yong-Man (Department of Applied Biology, Chungnam National University) ;
  • Cho, In Sook (National Institute of Horticultural & Herbal Science, Rural Development Administration) ;
  • Bae, Hanhong (School of Biotechnology, Yeungnam University) ;
  • DeBoer, Matt (Virology Department, Wageningen University) ;
  • Ju, Hojong (Department of Agricultural Biology, Chonbuk National University) ;
  • Hammond, John (USDA-ARS, US National Arboretum, Floral and Nursery Plants Research Unit) ;
  • Jackson, Andrew O. (Department of Plant and Microbial Biology, University of California)
  • Received : 2012.09.13
  • Accepted : 2012.10.10
  • Published : 2013.03.01

Abstract

Barley stripe mosaic virus (BSMV) induces massive actin filament thickening at the infection front of infected Nicotiana benthamiana leaves. To determine the mechanisms leading to actin remodeling, fluorescent protein fusions of the BSMV triple gene block (TGB) proteins were coexpressed in cells with the actin marker DsRed: Talin. TGB ectopic expression experiments revealed that TGB3 is a major elicitor of filament thickening, that TGB2 resulted in formation of intermediate DsRed:Talin filaments, and that TGB1 alone had no obvious effects on actin filament structure. Latrunculin B (LatB) treat-ments retarded BSMV cell-to-cell movement, disrupted actin filament organization, and dramatically decreased the proportion of paired TGB3 foci appearing at the cell wall (CW). BSMV infection of transgenic plants tagged with GFP-KDEL exhibited membrane proliferation and vesicle formation that were especially evident around the nucleus. Similar membrane proliferation occurred in plants expressing TGB2 and/or TGB3, and DsRed: Talin fluorescence in these plants colocalized with the ER vesicles. TGB3 also associated with the Golgi apparatus and overlapped with cortical vesicles appearing at the cell periphery. Brefeldin A treatments disrupted Golgi and also altered vesicles at the CW, but failed to interfere with TGB CW localization. Our results indicate that actin cytoskeleton interactions are important in BSMV cell-to-cell movement and for CW localization of TGB3.

Keywords

References

  1. Amari, K., Lerich, A., Schmitt-Keichinger, C., Dolja, V. V. and Ritzenthaler, C. 2011. Tubule-guided cell-to-cell movement of a plant virus requires class XI myosin motors. PLoS Pathol. e1002327.
  2. Baluska, F., Jasik, J., Edelmann, H. G., Salajova, T. and Volk-mann, D. 2001. Latrunculin B-induced plant dwarfism: Plant cell elongation is F-actin-dependent. Dev. Biol. 231:113−124.
  3. Boevink, P., Oparka, K., Santa Cruz, S., Martin, B., Betteridge, A. and Hawes, C. 1998. Stacks on tracks: the plant Golgi appara-tus traffics on an actin/ER network. Plant J. 15:441−447.
  4. Bragg, J. N., Lawrence, D. M. and Jackson, A. O. 2004. The N-terminal 85 amino acids of the barley stripe mosaic virus b pathogenesis protein contain three zinc-binding motifs. J. Virol. 78:7379−7391.
  5. Cowan, G. H., Lioliopoulou, F., Ziegler, A. and Torrance, L. 2002. Subcellular localisation, protein interactions, and RNA bind-ing of potato mop-top virus triple gene block proteins. Virol-ogy 298:106−115.
  6. daSilva, L. L., Snapp, E. L., Denecke, J., Lippincott-Schwartz, J., Hawes, C. and Brandizzi, F. 2004. Endoplasmic reticulum export sites and Golgi bodies behave as single mobile secre-tory units in plant cells. Plant Cell 16:1753−1771.
  7. Epel, B. L. 2009. Plant viruses spread by diffusion on ER-associ-ated movement-protein-rafts through plasmodesmata gated by viral induced host beta-1,3-glucanases. Semin Cell Dev. Biol. 20:1074−1081.
  8. Ferralli, J., Ashby, J., Fasler, M., Boyko, V. and Heinlein, M. 2006. Disruption of microtubule organization and centrosome function by expression of tobacco mosaic virus movement protein. J. Virol. 80:5807−5821.
  9. Gomord, V., Denmat, L. A., Fitchette-Laine, A. C., Satiat-Jeune-maitre, B., Hawes, C. and Faye, L. 1997. The C-terminal HDEL sequence is sufficient for retention of secretory proteins in the endoplasmic reticulum (ER) but promotes vacuolar targeting of proteins that escape the ER. Plant J. 11:313−325.
  10. Grangeon, R., Agbeci, M., Chen, J., Grondin, G., Zheng, H. and Laliberte, J. F. 2012. lmpact on the endoplasmic reticulum and Golgi apparatus of turnip mosaic virus infection. J. Virol. 86: 9255−9265.
  11. Harries, P. A., Park, J. W., Sasaki, N., Ballard, K. D., Maule, A. J. and Nelson, R. S. 2009. Differing requirements for actin and myosin by plant viruses for sustained intercellular movement. Proc. Natl. Acad. Sci. U S A. 106:17594−17599.
  12. Harries, P. A., Schoelz, J. E. and Nelson, R. S. 2010. Intracellular transport of viruses and their components: utilizing the cytosk-eleton and membrane highways. Mol. Plant-Microbe Interact. 23:1381−1393.
  13. Haupt, S., Cowan, G. H., Ziegler, A., Roberts, A. G., Oparka, K. J. and Torrance, L. 2005. Two plant-viral movement proteins traffic in the endocytic recycling pathway. Plant Cell 17:164−181. https://doi.org/10.1105/tpc.104.027821
  14. Hawes, C. and Satiat-Jeunemaitre, B. 2005. The plant Golgi appa-ratus--going with the flow. Biochim. Biophys. Acta. 1744:466−480.
  15. Jackson, A. O., Lim, H. S., Bragg, J., Ganesan, U. and Lee, M. Y. 2009. Hordeivirus replication, movement, and pathogenesis. Annu. Rev. Phytopathol. 47:385−422.
  16. Johansen, L. K. and Carrington, J. C. 2001. Silencing on the spot. Induction and suppression of RNA silencing in the Agrobacte-rium-mediated transient expression system. Plant Physiol. 126:930−938.
  17. Ju, H. J., Samuels, T. D., Wang, Y. S., Blancaflor, E., Payton, M., Mitra, R., Krishnamurthy, K., Nelson, R. S. and Verchot-Lubicz, J. 2005. The potato virus X TGBp2 movement protein associates with endoplasmic reticulum-derived vesicles during virus infection. Plant Physiol. 138:1877−1895.
  18. Kim, H., Park, M., Kim, S. J. and Hwang, I. 2005. Actin filaments play a critical role in vacuolar trafficking at the Golgi complex in plant cells. Plant Cell 17:888−902.
  19. Laliberte, J. F. and Sanfacon, H. 2010. Cellular remodeling during plant virus infection Annu. Rev. Phytopathol. 48:69−91.
  20. Lawrence, D. M. and Jackson, A. O. 2001a. Requirements for cell-to-cell movement of Barley stripe mosaic virus in mono-cot and dicot hosts. Mol. Plant Pathol. 2:65−75.
  21. Lawrence, D. M. and Jackson, A. O. 2001b. Interactions of the TGB1 protein during cell-to-cell movement of Barley stripe mosaic virus. J. Virol. 75:8712−8723.
  22. Lim, H. S., Bragg, J. N., Ganesan, U., Lawrence, D. M., Yu, J., Isogai, M., Hammond, J. and Jackson, A. O. 2008. Triple gene block protein interactions involved in movement of Barley stripe mosaic virus. J. Virol. 82:4991−5006.
  23. Lim, H. S., Bragg, J. N., Ganesan, U., Ruzin, S., Schichnes, D., Lee, M. Y., Vaira, A. M., Ryu, K. H., Hammond, J. and Jack-son, A. O. 2009. Subcellular localization of the barley stripe mosaic virus triple gene block proteins. J. Virol. 83:9432−9448.
  24. Lin, N. S. and Langenberg, W. G. 1985. Distribution of barley stripe mosaic virus protein in infected wheat root and shoot tips. J. Gen. Virol. 65:2217-2224.
  25. Lucas, W. J., Ham, B. K. and Kim, J. Y. 2009. Plasmodesmata -bridging the gap between neighboring plant cells. Trends Cell Biol. 19:495−503.
  26. Maule, A. J., Benitez-Alfonso, Y. and Faulkner, C. 2011. Plas-modesmata - membrane tunnels with attitude. Curr. Opin. Plant Biol. 14:683−690.
  27. Morozov, S. Y. and Solovyev, A. G. 2003. Triple gene block: Modular design of a multifunctional machine for plant virus movement. J. Gen.Virol. 84:1351−1366.
  28. Nebenführ, A., Ritzenthaler, C. and Robinson, D. G. 2002. Brefel-din A: deciphering an enigmatic inhibitor of secretion. Plant Physiol. 130:1102−1108.
  29. Niehl, A. and Heinlein, M. 2011. Cellular pathways for viral transport through plasmodesmata. Protoplasma 248:75−99. https://doi.org/10.1007/s00709-010-0246-1
  30. Ritzenthaler, C. 2011. Parallels and distinctions in the direct cell-to-cell spread of the plant and animal viruses. Curr. Opin. Virol. 1:403−409.
  31. Schepetilnikov, M. V., Solovyev, A. G., Gorshkova, E. N., Schie-mann, J., Prokhnevsky, A. I., Dolja, V. V. and Morozov, S. Y. 2008. Intracellular targeting of a hordeiviral membrane-span-ning movement protein: sequence requirements and involve-ment of an unconventional mechanism. J. Virol. 82:1284− 1293.
  32. Schoelz, J. E., Harries, P. A. and Nelson, R. S. 2011. Intracellular transport of plant viruses: finding the door out of the cell. Mol. Plant 4: 813−831.
  33. Scholthof, H. B. 2005. Plant virus transport: motions of functional equivalence. Trends Plant Sci.10:376−382. https://doi.org/10.1016/j.tplants.2005.07.002
  34. Semashko, M. A., González, I., Shaw, J., Leonova, O. G., Popenko, V. I., Taliansky, M. E., Canto, T. and Kalinina, N. O. 2012a. The extreme N-terminal domain of a hordeivirus TGB1 movement protein mediates its localization to the nucleolus and interaction with fibrillarin. Biochimie 94:1180− 1188.
  35. Semashko, M. A., Rakitina, D. V., González, I., Canto, T., Kalin-ina, N. O. and Taliansky, M. E. 2012b. Movement protein of hordeivirus interacts in vitro and in vivo with coilin, a major structural protein of Cajal bodies. Dokl. Biochem. Biophys. 442:57−60.
  36. Shemyakina, E. A., Solovyev, A. G., Leonova, O. G., Popenko, V. I., Schiemann, J. and Morozov, S. Y. 2011. The Role of Micro-tubule Association in Plasmodesmal Targeting of Potato mop-top virus Movement Protein TGBp1. Open Virol. J. 5:1−11.
  37. Solovyev, A. G., Schiemann, J. and Morozov, S. Y. 2012. Micro-scopic analysis of severe structural rearrangements of the plant endoplasmic reticulum and Golgi caused by overexpression of Poa semilatent virus movement protein. Scientific World Jour-nal 2012:416076.
  38. Su, S., Liu, Z., Chen, C., Zhang, Y., Wang, X., Zhu, L., Miao, L., Wang, X.-C. and Yuan, M. 2010. Cucumber mosaic virus movement protein severs actin filaments to increase the plas-modesmal size exclusion limit in tobacco. Plant Cell 4:1373−1387.
  39. Tilsner, J., Linnik, O., Wright, K. M., Bell, K., Roberts, A. G., Lacomme, C., Santa Cruz, S. and Oparka, K. J. 2012. The TGB1 movement protein of potato virus X re-organises actin and endomembranes into the 'X-body', a viral replication fac-tory. Plant Physiol. 158:1359−1370.
  40. Torrance, L., Wright, K. M., Crutzen, F., Cowan, G. H., Lukho-vitskaya, N. I., Bragard, C. and Savenkov, E. I. 2011. Unusual features of pomoviral RNA movement. Front. Microbiol. 2:259−266.
  41. Ueda, M., Schliwa, M. and Euteneuer, U. 1999. Unusual cen-trosome cycle in Dictyostelium: correlation of dynamic behavior and structural changes. Mol. Biol. Cell 10:151−160.
  42. Ueki, S. and Citovsky, V. 2011. To gate, or not to gate: regulatory mechanisms for intercellular protein transport and virus move-ment in plants. Mol. Plant 4:782−793. https://doi.org/10.1093/mp/ssr060
  43. Verchot, J. 2011. Wrapping membranes around plant virus infec-tion. Curr. Opin. Virol. 1:388−395. https://doi.org/10.1016/j.coviro.2011.09.009
  44. Verchot-Lubicz, J., Torrance, L., Solovyev, A. G., Morozov, S. Y., Jackson, A. O. and Gilmer, D. 2010. Varied movement strate-gies employed by triple gene block-encoding viruses. Mol. Plant- Microbe Interact. 23:1231−1247. https://doi.org/10.1094/MPMI-04-10-0086
  45. Vogel, F., Hofius, D. and Sonnewald, U. 2007. Intracellular traf-ficking of Potato leafroll virus movement protein in transgenic Arabidopsis. Traffic 8:1205−1214. https://doi.org/10.1111/j.1600-0854.2007.00608.x
  46. Wright, K. M., Wood, N. T., Roberts, A. G., Chapman, S., Boevink, P., Mackenzie, K. M. and Oparka, K. J. 2007. Target-ing of TMV movement protein to plasmodesmata requires the actin/ER network: evidence from FRAP. Traffic 8:21−31. https://doi.org/10.1111/j.1600-0854.2006.00510.x
  47. Wright, K. M. Cowan, G. H., Lukhovitskaya, N. I., Tilsner, J., Roberts, A. G., Savenkov, E. I. and Torrance, L. 2010. The N-terminal domain of PMTV TGB1 movement protein is required for nucleolar localization, microtubule association, and long distance movement. Mol. Plant-Microbe Interact. 11:1486−1497.
  48. Zamyatnin, A. A., Jr., Solovyev, A. G., Savenkov, E. I., Ger-mundsson, A., Sandgren, M., Valkonen, J. P. and Morozov, S. Y. 2004. 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. 17:921−930. https://doi.org/10.1094/MPMI.2004.17.8.921
  49. Zhou, H. and Jackson, A. O. 1996. Expression of the barley stripe mosaic virus RNA beta “triple gene block”. Virology 216: 367−379. https://doi.org/10.1006/viro.1996.0072

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