The Plant Pathology Journal

The Korean Society of Plant Pathology (한국식물병리학회)
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Localization of Barley yellow dwarf virus Movement Protein Modulating Programmed Cell Death in Nicotiana benthamiana

  • Ju, Jiwon (Department of Agricultural Biology, College of Agriculture & Life Sciences, Chonbuk National University) ;
  • Kim, Kangmin (Division of Biotechnology, Chonbuk National University,) ;
  • Lee, Kui-Jae (Division of Biotechnology, Chonbuk National University,) ;
  • Lee, Wang Hu (Department of Agricultural Biology, College of Agriculture & Life Sciences, Chonbuk National University) ;
  • Ju, Ho-Jong (Department of Agricultural Biology, College of Agriculture & Life Sciences, Chonbuk National University)
  • Received : 2016.10.30
  • Accepted : 2016.11.16
  • Published : 2017.02.01
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Abstract

Barley yellow dwarf virus (BYDV) belongs to Luteovirus and is limited only at phloem related tissues. An open reading frame (ORF) 4 of BYDV codes for the movement protein (MP) of BYDV gating plasmodesmata (PD) to facilitate virus movement. Like other Luteoviruses, ORF 4 of BYDV is embedded in the ORF3 but expressed from the different reading frame in leaky scanning manner. Although MP is a very important protein for systemic infection of BYDV, there was a little information. In this study, MP was characterized in terms of subcellular localization and programmed cell death (PCD). Gene of MP or its mutant (ΔMP) was expressed by Agroinfiltration method. MP was clearly localized at the nucleus and the PD, but ΔMP which was deleted distal N-terminus of MP showed no localization to PD exhibited the different target with original MP. In addition to PD localization, MP appeared associated with small granules in cytoplasm whereas ΔMP did not. MP associated with PD and small granules induced PCD, but ΔMP showed no association with PD and small granules did not exhibit PCD. Based on this study, the distal N-terminal region within MP is seemingly responsible for the localization of PD and the induction small granules and PCD induction. These results suggest that subcellular localization of BYDV MP may modulate the PCD in Nicotiana benthamiana.

Keywords

References

  1. Agrios, G. N. 2006. Plant pathology. 5th ed. World Science, Seoul, Korea. 929 pp. (Trans., in Korean).
  2. Amoah, B. K., Wu, H., Sparks, C. and Jones, H. D. 2001. Factors influencing Agrobacterium-mediated transient expression of uidA in wheat inflorescence tissue. J. Exp. Bot. 52: 1135-1142. https://doi.org/10.1093/jexbot/52.358.1135
  3. Apel, K. and Hirt, H. 2004. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55:373-399. https://doi.org/10.1146/annurev.arplant.55.031903.141701
  4. Baker, C. J. and Orlandi, E. W. 1995. Active oxygen in plant pathogenesis. Annu. Rev. Phytopathol. 33:299-321. https://doi.org/10.1146/annurev.py.33.090195.001503
  5. Baulcombe, D. C., Gilbert, J., Goulden, M., Kohm, B. and Cruz, S. S. 1994. Molecular biology of resistance to Potato virus X in potato. Biochem. Soc. Symp. 60:207-218.
  6. Beachy, R. N. 1999. Coat-protein-mediated resistance to tobacco mosaic virus: discovery mechanisms and exploitation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 354:659-664. https://doi.org/10.1098/rstb.1999.0418
  7. Bendahmane, A., Kohn, B. A., Dedi, C. and Baulcombe, D. C. 1995. The coat protein of potato virus X is a strain-specific elicitor of Rx1-mediated virus resistance in potato. Plant J. 8: 933-941. https://doi.org/10.1046/j.1365-313X.1995.8060933.x
  8. Bendahmane, A., Querci, M., Kanyuka, K. and Baulcombe, D. C. 2000. Agrobacterium transient expression system as a tool for the isolation of disease resistance genes: application to the Rx2 locus in potato. Plant J. 21:73-81. https://doi.org/10.1046/j.1365-313x.2000.00654.x
  9. Bendahmane, M., Fitchen, J. H., Zhang, G. and Beachy, R. N. 1997. Studies of coat protein-mediated resistance to tobacco mosaic tobamovirus: correlation between assembly of mutant coat proteins and resistance. J. Virol. 71:7942-7950.
  10. Berzal-Herranz, A., de la Cruz, A., Tenllado, F., Diaz-Ruiz, J. R., Lopez, L., Sanz, A. I., Vaquero, C., Serra, M. T. and Garcia-Luque, I. 1995. The Capsicum L3 gene-mediated resistance against the tobamoviruses is elicited by the coat protein. Virology 209:498-505. https://doi.org/10.1006/viro.1995.1282
  11. Blokhina, O., Virolainen, E. and Fagerstedt, K. V. 2003. Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann. Bot. 91:179-194. https://doi.org/10.1093/aob/mcf118
  12. Carr, J. P., Lewsey, M. G. and Palukaitis, P. 2010. Signaling in induced resistance. Adv. Virus Res. 76:57-121.
  13. Chay, C. A., Gunasinge, U. B., Dinesh-Kumar, S. P., Miller, W. A. and Gray, S. M. 1996. Aphid transmission and systemic plant infection determinants of Barley yellow dwarf luteovirus-PAV are contained in the coat protein readthrough domain and 17-kDa protein, respectively. Virology 219:57-65. https://doi.org/10.1006/viro.1996.0222
  14. Chen, M. H., Sheng, J., Hind, G., Handa, A. K. and Citovsky, V. 2000. Interaction between the tobacco mosaic virus movement protein and host cell pectin methylesterases is required for viral cell-to-cell movement. EMBO J. 19:913-920. https://doi.org/10.1093/emboj/19.5.913
  15. Citovsky, V. and Zambryski, P. 1991. How do plant virus nucleic acids move through intercellular connections? BioEssays 13:373-379. https://doi.org/10.1002/bies.950130802
  16. Clark, W. G., Fitchen, J. H. and Beachy, R. N. 1995b. Studies of coat protein-mediated resistance to TMV. I. The PM2 assembly defective mutant confers resistance to TMV. Virology 208:485-491. https://doi.org/10.1006/viro.1995.1179
  17. Clark, W. G., Fitchen, J., Nejidat, A., Deom, C. M. and Beachy, R. N. 1995a. Studies of coat protein-mediated resistance to tobacco mosaic virus (TMV). II. Challenge by a mutant with altered virion surface does not overcome resistance conferred by TMV coat protein. J. Gen. Virol. 76:2613-2617. https://doi.org/10.1099/0022-1317-76-10-2613
  18. Cruz, S. S., Roberts, A. G., Prior, D. A., Chapman, S. and Oparka, K. J. 1998. Cell-to-cell and phloem-mediated transport of potato virus X: the role of virions. Plant Cell 10:495-510. https://doi.org/10.1105/tpc.10.4.495
  19. Culver, J. M. and Dawson, W. O. 1991. Tobacco mosaic virus elicitor coat protein genes produce a hypersensitive phenotype in transgenic Nicotiana sylvestris plants. Mol. Plant-Microbe Interact. 4:458-463. https://doi.org/10.1094/MPMI-4-458
  20. D'Arcy, C. J. and Domier, L. L. 2000. Barley yellow dwarf. Plant Health Instr. Online publication. doi: 10.1094/PHI-I-2000-1103-01.
  21. Dat, J., Vandenabeele, S., Vranova, E., van Montagu, M., Inze, D. and van Breusegem, F. 2000. Dual action of the active oxygen species during plant stress responses. Cell. Mol. Life Sci. 57:779-795. https://doi.org/10.1007/s000180050041
  22. Deom, C. M., He, X. Z., Beachy, R. N. and Weissinger, A. K. 1994. Influence of heterologous tobamovirus movement protein and chimeric-movement protein genes on cell-to-cell and long-distance movement. Virology 205:198-209. https://doi.org/10.1006/viro.1994.1635
  23. Deom, C. M., Lapidot, M. and Beachy, R. N. 1992. Plant virus movement proteins. Cell 69:221-224. https://doi.org/10.1016/0092-8674(92)90403-Y
  24. Ding, B. 1998. Intercellular protein trafficking through plasmodesmata. Plant Mol. Biol. 38:279-310. https://doi.org/10.1023/A:1006051703837
  25. Ding, B., Turgeon, R. and Parthasarathy, M. V. 1992. Substructure of freeze-substituted plasmodesmata. Protoplasma 169:28-41. https://doi.org/10.1007/BF01343367
  26. Dolja, V. V., Haldeman-Cahill, R., Montgomery, A. E., Vandenbosch, K. A. and Carrington, J. C. 1995. Capsid protein determinants involved in cell-to-cell and long distance movement of Tobacco etch potyvirus. Virology 206:1007-1016. https://doi.org/10.1006/viro.1995.1023
  27. Dong, X. 1998. SA, JA, ethylene, and disease resistance in plants. Curr. Opin. Plant Biol. 1:316-323. https://doi.org/10.1016/1369-5266(88)80053-0
  28. Fink, S. L. and Cookson, B. T. 2005. Apoptosis, pyroptosis, and necrosis: mechanistic description of dead and dying eukaryotic cells. Infect. Immun. 73:1907-1916. https://doi.org/10.1128/IAI.73.4.1907-1916.2005
  29. Gechev, T. S., Van Breusegem, F., Stone, J. M., Denev, I. and Laloi, C. 2006. Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. BioEssays 28:1091-1101. https://doi.org/10.1002/bies.20493
  30. Gill, S. S. and Tuteja, N. 2010. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 48:909-930. https://doi.org/10.1016/j.plaphy.2010.08.016
  31. Goodin, M. M., Dietzgen, R. G., Schichnes, D., Ruzin, S. and Jackson, A. O. 2002. pGD vectors: versatile tools for the expression of green and red fluorescent protein fusions in agroinfiltrated plant leaves. Plant J. 31:375-383. https://doi.org/10.1046/j.1365-313X.2002.01360.x
  32. Goodman, R. N. and Novacky, A. J. 1994. The hypersensitive reaction in plants to pathogens: a resistance phenomenon. American Phytopathological Society, St. Paul, MN, USA. 256 pp.
  33. Govrin, E. M. and Levine, A. 2000. The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr. Biol. 10:751-757. https://doi.org/10.1016/S0960-9822(00)00560-1
  34. Greenberg, J. T. 1997. Programmed cell death in plant-pathogen interactions. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48: 525-545. https://doi.org/10.1146/annurev.arplant.48.1.525
  35. Guan, L. M., Zhao, J. and Scandalios, J. G. 2000. Cis-elements and trans-factors that regulate expression of the maize Cat1 antioxidant gene in response to ABA and osmotic stress: $H_2O_2$ is the likely intermediary signaling molecule for the response. Plant J. 22:87-95. https://doi.org/10.1046/j.1365-313x.2000.00723.x
  36. Haupt, S., Stroganova, T., Ryabov, E., Kim, S. H., Fraser, G., Duncan, G., Mayo, M. A., Barker, H. and Taliansky, M. 2005. Nucleolar localization of potato leafroll virus capsid proteins. J. Gen. Virol. 86:2891-2896. https://doi.org/10.1099/vir.0.81101-0
  37. Hosein, F. N., Lennon, A. M. and Umaharan, P. 2012. Optimization of an Agrobacterium-mediated transient assay for gene expression studies in Anthurium andraeanum. J. Am. Soc. Hortic. Sci. 137:263-272.
  38. Itaya, A., Hickman, H., Bao, Y., Nelson, R. and Ding, B. 1997. Cell-to-cell trafficking of cucumber mosaic virus movement protein: green fluorescent protein fusion produced by biolistic gene bombardment in tobacco. Plant J. 12:1223-1230. https://doi.org/10.1046/j.1365-313X.1997.12051223.x
  39. Jiang, M. and Zhang, J. 2002. Water stress-induced abscisic acid accumulation triggers the increased generation of reactive oxygen species and up-regulates the activities of antioxidant enzymes in maize leaves. J. Exp. Bot. 53:2401-2410. https://doi.org/10.1093/jxb/erf090
  40. Ju, H. J., Brown, J. E., Ye, C. M. and Verchot-Lubicz, J. 2007. Mutations in the central domain of potato virus X TGBp2 eliminate granular vesicles and virus cell-to-cell trafficking. J. Virol. 81:1899-1911. https://doi.org/10.1128/JVI.02009-06
  41. Komatsu, K., Hashimoto, M., Ozeki, J., Yamaji, Y., Maejima, K., Senshu, H., Himeno, M., Okano, Y., Kagiwada, S. and Namba, S. 2010. Viral-induced systemic necrosis in plants involves both programmed cell death and the inhibition of viral multiplication, which are regulated by independent pathways. Mol. Plant-Microbe Interact. 23:283-293. https://doi.org/10.1094/MPMI-23-3-0283
  42. Kwon, S. Y., Jeong, Y. J., Lee, H. S., Kim, J. S., Cho, K. Y., Allen, R. D. and Kwak, S. S. 2002. Enhanced tolerances of transgenic tobacco plants expressing both superoxide dismutase and ascorbate peroxidase in chloroplasts against methyl viologen-mediated oxidative stress. Plant Cell Environ. 25:873-882. https://doi.org/10.1046/j.1365-3040.2002.00870.x
  43. Lazarowitz, S. G. and Beachy, R. N. 1999. Viral movement proteins as probes for intracellular and intercellular trafficking in plants. Plant Cell 11:535-548. https://doi.org/10.1105/tpc.11.4.535
  44. Levine, A., Tenhaken, R., Dixon, R. and Lamb, C. 1994. $H_2O_2$ from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583-593. https://doi.org/10.1016/0092-8674(94)90544-4
  45. Li, Y., Bao, Y. M., Wei, C. H., Kang, Z. S., Zhong, Y. W., Mao, P., Wu, G., Chen, Z. L., Schiemann, J. and Nelson, R. S. 2004. Rice dwarf phytoreovirus segment S6-encoded nonstructural protein has a cell-to-cell movement function. J. Virol. 78: 5382-5389. https://doi.org/10.1128/JVI.78.10.5382-5389.2004
  46. Lim, P. O., Ryu, J. S., Lee, H. J., Lee, U., Park, Y. S., Kwak, J. M., Choi, J. K. and Nam, H. G. 1997. Resistance to tobamoviruses in transgenic tobacco plants expressing the coat protein gene of pepper mild mottle virus (Korean isolate). Mol. Cells 7:313-319.
  47. Link, K., Vogel, F. and Sonnewald, U. 2011. PD Trafficking of potato leaf roll virus movement protein in arabidopsis depends on site-specific protein phosphorylation. Front. Plant Sci. 2:18.
  48. Lucas, W. J. 2006. Plant viral movement proteins: agents for cell-to-cell trafficking of viral genomes. Virology 344:169-184. https://doi.org/10.1016/j.virol.2005.09.026
  49. Lucas, W. J. and Lee, J. Y. 2004. Plasmodesmata as a supracellular control network in plants. Nat. Rev. Mol. Cell Biol. 5: 712-726. https://doi.org/10.1038/nrm1470
  50. May, M. J., Hammond-Kosack, K. E. and Jones, J. 1996. Involvement of reactive oxygen species, glutathione metabolism, and lipid peroxidation in the Cf-gene-dependent defense response of tomato cotyledons induced by race-specific elicitors of Cladosporium fulvum. Plant Physiol. 110:1367-1379. https://doi.org/10.1104/pp.110.4.1367
  51. Miller, W. A., Liu, S. and Beckett, R. 2002. Barley yellow dwarf virus: Luteoviridae or Tombusviridae? Mol. Plant Pathol. 3: 177-183. https://doi.org/10.1046/j.1364-3703.2002.00112.x
  52. Miller, W. A. and Rasochova, L. 1997. Barley yellow dwarf viruses. Annu. Rev. Phytopathol. 35:167-190. https://doi.org/10.1146/annurev.phyto.35.1.167
  53. Nass, P. H., Domier, L. L., Jakstys, B. P. and D'Arcy, C. J. 1998. In situ localization of barley yellow dwarf virus-PAV 17-kDa protein and nucleic acids in oats. Phytopathology 88:1031-1039. https://doi.org/10.1094/PHYTO.1998.88.10.1031
  54. Nass, P. H., Jakstys, B. P. and D'Arcy, C. J. 1995. In situ localization of barley yellow dwarf virus coat protein in oats. Phytopathology 85:556-560. https://doi.org/10.1094/Phyto-85-556
  55. Osbourn, J. K., Sarkar, S. and Wilson, T. M. 1990. Complementation of coat protein-defective TMV mutants in transgenic tobacco plants expressing TMV coat protein. Virology 179: 921-925. https://doi.org/10.1016/0042-6822(90)90169-R
  56. Rizhsky, L. Shulaev, V. and Mittler, R. 2004. Measuring programmed cell death in plants. In: Apoptosis methods and protocols, ed. by H. J. M. Brady, pp. 197-189. Humana Press, Totowa, NJ, USA.
  57. Sager, R. and Lee, J. Y. 2014. Plasmodesmata in integrated cell signalling: insights from development and environmental signals and stresses. J. Exp. Bot. 65:6337-6358. https://doi.org/10.1093/jxb/eru365
  58. Sambade, A., Brandner, K., Hofmann, C., Seemanpillai, M., Mutterer, J. and Heinlein, M. 2008. Transport of TMV movement protein particles associated with the targeting of RNA to plasmodesmata. Traffic 9:2073-2088. https://doi.org/10.1111/j.1600-0854.2008.00824.x
  59. Satoh, H., Matsuda, H., Kawamura, T., Isogai, M., Yoshikawa, N. and Takahashi, T. 2000. Intracellular distribution, cell-tocell trafficking and tubule-inducing activity of the 50 kDa movement protein of Apple chlorotic leaf spot virus fused to green fluorescent protein. J. Gen. Virol. 81:2085-2093. https://doi.org/10.1099/0022-1317-81-8-2085
  60. Schmitz, J., Stussi-Garaud, C., Tacke, E., Prufer, D., Rohde, W. and Rohfritsch, O. 1997. In situ localization of the putative movement protein (pr17) from potato leafroll luteovirus (PLRV) in infected and transgenic potato plants. Virology 235:311-322. https://doi.org/10.1006/viro.1997.8679
  61. Taliansky, M., Mayo, M. A. and Barker, H. 2003. Potato leafroll virus: a classic pathogen shows some new tricks. Mol. Plant Pathol. 4:81-89. https://doi.org/10.1046/j.1364-3703.2003.00153.x
  62. Tran, P. T., Chol, H., Kim, S. B., Lee, H. A., Choi, D. and Kim, K. H. 2014. A simple method for screening of plant NBS-LRR genes that confer a hypersensitive response to plant viruses and its application for screening candidate pepper genes against Pepper mottle virus. J. Virol. Methods 201:57-64. https://doi.org/10.1016/j.jviromet.2014.02.003
  63. van Breusegem, F. and Dat, J. F. 2006. Reactive oxygen species in plant cell death. Plant Physiol. 141:384-390. https://doi.org/10.1104/pp.106.078295
  64. van Doorn, W. G. and Woltering, E. J. 2005. Many ways to exit? Cell death categories in plants. Trends Plant Sci. 10:117-122. https://doi.org/10.1016/j.tplants.2005.01.006
  65. Vogel, F., Hofius, D. and Sonnewald, U. 2007. Intracellular trafficking of Potato leafroll virus movement protein in transgenic Arabidopsis. Traffic 8:1205-1214. https://doi.org/10.1111/j.1600-0854.2007.00608.x
  66. Wang, J. Y., Chay, C., Gildow, F. E. and Gray, S. M. 1995. Readthrough protein associated with virions of Barley yellow dwarf luteovirus and its potential role in regulating the efficiency of aphid transmission. Virology 20:954-962.
  67. Wong, H. L., Pinontoan, R., Hayashi, K., Tabata, R., Yaeno, T., Hasegawa, K., Kojima, C., Yoshioka, H., Iba, K., Kawasaki, T. and Shimamoto, K. 2007. Regulation of rice NADPH oxidase by binding of Rac GTPase to its N-terminal extension. Plant Cell 19:4022-4034. https://doi.org/10.1105/tpc.107.055624
  68. Wydro, M., Kozubek, E. and Lehmann, P. 2006. Optimization of transient Agrobacterium-mediated gene expression system in leaves of Nicotiana benthamiana. Acta Biochimica Polonica 53:289-298.
  69. Xia, Z., Cao, R., Sun, K. and Zhang, H. 2012. The movement protein of barley yellow dwarf virus-GAV self-interacts and forms homodimers in vitro and in vivo. Arch. Virol. 157: 1233-1239. https://doi.org/10.1007/s00705-012-1288-9
  70. Xiong, L., Schumaker, K. S. and Zhu, J. K. 2002. Cell signaling during cold, drought, and salt stress. Plant Cell 14 Suppl:S165-S183. https://doi.org/10.1105/tpc.000596
  71. Xiong, R., Wu, J., Zhou, Y. and Zhou, X. 2008. Identification of a movement protein of the tenuivirus rice stripe virus. J. Virol. 82:12304-12311. https://doi.org/10.1128/JVI.01696-08
  72. Xu, S. J., Banks, P. M., Dong, Y. S., Zhou, R. H. and Larkin, P. J. 1994. Evaluation of Chinese Triticeae for resistance to barley yellow dwarf virus (BYDV). Genet. Resour. Crop Evol. 41: 35-41. https://doi.org/10.1007/BF00051421
  73. Yang, Y., Ding, B., Baulcombe, D. C. and Verchot, J. 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. https://doi.org/10.1094/MPMI.2000.13.6.599
  74. Ye, C., Dickman, M. B., Whitham, S. A., Payton, M. and Verchot, J. 2011. The unfolded protein response is triggered by a plant viral movement protein. Plant Physiol. 156:741-755. https://doi.org/10.1104/pp.111.174110

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