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The Plant Cellular Systems for Plant Virus Movement

  • Hong, Jin-Sung (Department of Applied Biology, College of Agriculture and Life Sciences, Kangwon National University) ;
  • Ju, Ho-Jong (Department of Agricultural Biology, College of Agricultural Life Science, Chonbuk National University)
  • Received : 2016.09.24
  • Accepted : 2016.11.13
  • Published : 2017.06.01

Abstract

Plasmodesmata (PDs) are specialized intercellular channels that facilitate the exchange of various molecules, including sugars, ribonucleoprotein complexes, transcription factors, and mRNA. Their diameters, estimated to be 2.5 nm in the neck region, are too small to transfer viruses or viral genomes. Tobacco mosaic virus and Potexviruses are the most extensively studied viruses. In viruses, the movement protein (MP) is responsible for the PD gating that allows the intercellular movement of viral genomes. Various host factors interact with MP to regulate complicated mechanisms related to PD gating. Virus replication and assembly occur in viral replication complex (VRC) with membrane association, especially in the endoplasmic reticulum. VRC have a highly organized structure and are highly regulated by interactions among the various host factors, proteins encoded by the viral genome, and the viral genome. Virus trafficking requires host machineries, such as the cytoskeleton and the secretory systems. MP facilitates the virus replication and movement process. Despite the current level of understanding of virus movement, there are still many unknown and complex interactions between virus replication and virus movement. While numerous studies have been conducted to understand plant viruses with regards to cell-to-cell movement and replication, there are still many knowledge gaps. To study these interactions, adequate research tools must be used such as molecular, and biochemical techniques. Without such tools, virologists will not be able to gain an accurate or detailed understanding of the virus infection process.

Keywords

References

  1. Aaziz, R., Dinant, S. and Epel, B. L. 2001. Plasmodesmata and plant cytoskeleton. Trends Plant Sci. 6:326-330. https://doi.org/10.1016/S1360-1385(01)01981-1
  2. Angell, S. M., Davies, C. and Baulcombe, D. C. 1996. Cell-tocell movement of Potato virus X is associated with a change in the size-exclusion limit of plasmodesmata in trichome cells of Nicotiana clevelandii. Virology 216:197-201. https://doi.org/10.1006/viro.1996.0046
  3. Ashby, J., Boutant, E., Seemanpillai, M., Groner, A., Sambade, A., Ritzenthaler, C. and Heinlein, M. 2006. Tobacco mosaic virus movement protein functions as a structural microtubule-associated protein. J. Virol. 80:8329-8344. https://doi.org/10.1128/JVI.00540-06
  4. Atabekov, J. G., Rodionova, N. P., Karpova, O. V., Kozlovsky, S. V., Novikov, V. K. and Arkhipenko, M. V. 2001. Translational activation of encapsidated Potato virus X RNA by coat protein phosphorylation. Virology 286:466-474. https://doi.org/10.1006/viro.2001.1013
  5. Atabekov, J. G., Rodionova, N. P., Karpova, O. V., Kozlovsky, S. V. and Poljakov, V. Y. 2000. The movement protein-triggered in situ conversion of Potato virus X virion RNA from a nontranslatable into a translatable form. Virology 271:259-263. https://doi.org/10.1006/viro.2000.0319
  6. Baluska, F., Cvrckova, F., Kendrick-Jone, J. and Volkmann, D. 2001. Sink plasmodesmata as gateways for phloem unloading. Myosin VIII and calreticulin as molecular determinants of sink strength? Plant Physiol. 126:39-46. https://doi.org/10.1104/pp.126.1.39
  7. Baluska, F., Samaj, J., Napier, R. and Volkmann, D. 1999. Maize calreticulin localizes preferentially to plasmodesmata in root apex. Plant J. 19:481-488. https://doi.org/10.1046/j.1365-313X.1999.00530.x
  8. Bamunusinghe, D., Hemenway, C. L., Nelson, R. S., Sanderfoot, A. A., Ye, C. M., Silva, M. A., Payton, M. and Verchot-Lubicz, J. 2009. Analysis of Potato virus X replicase and TGBp3 subcellular locations. Virology 393:272-285. https://doi.org/10.1016/j.virol.2009.08.002
  9. Bamunusinghe, D., Seo, J. K. and Rao, A. L. 2011. Subcellular localization and rearrangement of endoplasmic reticulum by Brome mosaic virus capsid protein. J. Virol. 85:2953-2963. https://doi.org/10.1128/JVI.02020-10
  10. Bayer, E., Thomas, C. L. and Maule, A. J. 2004. Plasmodesmata in Arabidopsis thaliana suspension cells. Protoplasma 223:93-102.
  11. Bayne, E. H., Rakitina, D. V., Morozov, S. Y. and Baulcombe, D. C. 2005. Cell-to-cell movement of Potato potexvirus X is dependent on suppression of RNA silencing. Plant J. 44:471-482. https://doi.org/10.1111/j.1365-313X.2005.02539.x
  12. Beauchemin, C., Boutet, N. and Laliberte, J. F. 2007. Visualization of the interaction between the precursors of VPg, the viral protein linked to the genome of Turnip mosaic virus, and the translation eukaryotic initiation factor iso 4E in planta. J. Virol. 81:775-782. https://doi.org/10.1128/JVI.01277-06
  13. Beauchemin, C. and Laliberte, J. F. 2007. The poly(A) binding protein is internalized in virus-induced vesicles or redistributed to the nucleolus during turnip mosaic virus infection. J. Virol. 81:10905-10913. https://doi.org/10.1128/JVI.01243-07
  14. Beffa, R. S., Hofer, R. M., Thomas, M. and Meins, F., Jr. 1996. Decreased susceptibility to viral disease of [beta]-1,3-glucanase-deficient plants generated by antisense transformation. Plant Cell 8:1001-1011.
  15. Blackman, L. M., Harper, J. D. and Overall, R. L. 1999. Localization of a centrin-like protein to higher plant plasmodesmata. Eur. J. Cell Biol. 78:297-304. https://doi.org/10.1016/S0171-9335(99)80063-6
  16. Blackman, L. M. and Overall, R. L. 1998. Immunolocalisation of the cytoskeleton to plasmodesmata of Chara corallina. Plant J. 14:733-741. https://doi.org/10.1046/j.1365-313x.1998.00161.x
  17. Bolwell, G. P., Bindschedler, L. V., Blee, K. A., Butt, V. S., Davies, D. R., Gardner, S. L., Gerrish, C. and Minibayeva, F. 2002. The apoplastic oxidative burst in response to biotic stress in plants: a three-component system. J. Exp. Bot. 53:1367-1376.
  18. Bombarely, A., Rosli, H. G., Vrebalov, J., Moffett, P., Mueller, L. A. and Martin, G. B. 2012. A draft genome sequence of Nicotiana benthamiana to enhance molecular plant-microbe biology research. Mol. Plant-Microbe Interact. 25:1523-1530. https://doi.org/10.1094/MPMI-06-12-0148-TA
  19. Boyko, V., Ferralli, J., Ashby, J., Schellenbaum, P. and Heinlein, M. 2000a. Function of microtubules in intercellular transport of plant virus RNA. Nat. Cell Biol. 2:826-832. https://doi.org/10.1038/35041072
  20. Boyko, V., Ferralli, J. and Heinlein, M. 2000b. 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. https://doi.org/10.1046/j.1365-313x.2000.00740.x
  21. Boyko, V., Hu, Q., Seemanpillai, M, Ashby, J. and Heinlein, M. 2007. Validation of microtubule-associated Tobacco mosaic virus RNA movement and involvement of microtubulealigned particle trafficking. Plant J. 51:589-603. https://doi.org/10.1111/j.1365-313X.2007.03163.x
  22. Brandner, K., Sambade, A., Boutant, E., Didier, P., Mély, Y., Ritzenthaler, C. and Heinlein, M. 2008. Tobacco mosaic virus movement protein interacts with green fluorescent protein-tagged microtubule end-binding protein 1. Plant Physiol. 147:611-623. https://doi.org/10.1104/pp.108.117481
  23. Brill, L. M., Dechongkit, S., DeLaBarre, B., Stroebel, J., Beachy, R. N. and Yeager, M. 2004. Dimerization of recombinant tobacco mosaic virus movement protein. J. Virol. 78:3372-3377. https://doi.org/10.1128/JVI.78.5.3372-3377.2004
  24. Brill, L. M., Nunn, R. S., Kahn, T. W., Yeager, M. and Beachy, R. N. 2000. Recombinant tobacco mosaic virus movement protein is an RNA-binding, alpha-helical membrane protein. Proc. Natl. Acad. Sci. U. S. A. 97:7112-7117. https://doi.org/10.1073/pnas.130187897
  25. Bucher, G. L., Tarina, C., Heinlein, M., Di Serio, F., Meins, F., Jr. and Iglesias, V. A. 2001. Local expression of enzymatically active class I beta-1, 3-glucanase enhances symptoms of TMV infection in tobacco. Plant J. 28:361-369. https://doi.org/10.1046/j.1365-313X.2001.01181.x
  26. Carette, J. E., Stuiver, M., Van Lent, J., Wellink, J. and Van Kammen, A. 2000. Cowpea mosaic virus infection induces a massive proliferation of endoplasmic reticulum but not Golgi membranes and is dependent on de novo membrane synthesis. J. Virol. 74:6556-6563. https://doi.org/10.1128/JVI.74.14.6556-6563.2000
  27. Carette, J. E., van Lent, J., MacFarlane, S. A., Wellink, J. and van Kammen, A. 2002. Cowpea mosaic virus 32- and 60-kilodalton replication proteins target and change the morphology of endoplasmic reticulum membranes. J. Virol. 76:6293-6301. https://doi.org/10.1128/JVI.76.12.6293-6301.2002
  28. Chen, M. H., Tian, G. W., Gafni, Y. and Citovsky, V. 2005. Effects of calreticulin on viral cell-to-cell movement. Plant Physiol. 138:1866-1876. https://doi.org/10.1104/pp.105.064386
  29. Chen, T., Wang, X., von Wangenheim, D., Zheng, M., Samaj, J., Ji, W. and Lin, J. 2012. Probing and tracking organelles in living plant cells. Protoplasma 249 Suppl 2:S157-S167. https://doi.org/10.1007/s00709-011-0364-4
  30. Cho, S. Y., Cho, W. K., Choi, H. S. and Kim, K. H. 2012. Cisacting element (SL1) of Potato virus X controls viral movement by interacting with the NbMPB2Cb and viral proteins. Virology 427:166-176. https://doi.org/10.1016/j.virol.2012.02.005
  31. Chrispeels, M. J. 1991. Sorting of proteins in the secretory system. Annu. Rev. Plant. Physiol. Plant Mol. Biol. 42:21-53. https://doi.org/10.1146/annurev.pp.42.060191.000321
  32. Christensen, N., Tilsner, J., Bell, K., Hammann, P., Parton, R., Lacomme, C. and Oparka, K. 2009. The 5' cap of Tobacco mosaic virus (TMV) is required for virion attachment to the actin/endoplasmic reticulum network during early infection. Traffic 10:536-551. https://doi.org/10.1111/j.1600-0854.2009.00889.x
  33. Citovsky, V., Wong, M. L., Shaw, A. L., Prasad, B. V. and Zambryski, P. 1992. Visualization and characterization of tobacco mosaic virus movement protein binding to single-stranded nucleic acids. Plant Cell 4:397-411. https://doi.org/10.1105/tpc.4.4.397
  34. Cotton, S., Grangeon, R., Thivierge, K., Mathieu, I., Ide, C., Wei, T., Wang, A. and Laliberte, J. F. 2009. Turnip mosaic virus RNA replication complex vesicles are mobile, align with microfilaments, and are each derived from a single viral genome. J. Virol. 83:10460-10471. https://doi.org/10.1128/JVI.00819-09
  35. Crawford, K. M. and Zambryski, P. C. 2000. Subcellular localization determines the availability of non-targeted proteins to plasmodesmatal transport. Curr. Biol. 10:1032-1040. https://doi.org/10.1016/S0960-9822(00)00657-6
  36. Curin, M., Ojangu, E. L., Trutnyeva, K., Ilau, B., Truve, E. and Waigmann, E. 2007. MPB2C, a microtubule-associated plant factor, is required for microtubular accumulation of tobacco mosaic virus movement protein in plants. Plant Physiol. 143:801-811.
  37. de Castro, I. F., Volonte, L. and Risco, C. 2013. Virus factories: biogenesis and structural design. Cell. Microbiol. 15:24-34. https://doi.org/10.1111/cmi.12029
  38. De Storme, N. and Geelen, D. 2014. Callose homeostasis at plasmodesmata: molecular regulators and developmental relevance. Front. Plant Sci. 5:138.
  39. Demchenko, K. N., Voitsekhovskaja, O. V. and Pawlowski, K. 2014. Plasmodesmata without callose and calreticulin in higher plants: open channels for fast symplastic transport? Front. Plant Sci. 5:74.
  40. Deom, C. M., Oliver, M. J. and Beachy, R. N. 1987. The 30-kilodalton gene product of Tobacco mosaic virus potentiates virus movement. Science 237:389-394. https://doi.org/10.1126/science.237.4813.389
  41. Diaz, A. and Ahlquist, P. 2012. Role of host reticulon proteins in rearranging membranes for positive-strand RNA virus replication. Curr. Opin. Microbiol. 15:519-524. https://doi.org/10.1016/j.mib.2012.04.007
  42. Diaz, A. and Wang, X. 2014. Bromovirus-induced remodeling of host membranes during viral RNA replication. Curr. Opin. Virol. 9:104-110. https://doi.org/10.1016/j.coviro.2014.09.018
  43. Ding, B. 1998. Intercellular protein trafficking through plasmodesmata. Plant Mol. Biol. 38:279-310. https://doi.org/10.1023/A:1006051703837
  44. Ding, B., Turgeon, R. and Parthasarathy, M. V. 1992. Substructure of freeze substituted plasmodesmata. Protoplasma 169:28-41. https://doi.org/10.1007/BF01343367
  45. Dolja, V. V., McBride, H. J. and Carrington, J. C. 1992. Tagging of plant potyvirus replication and movement by insertion of beta-glucuronidase into the viral polyprotein. Proc. Natl. Acad. Sci. U. S. A. 89:10208-10212. https://doi.org/10.1073/pnas.89.21.10208
  46. dos Reis Figueira, A., Golem, S., Goregaoker, S. P. and Culver, J. N. 2002. A nuclear localization signal and a membrane association domain contribute to the cellular localization of the Tobacco mosaic virus 126-kDa replicase protein. Virology 301:81-89. https://doi.org/10.1006/viro.2002.1560
  47. 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. https://doi.org/10.1128/JVI.00254-06
  48. Fridborg, I., Grainger, J., Page, A., Coleman, M., Findlay, K. and Angell, S. 2003. TIP, a novel host factor linking callose degradation with the cell-to-cell movement of Potato virus X. Mol. Plant-Microbe Interact. 16:132-140. https://doi.org/10.1094/MPMI.2003.16.2.132
  49. Fujiki, M., Kawakami, S., Kim, R. W. and Beachy, R. N. 2006. Domains of Tobacco mosaic virus movement protein essential for its membrane association. J. Gen. Virol. 87:2699-2707. https://doi.org/10.1099/vir.0.81936-0
  50. Genoves, A., Navarro, J. A. and Pallas, V. 2010. The intra- and intercellular movement of Melon necrotic spot virus (MNSV) depends on an active secretory pathway. Mol. Plant-Microbe Interact. 23:263-272. https://doi.org/10.1094/MPMI-23-3-0263
  51. Gergerich, R. C. and Dolja, V. V. 2006. Introduction to plant viruses, the invisible foe. Plant Health Instr. Online publication. doi: 10.1094/PHI-I-2006-0414-01.
  52. Gillespie, T., Boevink, P., Haupt, S., Roberts, A. G., Toth, R., Valentine, T., Chapman, S. and Oparka, K. J. 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. https://doi.org/10.1105/tpc.002303
  53. Goodin, M. M., Zaitlin, D., Naidu, R. A. and Lommel, S. A. 2008. Nicotiana benthamiana: its history and future as a model for plant-pathogen interactions. Mol. Plant-Microbe Interact. 21:1015-1026. https://doi.org/10.1094/MPMI-21-8-1015
  54. Grangeon, R., Agbeci, M., Chen, J., Grondin, G., Zheng, H. and Laliberte, J. F. 2012a. Impact on the endoplasmic reticulum and Golgi apparatus of Turnip mosaic virus infection. J. Virol. 86:9255-9265. https://doi.org/10.1128/JVI.01146-12
  55. Grangeon, R., Jiang, J. and Laliberte, J. F. 2012b. Host endomembrane recruitment for plant RNA virus replication. Curr. Opin. Virol. 2:683-690. https://doi.org/10.1016/j.coviro.2012.10.003
  56. Grangeon, R., Jiang, J., Wan, J., Agbeci, M., Zheng, H. and Laliberte, J. F. 2013. $6K_2$-induced vesicles can move cell to cell during turnip mosaic virus infection. Front. Microbiol. 4:351.
  57. Guenoune-Gelbart, D., Elbaum, M., Sagi, G., Levy, A. and Epel, B. L. 2008. Tobacco mosaic virus (TMV) replicase and movement protein function synergistically in facilitating TMV spread by lateral diffusion in the plasmodesmal desmotubule of Nicotiana benthamiana. Mol. Plant-Microbe Interact. 21:335-345. https://doi.org/10.1094/MPMI-21-3-0335
  58. Hagiwara, Y., Komoda, K., Yamanaka, T., Tamai, A., Meshi, T., Funada, R., Tsuchiya, T., Naito, S. and Ishikawa, M. 2003. Subcellular localization of host and viral proteins associated with tobamovirus RNA replication. EMBO J. 22:344-353. https://doi.org/10.1093/emboj/cdg033
  59. Haikonen, T., Rajamäki, M. L. and Valkonen, J. P. 2013. Interaction of the microtubule-associated host protein HIP2 with viral helper component proteinase is important in infection with Potato virus A. Mol. Plant-Microbe Interact. 26:734-744. https://doi.org/10.1094/MPMI-01-13-0023-R
  60. Hanton, S. L., Bortolotti, L. E., Renna, L., Stefano, G. and Brandizzi, F. 2005. Crossing the divide--transport between the endoplasmic reticulum and Golgi apparatus in plants. Traffic 6:267-277. https://doi.org/10.1111/j.1600-0854.2005.00278.x
  61. Harries, P. A., Palanichelvam, K., Yu, W., Schoelz, J. E. and Nelson, R. S. 2009a. The Cauliflower mosaic virus protein P6 forms motile inclusions that traffic along actin microfilaments and stabilize microtubules. Plant Physiol. 149:1005-1016.
  62. Harries, P. A., Park, J. W., Sasaki, N., Ballard, K. D., Maule, A. J. and Nelson, R. S. 2009b. Differing requirements for actin and myosin by plant viruses for sustained intercellular movement. Proc. Natl. Acad. Sci. U. S. A. 106:17594-17599. https://doi.org/10.1073/pnas.0909239106
  63. Harries, P. A., Schoelz, J. E. and Nelson, R. S. 2010. Intracellular transport of viruses and their components: utilizing the cytoskeleton and membrane highways. Mol. Plant-Microbe Interact. 23:1381-1393. https://doi.org/10.1094/MPMI-05-10-0121
  64. Heinlein, M. 2015. Plant virus replication and movement. Virology 479-480:657-671. https://doi.org/10.1016/j.virol.2015.01.025
  65. Heinlein, M. and Epel, B. L. 2004. Macromolecular transport and signaling through plasmodesmata. Int. Rev. Cytol. 235:93-164.
  66. Heinlein, M., Epel, B. L., Padgett, H. S. and Beachy, R. N. 1995. Interaction of tobamovirus movement proteins with the plant cytoskeleton. Science 270:1983-1985. https://doi.org/10.1126/science.270.5244.1983
  67. Heinlein, M., Padgett, H. S., Gens, J. S., Pickard, B. G., Casper, S. J., Epel, B. L. and Beachy, R. N. 1998. Changing patterns of localization of the Tobacco mosaic virus movement protein and replicase to the endoplasmic reticulum and microtubules during infection. Plant Cell 10:1107-1120. https://doi.org/10.1105/tpc.10.7.1107
  68. Hirashima, K. and Watanabe, Y. 2003. RNA helicase domain of tobamovirus replicase executes cell-to-cell movement possibly through collaboration with its nonconserved region. J. Virol. 77:12357-12362. https://doi.org/10.1128/JVI.77.22.12357-12362.2003
  69. Hofmann, C., Niehl, A., Sambade, A., Steinmetz, A. and Heinlein, M. 2009. Inhibition of tobacco mosaic virus movement by expression of an actin-binding protein. Plant Physiol. 149:1810-1823. https://doi.org/10.1104/pp.108.133827
  70. Howard, A. R., Heppler, M. L., Ju, H. J., Krishnamurthy, K., Payton, M. E. and Verchot-Lubicz, J. 2004. Potato virus X TGBp1 induces plasmodesmata gating and moves between cells in several host species whereas CP moves only in N. benthamiana leaves. Virology 328:185-197. https://doi.org/10.1016/j.virol.2004.06.039
  71. Hull, R. 2009. Comparative plant virology. 2nd ed. Academic Press, Burlington, MA, USA. 376 pp.
  72. Hwang, Y. T., McCartney, A. W., Gidda, S. K. and Mullen, R. T. 2008. Localization of the Carnation Italian ringspot virus replication protein p36 to the mitochondrial outer membrane is mediated by an internal targeting signal and the TOM complex. BMC Cell Biol. 9:54. https://doi.org/10.1186/1471-2121-9-54
  73. Iglesias, V. A. and Meins, F., Jr. 2000. Movement of plant viruses is delayed in a beta-1,3-glucanase-deficient mutant showing a reduced plasmodesmatal size exclusion limit and enhanced callose deposition. Plant J. 21:157-166. https://doi.org/10.1046/j.1365-313x.2000.00658.x
  74. Imlau, A., Truernit, E. and Sauer, N. 1999. Cell-to-cell and long-distance trafficking of the green fluorescent protein in the phloem and symplastic unloading of the protein into sink tissues. Plant Cell 11:309-322. https://doi.org/10.1105/tpc.11.3.309
  75. Ishikawa, M., Naito, S. and Ohno, T. 1993. Effects of the tom1 mutation of Arabidopsis thaliana on the multiplication of tobacco mosaic virus RNA in protoplasts. J. Virol. 67:5328-5338.
  76. Itaya, A., Liang, G., Woo, Y. M., Nelson, R. S. and Ding, B. 2000. Nonspecific intercellular protein trafficking probed by green fluorescent protein in plants. Protoplasma 213:165-175. https://doi.org/10.1007/BF01282154
  77. Itaya, A., Woo, Y. M., Masuta, C., Bao, Y., Nelson, R. S. and Ding, B. 1998. Developmental regulation of intercellular protein trafficking through plasmodesmata in tobacco leaf epidermis. Plant Physiol. 118:373-385. https://doi.org/10.1104/pp.118.2.373
  78. 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. https://doi.org/10.1104/pp.105.066019
  79. Kachar, B. 1985. Direct visualization of organelle movement along actin filaments dissociated from characean algae. Science 227:1355-1357. https://doi.org/10.1126/science.4038817
  80. Kalinina, N. O., Fedorkin, O. N., Samuilova, O. V., Maiss, E., Korpela, T., Morozov, S. Yu. and Atabekov, J. G. 1996. Expression and biochemical analyses of the recombinant potato virus X 25K movement protein. FEBS Lett. 397:75-78. https://doi.org/10.1016/S0014-5793(96)01138-6
  81. Kalinina, N. O., Rakitina, D. V., Solovyev, A. G., Schiemann, J. and Morozov, S. Y. 2002. RNA helicase activity of the plant virus movement proteins encoded by the first gene of the triple gene block. Virology 296:321-329. https://doi.org/10.1006/viro.2001.1328
  82. Karpova, O. V., Rodionova, N. P., Ivanov, K. I., Kozlovsky, S. V., Dorokhov, Y. L. and Atabekov, J. G. 1999. Phosphorylation of tobacco mosaic virus movement protein abolishes its translation repressing ability. Virology 261:20-24. https://doi.org/10.1006/viro.1999.9842
  83. Karpova, O. V., Zayakina, O. V., Arkhipenko, M. V., Sheval, E. V., Kiselyova, O. I., Poljakov, V. Y., Yaminsky, I. V., Rodionova, N. P. and Atabekov, J. G. 2006. Potato virus X RNAmediated assembly of single-tailed ternary 'coat protein--RNA--movement protein' complexes. J. Gen. Virol. 87:2731-2740. https://doi.org/10.1099/vir.0.81993-0
  84. Kathiria, P., Sidler, C., Golubov, A., Kalischuk, M., Kawchuk, L. M. and Kovalchuk, I. 2010. Tobacco mosaic virus infection results in an increase in recombination frequency and resistance to viral, bacterial, and fungal pathogens in the progeny of infected tobacco plants. Plant Physiol. 153:1859-1870. https://doi.org/10.1104/pp.110.157263
  85. Kawakami, S., Watanabe, Y. and Beachy, R. N. 2004. Tobacco mosaic virus infection spreads cell to cell as intact replication complexes. Proc. Natl. Acad. Sci. U. S. A. 101:6291-6296. https://doi.org/10.1073/pnas.0401221101
  86. Kiselyova, O. I., Yaminsky, I. V., Karpova, O. V., Rodionova, N. P., Kozlovsky, S. V., Arkhipenko, M. V. and Atabekov, J. G. 2003. AFM study of Potato virus X disassembly induced by movement protein. J. Mol. Biol. 332:321-325. https://doi.org/10.1016/S0022-2836(03)00835-0
  87. Kopek, B. G., Perkins, G., Miller, D. J., Ellisman, M. H. and Ahlquist, P. 2007. Three-dimensional analysis of a viral RNA replication complex reveals a virus-induced mini-organelle. PLoS Biol. 5:e220. https://doi.org/10.1371/journal.pbio.0050220
  88. Kotlizky, G., Katz, A., van der Laak, J., Boyko, V., Lapidot, M., Beachy, R. N., Heinlein, M. and Epel, B. L. 2001. A dysfunctional movement protein of Tobacco mosaic virus interferes with targeting of wild-type movement protein to microtubules. Mol. Plant-Microbe Interact. 14:895-904. https://doi.org/10.1094/MPMI.2001.14.7.895
  89. Kragler, F., Curin, M., Trutnyeva, K., Gansch, A. and Waigmann, E. 2003. MPB2C, a microtubule-associated plant protein binds to and interferes with cell-to-cell transport of tobacco mosaic virus movement protein. Plant Physiol. 132:1870-1883. https://doi.org/10.1104/pp.103.022269
  90. Krasavina, M. S., Malyshenko, S. I., Raldugina, G. N., Burmistrova, N. A. and Nosov, A. V. 2002. Can salicylic acid affect the intercellular transport of the tobacco mosaic virus by changing plasmodesmal permeability? Russ. J. Plant Physiol. 49:61-67. https://doi.org/10.1023/A:1013760227650
  91. Krishnamurthy, K., Heppler, M., Mitra, R., Blancaflor, E., Payton, M., Nelson, R. S. and Verchot-Lubicz, J. 2003. The Potato virus X TGBp3 protein associates with the ER network for virus cell-to-cell movement. Virology 309:135-151. https://doi.org/10.1016/S0042-6822(02)00102-2
  92. Laliberté, J. F. and Sanfaçon, H. 2010. Cellular remodeling during plant virus infection. Annu. Rev. Phytopathol. 48:69-91. https://doi.org/10.1146/annurev-phyto-073009-114239
  93. Laliberte, J. F. and Zheng, H. 2014. Viral manipulation of plant host membranes. Annu. Rev. Virol. 1:237-259. https://doi.org/10.1146/annurev-virology-031413-085532
  94. Laporte, C., Vetter, G., Loudes, A. M., Robinson, D. G., Hillmer, S., Stussi-Garaud, C. and Ritzenthaler, C. 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. https://doi.org/10.1105/tpc.013896
  95. Lee, J. Y., Yoo, B. C., Rojas, M. R., Gomez-Ospina, N., Staehelin, L. A. and Lucas, W. J. 2003. Selective trafficking of noncell-autonomous proteins mediated by NtNCAPP1. Science 299:392-396. https://doi.org/10.1126/science.1077813
  96. Leshchiner, A. D., Solovyev, A. G., Morozov, S. Y. and Kalinina, N. O. 2006. A minimal region in the NTPase/helicase domain of the TGBp1 plant virus movement protein is responsible for ATPase activity and cooperative RNA binding. J. Gen. Virol. 87:3087-3095. https://doi.org/10.1099/vir.0.81971-0
  97. Li, W., Zhao, Y., Liu, C., Yao, G., Wu, S., Hou, C., Zhang, M. and Wang, D. 2012. Callose deposition at plasmodesmata is a critical factor in restricting the cell-to-cell movement of Soybean mosaic virus. Plant Cell Rep. 31:905-916. https://doi.org/10.1007/s00299-011-1211-y
  98. Liu, C. and Nelson, R. S. 2013. The cell biology of Tobacco mosaic virus replication and movement. Front. Plant Sci. 4:12.
  99. Liu, J. Z., Blancaflor, E. B. and Nelson, R. S. 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. https://doi.org/10.1104/pp.105.065722
  100. Lough, T. J., Lee, R. H., Emerson, S. J., Forster, R. L. and Lucas, W. J. 2006. Functional analysis of the 5' untranslated region of potexvirus RNA reveals a role in viral replication and cell-to-cell movement. Virology 351:455-465. https://doi.org/10.1016/j.virol.2006.03.043
  101. Lough, T. J., Netzler, N. E., Emerson, S. J., Sutherland, P., Carr, F., Beck, D. L., Lucas, W. J. and Forster, R. L. 2000. Cell-tocell movement of Potexviruses: evidence for a ribonucleoprotein complex involving the coat protein and first triple gene block protein. Mol. Plant-Microbe Interact. 13:962-974. https://doi.org/10.1094/MPMI.2000.13.9.962
  102. Lough, T. J., Shash, K., Xoconostle-Cazares, B., Hofstra, K. R., Beck, D. L., Balmori, E., Forster, R. L. S. and Lucas, W. J. 1998. Molecular dissection of the mechanism by which potexvirus triple gene block proteins mediate cell-to-cell transport of infectious RNA. Mol. Plant-Microbe Interact. 11:801-814. https://doi.org/10.1094/MPMI.1998.11.8.801
  103. Lucas, W. J. 1995. Plasmodesmata: intercellular channels for macromolecular transport in plants. Curr. Opin. Cell. Biol. 7:673-680. https://doi.org/10.1016/0955-0674(95)80109-X
  104. 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
  105. Lucas, W. J., Ding, B. and van der Schoot, C. 1993. Plasmodesmata and the supracellular nature of plants. New Phytol. 125:435-476. https://doi.org/10.1111/j.1469-8137.1993.tb03897.x
  106. 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
  107. Lukashina, E., Badun, G., Fedorova, N., Ksenofontov, A., Nemykh, M., Serebryakova, M., Mukhamedzhanova, A., Karpova, O., Rodionova, N., Baratova, L. and Dobrov, E. 2009. Tritium planigraphy study of structural alterations in the coat protein of Potato virus X induced by binding of its triple gene block 1 protein to virions. FEBS J. 276:7006-7015. https://doi.org/10.1111/j.1742-4658.2009.07408.x
  108. Martindale, V. E. and Salisbury, J. L. 1990. Phosphorylation of algal centrin is rapidly responsive to changes in the external milieu. J. Cell Sci. 96:395-402.
  109. Martiniere, A., Gargani, D., Uzest, M., Lautredou, N., Blanc, S. and Drucker, M. 2009. A role for plant microtubules in the formation of transmission-specific inclusion bodies of Cauliflower mosaic virus. Plant J. 58:135-146. https://doi.org/10.1111/j.1365-313X.2008.03768.x
  110. Mas, P. and Beachy, R. N. 1999. Replication of Tobacco mosaic virus on endoplasmic reticulum and role of the cytoskeleton and virus movement protein in intracellular distribution of viral RNA. J. Cell Biol. 147:945-958. https://doi.org/10.1083/jcb.147.5.945
  111. Mas, P. and Beachy, R. N. 2000. Role of microtubules in the intracellular distribution of tobacco mosaic virus movement protein. Proc. Natl. Acad. Sci. U. S. A. 97:12345-12349. https://doi.org/10.1073/pnas.97.22.12345
  112. Maule, A. J. 2008. Plasmodesmata: structure, function and biogenesis. Curr. Opin. Plant Biol. 11:680-686. https://doi.org/10.1016/j.pbi.2008.08.002
  113. McCartney, A. W., Greenwood, J. S., Fabian, M. R., White, K. A. and Mullen, R. T. 2005. Localization of the tomato bushy stunt virus replication protein p33 reveals a peroxisome-toendoplasmic reticulum sorting pathway. Plant Cell 17:3513-3531. https://doi.org/10.1105/tpc.105.036350
  114. McLean, B. G., Zupan, J. and Zambryski, P. C. 1995. Tobacco mosaic virus movement protein associates with the cytoskeleton in tobacco cells. Plant Cell. 7:2101-2114. https://doi.org/10.1105/tpc.7.12.2101
  115. Michalak, M., Corbett, E. F., Mesaeli, N., Nakamura, K. and Opas, M. 1999. Calreticulin: one protein, one gene, many functions. Biochem. J. 344:281-292. https://doi.org/10.1042/bj3440281
  116. Mitra, R., Krishnamurthy, K., Blancaflor, E., Payton, M., Nelson, R. S. and Verchot-Lubicz, J. 2003. The Potato virus X TGBp2 protein association with the endoplasmic reticulum plays a role in but is not sufficient for viral cell-to-cell movement. Virology 312:35-48. https://doi.org/10.1016/S0042-6822(03)00180-6
  117. Morita, M. T. and Shimada, T. 2014. The plant endomembrane system--a complex network supporting plant development and physiology. Plant Cell Physiol. 55:667-671. https://doi.org/10.1093/pcp/pcu049
  118. Netherton, C., Moffat, K., Brooks, E. and Wileman, T. 2007. A guide to viral inclusions, membrane rearrangements, factories, and viroplasm produced during virus replication. Adv. Virus. Res. 70:101-182.
  119. Niehl, A., Pena, E. J., Amari, K. and Heinlein, M. 2013. Microtubules in viral replication and transport. Plant J. 75:290-308. https://doi.org/10.1111/tpj.12134
  120. Novoa, R. R., Calderita, G., Arranz, R., Fontana, J., Granzow, H. and Risco, C. 2005. Virus factories: associations of cell organelles for viral replication and morphogenesis. Biol. Cell. 97:147-172. https://doi.org/10.1042/BC20040058
  121. Oparka, K. J., Roberts, A. G., Boevink, P., Santa Cruz, S., Roberts, I., Pradel, K. S., Imlau, A., Kotlizky, G., Sauer, N. and Epel, B. 1999. Simple, but not branched, plasmodesmata allow the nonspecific trafficking of proteins in developing tobacco leaves. Cell 97:743-754. https://doi.org/10.1016/S0092-8674(00)80786-2
  122. Oparka, K. J., Roberts, A. G., Roberts, I. M., Prior, D. A. M. and Santa Cruz, S. 1996. Viral coat protein is targeted to, but does not gate, plasmodesmata during cell-to-cell movement of Potato virus X. Plant J. 10:805-813. https://doi.org/10.1046/j.1365-313X.1996.10050805.x
  123. Ostwald, T. J. and MacLennan, D. H. 1974. Isolation of a high affinity calcium-binding protein from sarcoplasmic reticulum. J. Biol. Chem. 249:974-979.
  124. Padgett, H. S., Epel, B. L., Kahn, T. W., Heinlein, M., Watanabe, Y. and Beachy, R. N. 1996. Distribution of tobamovirus movement protein in infected cells and implications for cell-to-cell spread of infection. Plant J. 10:1079-1088. https://doi.org/10.1046/j.1365-313X.1996.10061079.x
  125. Pena, E. J. and Heinlein, M. 2012. RNA transport during TMV cell-to-cell movement. Front. Plant Sci. 3:193.
  126. Prod'homme, D., Jakubiec, A., Tournier, V., Drugeon, G. and Jupin, I. 2003. Targeting of the Turnip yellow mosaic virus 66K replication protein to the chloroplast envelope is mediated by the 140K protein. J. Virol. 77:9124-9135. https://doi.org/10.1128/JVI.77.17.9124-9135.2003
  127. Reichel, C. and Beachy, R. N. 1998. Tobacco mosaic virus infection induces severe morphological changes of the endoplasmic reticulum. Proc. Natl. Acad. Sci. U. S. A. 95:11169-11174. https://doi.org/10.1073/pnas.95.19.11169
  128. Ritzenthaler, C., Laporte, C., Gaire, F., Dunoyer, P., Schmitt, C., Duval, S., Piéquet, A., Loudes, A. M., Rohfritsch, O., Stussi-Garaud, C. and Pfeiffer, P. 2002. Grapevine fanleaf virus replication occurs on endoplasmic reticulum-derived membranes. J. Virol. 76:8808-8819. https://doi.org/10.1128/JVI.76.17.8808-8819.2002
  129. Robards, A. W. and Lucas, W. J. 1990. Plasmodesmata. Annu. Rev. Plant Physiol. Plant Mol. Biol. 41:369-419. https://doi.org/10.1146/annurev.pp.41.060190.002101
  130. Roberts, A. G. and Oparka, K. J. 2003. Plasmodesmata and the control of symplastic transport. Plant Cell Environ. 26:103-124. https://doi.org/10.1046/j.1365-3040.2003.00950.x
  131. Roberts, I. M., Boevink, P., Roberts, A. G., Sauer, N., Reichel, C. and Oparka, K. J. 2001. Dynamic changes in the frequency and architecture of plasmodesmata during the sink-source transition in tobacco leaves. Protoplasma 218:31-44. https://doi.org/10.1007/BF01288358
  132. Rodionova, N. P., Karpova, O. V., Kozlovsky, S. V., Zayakina, O. V., Arkhipenko, M. V. and Atabekov, J. G. 2003. Linear remodeling of helical virus by movement protein binding. J. Mol. Biol. 333:565-572. https://doi.org/10.1016/j.jmb.2003.08.058
  133. Runions, J., Brach, T., Kuhner, S. and Hawes, C. 2006. Photoactivation of GFP reveals protein dynamics within the endoplasmic reticulum membrane. J. Exp. Bot. 57:43-50. https://doi.org/10.1093/jxb/eri289
  134. Sanfacon, H. 2005. Replication of positive-strand RNA viruses in plants: contact points between plant and virus components. Can. J. Bot. 83:1529-1549. https://doi.org/10.1139/b05-121
  135. Seemanpillai, M., Elamawi, R., Ritzenthaler, C. and Heinlein, M. 2006. Challenging the role of microtubules in Tobacco mosaic virus movement by drug treatments is disputable. J. Virol. 80:6712-6715. https://doi.org/10.1128/JVI.00453-06
  136. Shaw, J. G. 1999. Tobacco mosaic virus and the study of early events in virus infections. Philos. Trans. R. Soc. Lond. B Biol. Sci. 354:603-611. https://doi.org/10.1098/rstb.1999.0412
  137. Shen, W., Yan, P., Gao, L., Pan, X., Wu, J. and Zhou, P. 2010. Helper component-proteinase (HC-Pro) protein of Papaya ringspot virus interacts with papaya calreticulin. Mol. Plant Pathol. 11:335-346. https://doi.org/10.1111/j.1364-3703.2009.00606.x
  138. Stass, A. and Horst, W. J. 2009. Callose in abiotic stress. In: Chemistry, biochemistry and biology of (1-3)-beta-glucans and related polysaccharides, eds. by A. Bacic, G. B. Fincher and B. A. Stone, pp. 499-524. Academic Press, London, UK.
  139. Tamai, A. and Meshi, T. 2001. Cell-to-cell movement of Potato virus X: the role of p12 and p8 encoded by the second and third open reading frames of the triple gene block. Mol. Plant-Microbe Interact. 14:1158-1167. https://doi.org/10.1094/MPMI.2001.14.10.1158
  140. Thomas, C. L., Bayer, E. M., Ritzenthaler, C., Fernandez-Calvino, L. and Maule, A. J. 2008. Specific targeting of a plasmodesmal protein affecting cell-to-cell communication. PLoS Biol. 6:e7. https://doi.org/10.1371/journal.pbio.0060007
  141. Tilney, L. G., Cooke, T. J., Connelly, P. S. and, Tilney, M. S. 1991. The structure of plasmodesmata as revealed by plasmolysis, detergent extraction, and protease digestion. J. Cell Biol. 112:739-747. https://doi.org/10.1083/jcb.112.4.739
  142. 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 reorganizes actin and endomembranes into the X-body, a viral replication factory. Plant Physiol. 158:1359-1370. https://doi.org/10.1104/pp.111.189605
  143. Tilsner, J. and Oparka, K. J. 2012. Missing links?--the connection between replication and movement of plant RNA viruses. Curr. Opin. Virol. 2:705-711. https://doi.org/10.1016/j.coviro.2012.09.007
  144. Toivola, D. M., Strnad, P., Habtezion, A. and Omary, M. B. 2010. Intermediate filaments take the heat as stress proteins. Trends Cell Biol. 20:79-91. https://doi.org/10.1016/j.tcb.2009.11.004
  145. Tomenius, K., Clapham, D. and Meshi, T. 1987. Localization by immunogold cytochemistry of the virus-coded 30K protein in plasmodesmata of leaves infected with tobacco mosaic virus. Virology 160:363-371. https://doi.org/10.1016/0042-6822(87)90007-9
  146. Tsujimoto, Y., Numaga, T., Ohshima, K., Yano, M. A., Ohsawa, R., Gotom, D. B., Naito, S. and Ishikawa, M. 2003. Arabidopsis TOBAMOVIRUS MULTIPLICATION (TOM) 2 locus encodes a transmembrane protein that interacts with TOM1. EMBO J. 22:335-343. https://doi.org/10.1093/emboj/cdg034
  147. Ueki, S. and Citovsky, V. 2002. The systemic movement of a tobamovirus is inhibited by a cadmium-ion-induced glycinerich protein. Nat. Cell Biol. 4:478-486.
  148. Verchot, J. 2011. Wrapping membranes around plant virus infection. Curr. Opin. Virol. 1:388-395. https://doi.org/10.1016/j.coviro.2011.09.009
  149. Verchot, J. 2014. The ER quality control and ER associated degradation machineries are vital for viral pathogenesis. Front. Plant Sci. 5:66.
  150. Verchot-Lubicz, J. and Goldstein, R. E. 2010. Cytoplasmic streaming enables the distribution of molecules and vesicles in large plant cells. Protoplasma 240:99-107. https://doi.org/10.1007/s00709-009-0088-x
  151. Voigt, C. A. and Somerville, S. C. 2009. Callose in biotic stress (pathogenesis): biology, biochemistry and molecular biology of callose in plant defence: callose deposition and turnover in plant--pathogen interactions. In: Chemistry, biochemistry and biology of (1-3)-beta-glucans and related polysaccharides, eds. by A. Bacic, G. B. Fincher and B. A. Stone, pp. 525-562. Academic Press, London, UK.
  152. Voinnet, O., Lederer, C. and Baulcombe, D. C. 2000. A viral movement protein prevents spread of the gene silencing signal in Nicotiana benthamiana. Cell 103:157-167. https://doi.org/10.1016/S0092-8674(00)00095-7
  153. Waigmann, E., Chen, M. H., Bachmaier, R., Ghoshroy, S. and Citovsky, V. 2000. Regulation of plasmodesmal transport by phosphorylation of tobacco mosaic virus cell-to-cell movement protein. EMBO J. 19:4875-4884. https://doi.org/10.1093/emboj/19.18.4875
  154. Walsh, D. and Mohr, I. 2011. Viral subversion of the host protein synthesis machinery. Nat. Rev. Microbiol. 9:860-875. https://doi.org/10.1038/nrmicro2655
  155. Wan, J., Basu, K., Mui, J., Vali, H., Zheng, H. and Laliberte, J. F. 2015. Ultrastructural characterization of turnip mosaic virusinduced cellular rearrangements reveals membrane-bound viral particles accumulating in vacuoles. J. Virol. 89:12441-12456. https://doi.org/10.1128/JVI.02138-15
  156. Wang, P. and Hussey, P. J. 2015. Interactions between plant endomembrane systems and the actin cytoskeleton. Front. Plant Sci. 6:422.
  157. Wei, T., Huang, T. S., McNeil, J., Laliberte, J. F., Hong, J., Nelson, R. S. and Wang, A. 2010. Sequential recruitment of the endoplasmic reticulum and chloroplasts for plant potyvirus replication. J. Virol. 84:799-809. https://doi.org/10.1128/JVI.01824-09
  158. Wei, T. and Wang, A. 2008. Biogenesis of cytoplasmic membranous vesicles for plant potyvirus replication occurs at endoplasmic reticulum exit sites in a COPI- and COPII-dependent manner. J. Virol. 82:12252-12264. https://doi.org/10.1128/JVI.01329-08
  159. White, R. G., Badelt, K., Overall, R. L. and Vesk, M. 1994. Actin associated with plasmodesmata. Protoplasma 180:169-184. https://doi.org/10.1007/BF01507853
  160. Wolf, S., Deom, C. M., Beachy, R. N. and Lucas, W. J. 1989. Movement protein of Tobacco mosaic virus modifies plasmodesmatal size exclusion limit. Science 246:377-379. https://doi.org/10.1126/science.246.4928.377
  161. Wolf, S., Deom, C. M., Beachy, R. and Lucas, W. J. 1991. Plasmodesmatal function is probed using transgenic tobacco plants that express a virus movement protein. Plant Cell 3:593-604. https://doi.org/10.1105/tpc.3.6.593
  162. Wright, K. M., Wood, N. T., Roberts, A. G., Chapman, S., Boevink, P., Mackenzie, K. M. and Oparka, K. J. 2007. Targeting 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
  163. Wu, X., Xu, Z. and Shaw, J. G. 1994. Uncoating of tobacco mosaic virus RNA in protoplasts. Virology 200:256-262. https://doi.org/10.1006/viro.1994.1183
  164. Yan, F., Lu, Y., Lin, L., Zheng, H. and Chen, J. 2012. The ability of PVX p25 to form RL structures in plant cells is necessary for its function in movement, but not for its suppression of RNA silencing. PLoS One 7:e43242. https://doi.org/10.1371/journal.pone.0043242
  165. 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
  166. Ye, C. M., Chen, S., Payton, M., Dickman, M. B. and Verchot, J. 2013. TGBp3 triggers the unfolded protein response and SKP1-dependent programmed cell death. Mol. Plant Pathol. 14:241-255. https://doi.org/10.1111/mpp.12000
  167. Zambryski, P. and Crawford, K. 2000. Plasmodesmata: gatekeepers for cell-to-cell transport of developmental signals in plants. Annu. Rev. Cell Dev. Biol. 16:393-421. https://doi.org/10.1146/annurev.cellbio.16.1.393
  168. Zavaliev, R., Sagi, G., Gera, A. and Epel, B. L. 2010. The constitutive expression of Arabidopsis plasmodesmal-associated class 1 reversibly glycosylated polypeptide impairs plant development and virus spread. J. Exp. Bot. 61:131-142. https://doi.org/10.1093/jxb/erp301
  169. Zavaliev, R., Ueki, S., Epel, B. L. and Citovsky, V. 2011. Biology of callose (${\beta}$-1,3-glucan) turnover at plasmodesmata. Protoplasma 248:117-130. https://doi.org/10.1007/s00709-010-0247-0
  170. Zwart, M. P., Daros, J. A. and Elena, S. F. 2012. Effects of Potyvirus effective population size in inoculated leaves on viral accumulation and the onset of symptoms. J. Virol. 86:9737-9747. https://doi.org/10.1128/JVI.00909-12

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