The induction of stromule formation by a plant DNA-virus in epidermal leaf tissues suggests a novel intra- and intercellular macromolecular trafficking route

Frontiers in Plant Science

Volumn 3, Issue DEC, 2012, Pages

  Krenz, Björn ^a   Jeske, Holger ^b   Kleinow, Tatjana ^b  

^a Department of Obstetrics Gynecology   (United States)

^b UNIVERSITY OF STUTTGART   (Germany)

Author keywords

Chaperone; Geminivirus; Heat shock protein; Movement protein; Plastid

Indexed keywords

EID: 84879882207     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2012.00291     Document Type: Article

References (144)

1. Aberle, H. J., Rütz, M. L., Karayavuz, M., Frischmuth, S., Wege, C., Hülser, D., et al. (2002). Localizing BC1 movement proteins of Abutilon mosaic geminivirus in yeasts by subcellular fractionation and freeze-fracture immunolabelling. Arch. Virol. 147, 103-107.
2. Alzhanova, D. V., Prokhnevsky, A. I., Peremyslov, V. V., and Dolja, V. V. (2007). Virion tails of beet yellows virus: coordinated assembly by three structural proteins. Virology 359, 220-226.
3. Aoki, K., Kragler, F., Xoconostle-Cazares, B., and Lucas, W. J. (2002). A subclass of plant heat shock cognate 70 chaperones carries a motif that facilitates trafficking through plasmodesmata. Proc. Natl. Acad. Sci. U.S.A. 99, 16342-16347.
4. Aparicio, F., Thomas, C. L., Lederer, C., Niu, Y., Wang, D., and Maule, A. J. (2005). Virus induction of heat shock protein 70 reflects a general response to protein accumulation in the plant cytosol. Plant Physiol. 138, 529-536.
5. Avisar, D., Prokhnevsky, A. I., and Dolja, V. V. (2008). Class VIII myosins are required for plasmodesmatal localization of a closterovirus HSP70 homolog. J. Virol. 82, 2836-2843.
6. Bae, M. S., Cho, E. J., Choi, E. Y., and Park, O. K. (2003). Analysis of the Arabidopsis nuclear proteome and its response to cold stress. Plant J. 36, 652-663.
7. Benitez-Alfonso, Y., Faulkner, C., Ritzenthaler, C., and Maule, A. J. (2010). Plasmodesmata: gateways to local and systemic virus infection. Mol. Plant Microbe Interact. 23, 1403-1412.
8. Brizard, J. P., Carapito, C., Delalande, F., Van Dorsselaer, A., and Brugidou, C. (2006). Proteome analysis of plant-virus interactome: comprehensive data for virus multiplication inside their hosts. Mol. Cell. Proteomics 5, 2279-2297.
9. Bukau, B., Weissman, J., and Horwich, A. (2006). Molecular chaperones and protein quality control. Cell 125, 443-451.
10. Burch-Smith, T. M., Brunkard, J. O., Choi, Y. G., and Zambryski, P. C. (2011). Organelle-nucleus cross-talk regulates plant intercellular communication via plasmodesmata. Proc. Natl. Acad. Sci. U.S.A. 108, E1451-E1460.
11. Burch-Smith, T. M., and Zambryski, P. C. (2012). Plasmodesmata paradigm shift: regulation from without versus within. Annu. Rev. Plant Biol. 63, 239-260.
12. Caplan, J. L., Mamillapalli, P., Burch-Smith, T. M., Czymmek, K., and Dinesh-Kumar, S. P. (2008). Chloroplastic protein NRIP1 mediates innate immune receptor recognition of a viral effector. Cell 132, 449-462.
13. Carvalho, C. M., Fontenelle, M. R., Florentino, L. H., Santos, A. A., Zerbini, F. M., and Fontes, E. P. (2008a). A novel nucleocytoplasmic traffic GTPase identified as a functional target of the bipartite geminivirus nuclear shuttle protein. Plant J. 55, 869-880.
14. Carvalho, C. M., Machado, J. P., Zerbini, F. M., and Fontes, E. P. (2008b). NSP-interacting GTPase: a cytosolic protein as cofactor for nuclear shuttle proteins. Plant Signal. Behav. 3, 752-754.
15. Carvalho, C. M., Santos, A. A., Pires, S. R., Rocha, C. S., Saraiva, D. I., Machado, J. P., et al. (2008c). Regulated nuclear trafficking of rpL10A mediated by NIK1 represents a defense strategy of plant cells against virus. PLoS Pathog. 4:e1000247. doi: 10.1371/journal.ppat.1000247
16. Carvalho, M. F., and Lazarowitz, S. G. (2004). Interaction of the movement protein NSP and the Arabidopsis acetyltransferase AtNSI is necessary for cabbage leaf curl geminivirus infection and pathogenicity. J. Virol. 78, 11161-11171.
17. Carvalho, M. F., Turgeon, R., and Lazarowitz, S. G. (2006). The geminivirus nuclear shuttle protein NSP inhibits the activity of AtNSI, a vascular-expressed Arabidopsis acetyltransferase regulated with the sink-to-source transition. Plant Physiol. 140, 1317-1330.
18. Channarayappa, V. M., Schwegler-Berry, D., and Shivashankar, G. (1992). Ultrastructural changes in tomato infected with tomato leaf curl virus, a whitefly-transmitted geminivirus. Can. J. Bot. 70, 1747-1753.
19. Duan, Y. P., Powell, C. A., Purcifull, D. E., Broglio, P., and Hiebert, E. (1997). Phenotypic variation in transgenic tobacco expressing mutated geminivirus movement/pathogenicity (BC1) proteins. Mol. Plant Microbe Interact. 10, 1065-1074.
20. Esau, K. (1933). Pathologic changes in the anatomy of leaves of the sugar beet, Beta vulgaris L., affected by curly top. Phytopathology 23, 679-712.
21. Esau, K. (1944). Anatomical and cytological studies on beet mosaic. J. Agric. Res. 69, 95-117.
22. Escaler, M., Aranda, M. A., Roberts, I. M., Thomas, C. L., and Maule, A. J. (2000a). A comparison between virus replication and abiotic stress (heat) as modifiers of host gene expression in pea. Mol. Plant Pathol. 1, 159-167.
23. Escaler, M., Aranda, M. A., Thomas, C. L., and Maule, A. J. (2000b). Pea embryonic tissues show common responses to the replication of a wide range of viruses. Virology 267, 318-325.
24. Fester, T., Strack, D., and Hause, B. (2001). Reorganization of tobacco root plastids during arbuscule development. Planta 213, 864-868.
25. Florentino, L. H., Santos, A. A., Fontenelle, M. R., Pinheiro, G. L., Zerbini, F. M., Baracat-Pereira, M. C., et al. (2006). A PERK-like receptor kinase interacts with the geminivirus nuclear shuttle protein and potentiates viral infection. J. Virol. 80, 6648-6656.
26. Flores-Pérez, U., and Jarvis, P. (2012). Molecular chaperone involvement in chloroplast protein import. Biochim. Biophys. Acta. doi: 10.1016/j.bbamcr.2012.1003.1019 [Epub ahead of print].
27. Fontes, E. P., Santos, A. A., Luz, D. F., Waclawovsky, A. J., and Chory, J. (2004). The geminivirus nuclear shuttle protein is a virulence factor that suppresses transmembrane receptor kinase activity. Genes Dev. 18, 2545-2556.
28. Frischmuth, S., Kleinow, T., Aberle, H.-J., Wege, C., Hülser, D., and Jeske, H. (2004). Yeast two-hybrid systems confirm the membrane-association and oligomerization of BC1 but do not detect an interaction of the movement proteins BC1 and BV1 of Abutilon mosaic geminivirus. Arch. Virol. 149, 2349-2364.
29. Frischmuth, S., Wege, C., Hülser, D., and Jeske, H. (2007). The movement protein BC1 promotes redirection of the nuclear shuttle protein BV1 of Abutilon mosaic geminivirus to the plasma membrane in fission yeast. Protoplasma 230, 117-123.
30. Gafni, Y., and Epel, B. L. (2002). The role of host and viral proteins in intra-and inter-cellular trafficking of geminiviruses. Physiol. Mol. Plant Pathol. 60, 231-241.
31. Gray, J. C., Hansen, M. R., Shaw, D. J., Graham, K., Dale, R., Smallman, P., et al. (2012). Plastid stromules are induced by stress treatments acting through abscisic acid. Plant J. 69, 387-398.
32. Gray, J. C., Sullivan, J. A., Hibberd, J. M., and Hansson, M. R. (2001). Stromules: mobile protrusions and interconnections between plastids. Plant Biol. 3, 223-233.
33. Gröning, B. R., Abouzid, A., and Jeske, H. (1987). Single-stranded DNA from Abutilon mosaic virus is present in the plastids of infected Abutilon sellovianum. Proc. Natl. Acad. Sci. U.S.A. 84, 8996-9000.
34. Gröning, B. R., Frischmuth, T., and Jeske, H. (1990). Replicative form DNA of Abutilon mosaic virus is present in plastids. Mol. Gen. Genet. 220, 485-488.
35. Gunning, B. E. (2005). Plastid stromules: video microscopy of their outgrowth, retraction, tensioning, anchoring, branching, bridging, and tip-shedding. Protoplasma 225, 33-42.
36. Hans, J., Hause, B., Strack, D., and Walter, M. H. (2004). Cloning, characterization, and immunolocalization of a mycorrhiza-inducible 1-deoxy-d-xylulose 5-phosphate reductoisomerase in arbuscule-containing cells of maize. Plant Physiol. 134, 614-624.
37. Hanson, M. R., and Sattarzadeh, A. (2008). Dynamic morphology of plastids and stromules in angiosperm plants. Plant Cell Environ. 31, 646-657.
38. Hanson, M. R., and Sattarzadeh, A. (2011). Stromules: recent insights into a long neglected feature of plastid morphology and function. Plant Physiol. 155, 1486-1492.
39. Hao, L., Wang, H., Sunter, G., and Bisaro, D. M. (2003). Geminivirus AL2 and L2 proteins interact with and inactivate SNF1 kinase. Plant Cell 15, 1034-1048.
40. Harries, P., and Ding, B. (2011). Cellular factors in plant virus movement: at the leading edge of macromolecular trafficking in plants. Virology 411, 237-243.
41. 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.
42. Harries, P. A., Schoelz, J. E., and Nelson, R. S. (2011). Intracellular transport of viruses and their components: utilizing the cytoskeleton and membrane highways. Mol. Plant Microbe Interact. 23, 1381-1393.
43. Hehnle, S., Wege, C., and Jeske, H. (2004). Interaction of DNA with the movement proteins of geminiviruses revisited. J. Virol. 78, 7698-7706.
44. Holzinger, A., Buchner, O., Lutz, C., and Hanson, M. R. (2007). Temperature-sensitive formation of chloroplast protrusions and stromules in mesophyll cells of Arabidopsis thaliana. Protoplasma 230, 23-30.
45. Horns, T., and Jeske, H. (1991). Localization of Abutilon mosaic virus DNA within leaf tissue by in situ hybridization. Virology 181, 580-588.
46. Hou, Y. M., Sanders, R., Ursin, V. M., and Gilbertson, R. L. (2000). Transgenic plants expressing geminivirus movement proteins: abnormal phenotypes and delayed infection by tomato mottle virus in transgenic tomatoes expressing the bean dwarf mosaic virus BV1 or BC1 proteins. Mol. Plant Microbe Interact. 13, 297-308.
47. Ingham, D. J., and Lazarowitz, S. G. (1993). A single missense mutation in the BR1 movement protein alters the host range of the squash leaf curl geminivirus. Virology 196, 694-702.
48. Isemer, R., Mulisch, M., Schafer, A., Kirchner, S., Koop, H. U., and Krupinska, K. (2012). Recombinant Whirly1 translocates from transplastomic chloroplasts to the nucleus. FEBS Lett. 586, 85-88.
49. Ito, J., Heazlewood, J. L., and Millar, A. H. (2006). Analysis of the soluble ATP-binding proteome of plant mitochondria identifies new proteins and nucleotide triphosphate interactions within the matrix. J. Proteome Res. 5, 3459-3469.
50. Itoh, R. D., Yamasaki, H., Septiana, A., Yoshida, S., and Fujiwara, M. T. (2010). Chemical induction of rapid and reversible plastid filamentation in Arabidopsis thaliana roots. Physiol. Plant 139, 144-158.
51. Jeske, H. (1986). The detection of the Abutilon mosaic virus depends on the experimental daytime. J. Phytopathol. 115, 243-256.
52. Jeske, H. (2007). "Replication of geminiviruses and the use of rolling circle amplification for their diagnosis, " in Tomato Yellow Leaf Curl Virus Disease: Management, Molecular Biology, and Breeding for Resistance, ed. H. Czosnek (Dordrecht: Springer Science Business Media), 141-156.
53. Jeske, H. (2009). Geminiviruses. Curr. Top. Microbiol. Immunol. 185-226.
54. Jeske, H., and Schuchalter-Eicke, G. (1984). The Abutilon mosaic virus (AbMV) in different leaf tissue of several host plant species of Malvaceae. Phytopathol. Z. 109, 353-362.
55. Jeske, H., and Werz, G. (1978). The influence of light intensity on pigment composition and ultrastructure of plastids in leaves of diseased Abutilon sellowianum Reg. Phytopathol. Z. 91, 1-13.
56. Jeske, H., and Werz, G. (1980a). Cytochemical characterization of plastidal inclusions in Abutilon mosaic-infected Malva parviflora mesophyll cells. Virology 106, 155-158.
57. Jeske, H., and Werz, G. (1980b). Ultrastructural and biochemical investigations on the whitefly transmitted Abutilon mosaic virus (AbMV). Phytopathol. Z. 97, 43-55.
58. Jimenez, I., Lopez, L., Alamillo, J. M., Valli, A., and Garcia, J. A. (2006). Identification of a plum pox virus CI-interacting protein from chloroplast that has a negative effect in virus infection. Mol. Plant Microbe Interact. 19, 350-358.
59. Kampinga, H. H., and Craig, E. A. (2010). The HSP70 chaperone machinery: J proteins as drivers of functional specificity. Nat. Rev. Mol. Cell Biol. 11, 579-592.
60. Kanzaki, H., Saitoh, H., Ito, A., Fujisawa, S., Kamoun, S., Katou, S., et al. (2003). Cytosolic HSP90 and HSP70 are essential components of INF1-mediated hypersensitive response and non-host resistance to Pseudomonas cichorii in Nicotiana benthamiana. Mol. Plant Pathol. 4, 383-391.
61. Kleinow, T., Nischang, M., Beck, A., Kratzer, U., Tanwir, F., Preiss, W., et al. (2009a). Three C-terminal phosphorylation sites in the Abutilon mosaic virus movement protein affect symptom development and viral DNA accumulation. Virology 390, 89-101.
62. Kleinow, T., Tanwir, F., Kocher, C., Krenz, B., Wege, C., and Jeske, H. (2009b). Expression dynamics and ultrastructural localization of epitope-tagged Abutilon mosaic virus nuclear shuttle and movement proteins in Nicotiana benthamiana cells. Virology 391, 212-220.
63. Köhler, R. H., Cao, J., Zipfel, W. R., Webb, W. W., and Hanson, M. R. (1997). Exchange of protein molecules through connections between higher plant plastids. Science 276, 2039-2042.
64. Köhler, R. H., and Hanson, M. R. (2000). Plastid tubules of higher plants are tissue-specific and developmentally regulated. J. Cell Sci. 113, 81-89.
65. Köhler, R. H., Schwille, P., Webb, W. W., and Hanson, M. R. (2000). Active protein transport through plastid tubules: velocity quantified by fluorescence correlation spectroscopy. J. Cell Sci. 113, 3921-3930.
66. Kong, L. J., and Hanley-Bowdoin, L. (2002). A geminivirus replication protein interacts with a protein kinase and a motor protein that display different expression patterns during plant development and infection. Plant Cell 14, 1817-1832.
67. Kozlov, M. M., McMahon, H. T., and Chernomordik, L. V. (2010). Protein-driven membrane stresses in fusion and fission. Trends Biochem. Sci. 35, 699-706.
68. Krause, K., and Krupinska, K. (2009). Nuclear regulators with a second home in organelles. Trends Plant Sci. 14, 194-199.
69. Krenz, B., Neugart, F., Kleinow, T., and Jeske, H. (2011). Self-interaction of Abutilon mosaic virus replication initiator protein (Rep) in plant cell nuclei. Virus Res. 161, 194-197.
70. Krenz, B., Windeisen, V., Wege, C., Jeske, H., and Kleinow, T. (2010). A plastid-targeted heat shock cognate 70 kDa protein interacts with the Abutilon mosaic virus movement protein. Virology 401, 6-17.
71. Krichevsky, A., Kozlovsky, S. V., Gafni, Y., and Citovsky, V. (2006). Nuclear import and export of plant virus proteins and genomes. Mol. Plant Pathol. 7, 131-146.
72. Kwok, E. Y., and Hanson, M. R. (2003). Microfilaments and microtubules control the morphology and movement of non-green plastids and stromules in Nicotiana tabacum. Plant J. 35, 16-26.
73. Kwok, E. Y., and Hanson, M. R. (2004a). Plastids and stromules interact with the nucleus and cell membrane in vascular plants. Plant Cell Rep. 23, 188-195.
74. Kwok, E. Y., and Hanson, M. R. (2004b). Stromules and the dynamic nature of plastid morphology. J. Microsc. 214, 124-137.
75. Latijnhouwers, M., Xu, X. M., and Moller, S. G. (2010). Arabidopsis stromal 70-kDa heat shock proteins are essential for chloroplast development. Planta 232, 567-578.
76. Lee, J. Y., and Lu, H. (2011). Plasmodesmata: the battleground against intruders. Trends Plant Sci. 16, 201-210.
77. Lee, J. Y., Yoo, B. C., Rojas, M. R., Gomez-Ospina, N., Staehelin, L. A., and Lucas, W. J. (2003). Selective trafficking of non-cell-autonomous proteins mediated by NtNCAPP1. Science 299, 392-396.
78. Levy, A., and Tzfira, T. (2011). Bean dwarf mosaic virus: a model system for the study of viral movement. Mol. Plant Pathol. 11, 451-461.
79. Lewis, J. D., and Lazarowitz, S. G. (2010). Arabidopsis synaptotagmin SYTA regulates endocytosis and virus movement protein cell-to-cell transport. Proc. Natl. Acad. Sci. U.S.A. 107, 2491-2496.
80. Lim, H. S., Vaira, A. M., Bae, H., Bragg, J. N., Ruzin, S. E., Bauchan, G. R., et al. (2010). Mutation of a chloroplast-targeting signal in Alternanthera mosaic virus TGB3 impairs cell-to-cell movement and eliminates long-distance virus movement. J. Gen. Virol. 91, 2102-2115.
81. Lin, J. W., Ding, M. P., Hsu, Y. H., and Tsai, C. H. (2007). Chloroplast phosphoglycerate kinase, a gluconeogenetic enzyme, is required for efficient accumulation of bamboo mosaic virus. Nucleic Acids Res. 35, 424-432.
82. Lohse, S., Schliemann, W., Ammer, C., Kopka, J., Strack, D., and Fester, T. (2005). Organization and metabolism of plastids and mitochondria in arbuscular mycorrhizal roots of Medicago truncatula. Plant Physiol. 139, 329-340.
83. Lozano-Duran, R., Rosas-Diaz, T., Luna, A. P., and Bejarano, E. R. (2011). Identification of host genes involved in geminivirus infection using a reverse genetics approach. PLoS ONE 6:e22383. doi: 10.1371/journal.pone.0022383
84. Lucas, W. J. (2006). Plant viral movement proteins: agents for cell-to-cell trafficking of viral genomes. Virology 344, 169-184.
85. Mariano, A. C., Andrade, M. O., Santos, A. A., Carolino, S. M., Oliveira, M. L., Baracat-Pereira, M. C., et al. (2004). Identification of a novel receptor-like protein kinase that interacts with a geminivirus nuclear shuttle protein. Virology 318, 24-31.
86. Maule, A. J., Benitez-Alfonso, Y., and Faulkner, C. (2011). Plasmodesmata-membrane tunnels with attitude. Curr. Opin. Plant Biol. 14, 683-690.
87. Maule, A. J., Escaler, M., and Aranda, M. A. (2000). Programmed responses to virus replication in plants. Mol. Plant Pathol. 1, 9-15.
88. Mayer, M. P. (2010). Gymnastics of molecular chaperones. Mol. Cell 39, 321-331.
89. Mayer, M. P., and Bukau, B. (2005). HSP70 chaperones: cellular functions and molecular mechanism. Cell. Mol. Life Sci. 62, 670-684.
90. McGarry, R. C., Barron, Y. D., Carvalho, M. F., Hill, J. E., Gold, D., Cheung, E., et al. (2003). A novel Arabidopsis acetyltransferase interacts with the geminivirus movement protein NSP. Plant Cell 15, 1605-1618.
91. McMahon, H. T., Kozlov, M. M., and Martens, S. (2010). Membrane curvature in synaptic vesicle fusion and beyond. Cell 140, 601-605.
92. Nagy, P. D., Wang, R. Y., Pogany, J., Hafren, A., and Makinen, K. (2011). Emerging picture of host chaperone and cyclophilin roles in RNA virus replication. Virology 411, 374-382.
93. Natesan, S. K., Sullivan, J. A., and Gray, J. C. (2009). Myosin XI is required for actin-associated movement of plastid stromules. Mol. Plant 2, 1262-1272.
94. Natesan, S. K. A., Sullivan, J. A., and Gray, J. C. (2005). Stromules: a characteristic cell-specific feature of plastid morphology. J. Exp. Bot. 56, 787-797.
95. Newell, C. A., Natesan, S. K. A., Sullivan, J. A., Jouhet, J., Kavanagh, T. A., and Gray, J. C. (2012). Exclusion of plastid nucleoids and ribosomes from stromules in tobacco and Arabidopsis. Plant J. 69, 399-410.
96. Niehl, A., and Heinlein, M. (2011). Cellular pathways for viral transport through plasmodesmata. Protoplasma 248, 75-99.
97. Noel, L. D., Cagna, G., Stuttmann, J., Wirthmuller, L., Betsuyaku, S., Witte, C. P., et al. (2007). Interaction between SGT1 and cytosolic/nuclear HSC70 chaperones regulates Arabidopsis immune responses. Plant Cell 19, 4061-4076.
98. Noueiry, A. O., Lucas, W. J., and Gilbertson, R. L. (1994). Two proteins of a plant DNA virus coordinate nuclear and plasmodesmal transport. Cell 76, 925-932.
99. Oparka, K. J. (2004). Getting the message across: how do plant cells exchange macromolecular complexes? Trends Plant Sci. 9, 33-41.
100. Pascal, E., Goodlove, P. E., Wu, L. C., and Lazarowitz, S. G. (1993). Transgenic tobacco plants expressing the geminivirus BL1 protein exhibit symptoms of viral disease. Plant Cell 5, 795-807.
101. Pascal, E., Sanderfoot, A. A., Ward, B. M., Medville, R., Turgeon, R., and Lazarowitz, S. G. (1994). The geminivirus BR1 movement protein binds single-stranded DNA and localizes to the cell nucleus. Plant Cell 6, 995-1006.
102. Peltier, J. B., Cai, Y., Sun, Q., Zabrouskov, V., Giacomelli, L., Rudella, A., et al. (2006). The oligomeric stromal proteome of Arabidopsis thaliana chloroplasts. Mol. Cell. Proteomics 5, 114-133.
103. Peltier, J. B., Emanuelsson, O., Kalume, D. E., Ytterberg, J., Friso, G., Rudella, A., et al. (2002). Central functions of the lumenal and peripheral thylakoid proteome of Arabidopsis determined by experimentation and genome-wide prediction. Plant Cell 14, 211-236.
104. 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.
105. Pyke, K. A., and Howells, C. A. (2002). Plastid and stromule morphogenesis in tomato. Ann. Bot. 90, 559-566.
106. Qin, S. W., Ward, B. M., and Lazarowitz, S. G. (1998). The bipartite geminivirus coat protein aids BR1 function in viral movement by affecting the accumulation of viral single-stranded DNA. J. Virol. 72, 9247-9256.
107. Reinero, A., and Beachy, R. N. (1986). Association of TMV coat protein with chloroplast membranes in virus-infected leaves. Plant Mol. Biol. 291-301.
108. Rocha, C. S., Santos, A. A., Machado, J. P., and Fontes, E. P. (2008). The ribosomal protein L10/QM-like protein is a component of the NIK-mediated antiviral signaling. Virology 380, 165-169.
109. Rojas, M. R., Hagen, C., Lucas, W. J., and Gilbertson, R. L. (2005). Exploiting chinks in the plant's armor: evolution and emergence of geminiviruses. Annu. Rev. Phytopathol. 43, 361-394.
110. Rojas, M. R., Noueiry, A. O., Lucas, W. J., and Gilbertson, R. L. (1998). Bean dwarf mosaic geminivirus movement proteins recognize DNA in a form-and size-specific manner. Cell 95, 105-113.
111. Rushing, A. E., Sunter, G., Gardiner, W. E., Dute, R. R., and Bisaro, D. M. (1987). Ultrastructural aspects of tomato golden mosaic virus infection in tobacco. Phytopathology 77, 1231-1236.
112. Sanderfoot, A. A., Ingham, D. J., and Lazarowitz, S. G. (1996). A viral movement protein as a nuclear shuttle. The geminivirus BR1 movement protein contains domains essential for interaction with BL1 and nuclear localization. Plant Physiol. 110, 23-33.
113. Sanderfoot, A. A., and Lazarowitz, S. G. (1995). Cooperation in viral movement: the geminivirus BL1 movement protein interacts with BR1 and redirects it from the nucleus to the cell periphery. Plant Cell 7, 1185-1194.
114. Santos, A. A., Lopes, K. V., Apfata, J. A., and Fontes, E. P. (2010). NSP-interacting kinase, NIK: a transducer of plant defence signalling. J. Exp. Bot. 61, 3839-3845.
115. Sattarzadeh, A., Krahmer, J., Germain, A. D., and Hanson, M. R. (2009). A myosin XI tail domain homologous to the yeast myosin vacuole-binding domain interacts with plastids and stromules in Nicotiana benthamiana. Mol. Plant 2, 1351-1358.
116. Saunders, K., Wege, C., Veluthambi, K., Jeske, H., and Stanley, J. (2001). The distinct disease phenotypes of the common and yellow vein strains of tomato golden mosaic virus are determined by nucleotide differences in the 3′-terminal region of the gene encoding the movement protein. J. Gen. Virol. 82, 45-51.
117. Schattat, M., Barton, K., Baudisch, B., Klosgen, R. B., and Mathur, J. (2011). Plastid stromule branching coincides with contiguous endoplasmic reticulum dynamics. Plant Physiol. 155, 1667-1677.
118. Schattat, M. H., Griffiths, S., Mathur, N., Barton, K., Wozny, M. R., Dunn, N., et al. (2012). Differential coloring reveals that plastids do not form networks for exchanging macromolecules. Plant Cell 24, 1465-1477.
119. Schattat, M. H., and Klösgen, R. B. (2011). Induction of stromule formation by extracellular sucrose and glucose in epidermal leaf tissue of Arabidopsis thaliana. BMC Plant Biol. 11:115. doi: 10.1186/1471-2229-11-115
120. 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.
121. Schoelz, J. E., and Zaitlin, M. (1989). Tobacco mosaic virus RNA enters chloroplasts in vivo. Proc. Natl. Acad. Sci. U.S.A. 86, 4496-4500.
122. Schuchalter-Eicke, G., and Jeske, H. (1983). Seasonal changes in the chloroplast ultrastructure in Abutilon mosaic virus (AbMV) infected Abutilon spec. (Malvaceae). Phytopathol. Z. 108, 172-184.
123. Shalla, T. A. (1964). Assembly and aggregation of tobacco mosaic virus in tomato leaflets. J. Cell Biol. 21, 253-264.
124. Shen, W., and Hanley-Bowdoin, L. (2006). Geminivirus infection up-regulates the expression of two Arabidopsis protein kinases related to yeast SNF1 and mammalian AMPK activating kinases. Plant Physiol. 142, 1642-1655.
125. Simpson, C., Thomas, C., Findlay, K., Bayer, E., and Maule, A. J. (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.
126. Su, P.-H., and Li, H.-M. (2008). Arabidopsis stromal 70-kD heat shock proteins are essential for plant development and important for thermotolerance of germinating seeds. Plant Physiol. 146, 1231-1241.
127. Su, P. H., and Li, H. M. (2010). Stromal Hsp70 is important for protein translocation into pea and Arabidopsis chloroplasts. Plant Cell 22, 1516-1531.
128. Sung, D. Y., Vierling, E., and Guy, C. L. (2001). Comprehensive expression profile analysis of the Arabidopsis HSP70 gene family. Plant Physiol. 126, 789-800.
129. Swindell, W. R., Huebner, M., and Weber, A. P. (2007). Transcriptional profiling of Arabidopsis heat shock proteins and transcription factors reveals extensive overlap between heat and non-heat stress response pathways. BMC Genomics 8:125. doi: 10.1186/1471-2164-8-125
130. Tirlapur, U. K., Dahse, I., Reiss, B., Meurer, J., and Oelmuller, R. (1999). Characterization of the activity of a plastid-targeted green fluorescent protein in Arabidopsis. Eur. J. Cell Biol. 78, 233-240.
131. Torrance, L., Cowan, G. H., Gillespie, T., Ziegler, A., and Lacomme, C. (2006). Barley stripe mosaic virus-encoded proteins triple-gene block 2 and γb localize to chloroplasts in virus-infected monocot and dicot plants, revealing hitherto-unknown roles in virus replication. J. Gen. Virol. 87, 2403-2411.
132. Trejo-Saavedra, D. L., Vielle-Calzada, J. P., and Rivera-Bustamante, R. F. (2009). The infective cycle of cabbage leaf curl virus (CaLCuV) is affected by CRUMPLED LEAF (CRL) gene in Arabidopsis thaliana. Virol. J. 6, 169.
133. Ueki, S., and Citovsky, V. (2011). To Gate, or not to gate: regulatory mechanisms for intercellular protein transport and virus movement in plants. Mol. Plant 4, 782-793.
134. von Arnim, A., and Stanley, J. (1992). Determinants of tomato golden mosaic virus symptom development located on DNA B. Virology 186, 286-293.
135. Waigmann, E., Ueki, S., Trutnyeva, K., and Citovsky, V. (2004). The ins and outs of nondestructive cell-to-cell and systemic movement of plant viruses. Crit. Rev. Plant Sci. 23, 195-250.
136. Waters, M. T., Fray, R. G., and Pyke, K. A. (2004). Stromule formation is dependent upon plastid size, plastid differentiation status and the density of plastids within the cell. Plant J. 39, 655-667.
137. Wege, C. (2007). "Movement and localization of tomato yellow leaf curl viruses in the infected plant, " in Tomato Yellow Leaf Curl Virus Disease: Management, Molecular Biology, and Breeding for Resistance, ed. H. Czosnek (Dordrecht: Springer Science Business Media), 185-206.
138. Weibezahn, J., Schlieker, C., Tessarz, P., Mogk, A., and Bukau, B. (2005). Novel insights into the mechanism of chaperone-assisted protein disaggregation. Biol. Chem. 386, 739-744.
139. Xiang, Y., Kakani, K., Reade, R., Hui, E., and Rochon, D. (2006). A 38-amino-acid sequence encompassing the arm domain of the cucumber necrosis virus coat protein functions as a chloroplast transit peptide in infected plants. J. Virol. 80, 7952-7964.
140. 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.
141. Zhang, S. C., Ghosh, R., and Jeske, H. (2002). Subcellular targeting domains of Abutilon mosaic geminivirus movement protein BC1. Arch. Virol. 147, 2349-2363.
142. Zhang, S. C., Wege, C., and Jeske, H. (2001). Movement proteins (BC1 and BV1) of Abutilon mosaic geminivirus are cotransported in and between cells of sink but not of source leaves as detected by green fluorescent protein tagging. Virology 290, 249-260.
143. Zhou, Y., Rojas, M. R., Park, M.-R., Seo, Y.-S., Lucas, W. J., and Gilbertson, R. L. (2011). Histone H3 interacts and co-localizes with the nuclear shuttle protein and movement protein of a geminivirus. J. Virol. 85, 11821-11832.
144. Zhou, Y. C., Garrido-Ramirez, E. R., Sudarshana, M. R., Yendluri, S., and Gilbertson, R. L. (2007). The N-terminus of the begomovirus nuclear shuttle protein (BV1) determines virulence or avirulence in Phaseolus vulgaris. Mol. Plant Microbe Interact. 20, 1523-1534.