Plant Molecular Biology

, Volume 38, Issue 1–2, pp 279–310 | Cite as

Intercellular protein trafficking through plasmodesmata

  • Biao Ding


During plant morphogenesis, groups of cells differentiate to form specialized tissues possessing distinct structures and functions. Cell specialization is a result of specific gene expression at the individual cell level. Coordination of differential gene expression among cells requires that cells communicate with one another. Plasmodesmata provide a cytoplasmic pathway for direct intercellular communication. Recent discoveries that macromolecules such as transcription factors, viral proteins, and plant defense-related proteins can traffic through plasmodesmata suggest that intercellular protein trafficking is potentially an important means to regulate plant developmental processes, physiological functions, plant-pathogen interactions, and plant defense reactions. Thus, elucidating the specific functions and mechanisms of intercellular protein trafficking has broad implications in understanding how a plant develops and functions at the molecular level. This review is to provide an update on this rapidly developing area of plant biology, with emphasis on the discussion of possible mechanisms underlying intercellular protein trafficking.

plasmodesmata protein trafficking viral movement protein virus movement plant development plant defense 


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  1. 1.
    Abel S, Theologis A: A polymorphic bipartite motif signals nuclear targeting of early auxin-inducible proteins related to PS-IAA4 from pea (Pisum sativum). Plant J 8: 87–96 (1995).Google Scholar
  2. 2.
    Ainger K, Avossa D, Morgan F, Hill SJ, Barry C, Barbarese E, Carson JH: Transport and localization of exogenous myelin basic protein mRNA microinjected into oligodendrocytes. J Cell Biol 123: 431–441 (1993).Google Scholar
  3. 3.
    Anderson JM, Palukaitis P, Zaitlin M: A defective replicase gene induces resistance to cucumber mosaic virus in transgenic tobacco plants. Proc Natl Acad Sci USA 89: 8759–8763 (1992).Google Scholar
  4. 4.
    Angell SM, Baulcombe DC: Cell-to-cell movement of potato virus X revealed by microinjection of a viral vector tagged with the ß-glucuronidase gene. Plant J 7: 135–140 (1995).Google Scholar
  5. 5.
    Angell SM, Davies C, Baulcombe DC: Cell-to-cell 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 (1996).Google Scholar
  6. 6.
    Atabekov JG, Taliansky ME: Expression of a plant viruscoded transport function by different viral genomes. Adv Virus Res 38: 201–248 (1990).Google Scholar
  7. 7.
    Atkins D, Hull R, Wells B, Roberts K, Moore P, Beachy RN: The tobacco mosaic virus 30K movement protein in transgenic tobacco plants is localized to plasmodesmata. J Gen Virol 72: 209–211 (1991).Google Scholar
  8. 8.
    Balachandran S, Xiang Y, Schobert C, Thompson GA, Lucas WJ: Phloem sap proteins from Cucurbita maxima and Ricinus communis have the capacity to traffic cell to cell through plasmodesmata. Proc Natl Acad Sci USA 94: 14150–14155 (1997).Google Scholar
  9. 9.
    Barker H, Harrison BD: Restricted distribution of potato leafroll virus antigen in resistant potato genotypes and its effect on transmission of the virus by aphids. Ann Appl Biol 109: 595–604 (1986).Google Scholar
  10. 10.
    Baskin TI, Busby CH, Fowke LC, Sammut M, Gubler F: Improvements in immunostaining samples embedded in methacrylate: localization of microtubules and other antigens throughout developing organs in plants of diverse taxa. Planta 187: 405–413 (1992).Google Scholar
  11. 11.
    Bassell G, Singer RH: Messenger RNA and cytoskeletal filaments. Curr Opin Cell Biol 9: 109–115 (1996).Google Scholar
  12. 12.
    Beck DL, Guilford PJ, Voot DM, Andersen MT, Forster RLS: Triple gene block proteins of white clover mosaic potexvirus are required for transport. Virology 183: 695–702 (1991).Google Scholar
  13. 13.
    Bergey DR, Howe GA, Ryan CA: Polypeptide signaling for plant defensive genes exhibits analogies to defense signaling in animals. Proc Natl Acad Sci USA 93: 12053–12058 (1996).Google Scholar
  14. 14.
    Bleykasten C, Gilmer D, Guilley H, Richards KE, Jonard G: Beet necrotic yellow vein virus 42 kDa triple gene block protein binds nucleic acid in vitro. J Gen Virol 77: 889–897 (1996).Google Scholar
  15. 15.
    Boccard F, Baulcombe D: Mutational analysis of cis-acting sequences and gene function in RNA3 of cucumber mosaic virus. Virology 193: 563–578 (1993).Google Scholar
  16. 16.
    Bostwick DE, Dannenhoffer JM, Skaggs MI, Lister RM, Larkins BA, Thompson GA: Pumpkin phloem lectin genes are specifically expressed in companion cells. Plant Cell 4: 1539–1548 (1992).Google Scholar
  17. 17.
    Botha CEJ, Hartley BJ, Cross RHM: The ultrastructure and computer-enhanced digital image analysis of plasmodesmata at the Kranz mesophyll-bundle sheath interface of Themeda triandra var. imberbis (Retz) A. Camus in conventionally-fixed leaf blades. Ann Bot 72: 255–261 (1993).Google Scholar
  18. 18.
    Bouhidel K, Irish VF: Cellular interactions mediated by the homeotic PISTILLATA gene determine cell fate in the Arabidopsis flower. Devel Biol 174: 22–31 (1996).Google Scholar
  19. 19.
    Boulton MI, Pallaghy CK, Chatani M, MacFarlane S, Davies JW: Replication of maize streak virus mutants in maize protoplasts: evidence for a movement protein. Virology 192: 85–93 (1993).Google Scholar
  20. 20.
    Bowles DJ: Defense-related proteins in higher plants. Annu Rev Biochem 59: 873–907 (1990).Google Scholar
  21. 21.
    Bowman JL, Smyth DR, Meyerowitz EM: Genes directing flower development in Arabidopsis. Plant Cell 1: 37–52 (1989).Google Scholar
  22. 22.
    Brakke M, Ball EM, Langenberg WG: A non-capsid protein associated with unencapsidated virus RNA in barley infected with barley stripe mosaic virus. J Gen Virol 69: 481–491 (1988).Google Scholar
  23. 23.
    Canto T, Prior DAM, Hellward KH, Oparka KJ, Palukaitis P: Characterization of cucumber mosaic virus. 4. movement protein and coat proteins are both essential for cell-to-cell movement of cucumber mosaic virus. Virology 237: 237–248 (1997).Google Scholar
  24. 24.
    Carpenter R, Coen ES: Floral homeotic mutations produced by transposon-mutagenesis in Antirrhinum majus. Genes Devel 4: 1483–1493 (1990).Google Scholar
  25. 25.
    Carpenter R, Coen ES: Transposon induced chimeras show that floricaula, a meristem identity gene, acts nonautonomously between cell layers. Development 121: 19–26 (1995).Google Scholar
  26. 26.
    Carrington JC, Freed DD, Leinicke AJ: Bipartite signal sequence mediates nuclear translocation of the plant potyviral NIa protein. Plant Cell 3: 953–962 (1991).Google Scholar
  27. 27.
    Carrington JC, Kasschau KD, Mahajan SK, Schaad MC: Cell-to-cell and long-distance transport of viruses in plants. Plant Cell 8: 1669–1681 (1996).Google Scholar
  28. 28.
    Casacuberta JM, Puigdoménech P, San Segundo B: A gene coding for a basic pathogenesis-related (PR-like) protein from Zea mays.Molecular cloning and induction by a fungus (Fusarium moniliforme) in germinating maize seeds. Plant Mol Biol 16: 527–536 (1991).Google Scholar
  29. 29.
    Chalfie M, Tu Y, Euskirchen G, Ward WW, Prasher DC: Green fluorescent protein as a marker for gene expression. Science 263: 802–805 (1994).Google Scholar
  30. 30.
    Chalfie M: Green fluorescent protein. Photochem Photobiol 62: 651–656 (1995).Google Scholar
  31. 31.
    Chapman S, Hills GJ, Watts J, Baulcombe DC: Mutational analysis of the coat protein gene of potato virus X: effects on virion morphology and viral pathogenecity. Virology 191: 223–230 (1992).Google Scholar
  32. 32.
    Chapman S, Kavanagh T, Baulcombe DC: Potato virus X as a vector for gene expression in plants. Plant J 2: 549–557 (1992).Google Scholar
  33. 33.
    Chuck G, Lincoln C, Hake S: KNAT1 induces lobed leaves with ectopic meristems when overexpressed in Arabidopsis. Plant Cell 8: 1277–1289 (1996).Google Scholar
  34. 34.
    Citovsky V, Knorr D, Schuster G, Zambryski P: The P30 movement protein of tobacco mosaic virus is a single-strand nucleic acid binding protein. Cell 60: 637–647 (1990).Google Scholar
  35. 35.
    Citovsky V, Knorr D, Zambryski P: Gene 1, a potential movement locus of CaMV, encodes an RNA binding protein. Proc Natl Acad Sci USA 88: 2476–2480 (1991).Google Scholar
  36. 36.
    Citovsky V, Wong ML, Shaw AL, Venkataram Prasad BV, Zambryski P: Visualization and characterization of tobacco mosaic virus movement protein binding to single-stranded nucleic acids. Plant Cell 4: 397–411 (1992).Google Scholar
  37. 37.
    Citovsky V, McLean BG, Zupan JR, Zambryski P: Phosphorylation of tobacco mosaic virus cell-to-cell movement protein by a developmentally regulated plant cell wall-associated protein kinase. Genes Devel 7: 904–910 (1993).Google Scholar
  38. 38.
    Clark AM, Jacobsen KR, Bostwick DE, Dannenhoffer JM, Skaggs MI, Thompson GA: Molecular characterization of a phloem-specific gene encoding the filament protein, phloem protein 1 (PP1), from Cucurbita maxima. Plant J 12: 49–61 (1997).Google Scholar
  39. 39.
    Cleary A, Gunning BES, Wasteneys GO, Hepler PK: Microtubule and F-actin dynamics at the division site in living Tradescantia stamen hair cells. J Cell Sci 103: 977–988 (1992).Google Scholar
  40. 40.
    Coen ES, Romero JM, Doyle S, Elliot R, Murphy G, Carpenter R: floricaula: a homeotic gene required for flower development in Antirrhinum majus. Cell 63: 1311–1322 (1990).Google Scholar
  41. 41.
    Coen ES: The role of homeotic genes in flower development and evolution. Annu Rev Plant Physiol Plant Mol Biol 42: 241–279 (1991).Google Scholar
  42. 42.
    Coen ES, Meyerowitz EM: The war of the whorls: genetic interactions controlling flower development. Nature 353: 31–37 (1991).Google Scholar
  43. 43.
    Conti GG, Vegetti G, Bassi M, Favali MA: Some ultrastructural and cytochemical observations on Chinese cabbage leaves infected with cauliflower mosaic virus. Virology 47: 694–700 (1972).Google Scholar
  44. 44.
    Cook ME, Graham LE, Botha CEJ, Lavin CA: Comparative ultrastructure of plasmodesmata of Chara and selected bryophytes: toward an elucidation of the evolutionary origin of plant plasmodesmata. Am J Bot 84: 1169–1178 (1997).Google Scholar
  45. 45.
    Cooper B, Schmitz I, Rao ALN, Beachy RN, Dodds JA: Cellto-cell transport of movement-defective cucumber mosaic and tobacco mosaic viruses in transgenic plants expressing heterologous movement protein genes. Virology 216: 208–213 (1996).Google Scholar
  46. 46.
    Cresti M, Lancelle SA, Hepler PK: Structure of the generative cell wall complex after freeze substitution in pollen tubes of Nicotiana and Impatiens. J Cell Sci 88: 373–378 (1987).Google Scholar
  47. 47.
    Cronin S, Verchot J, Haldeman-Cahill R, Schaad MC, Carrington JC: Long-distance movement factor: a transport function of the potyvirus helper component proteinase. Plant Cell 7: 549–559 (1995).Google Scholar
  48. 48.
    Dannenhoffer JM, Schulz A, Skaggs MI, Bostwick DE, Thompson GA: Expression of the phloem lectin is developmentally linked to vascular differentiation in cucurbits. Planta 201: 405–414 (1997).Google Scholar
  49. 49.
    D'Arcy CJ, de Zoeten GA: Beet western yellows virus in phloem tissue of Thlaspi arvense. Phytopathology 69: 1194–1198 (1979).Google Scholar
  50. 50.
    Davison EM: Cell to cell movement of tobacco ringspot virus. Virology 37: 694–696 (1969).Google Scholar
  51. 51.
    De Jong W, Ahlquist P: A hybrid plant RNA virus made by transferring the noncapsid movement protein from a rodshaped to an icosahedral virus is competent for systemic infection. Proc Natl Acad Sci USA 89: 6808–6812 (1992).Google Scholar
  52. 52.
    Dehesh K, Smith LG, Tepperman JM, Quail PH: Twin authonomous bipartite nuclear localization signals direct nuclear import of GT-2. Plant J 8: 25–36 (1995).Google Scholar
  53. 53.
    Deom CM, Oliver MJ, Beachy RN: The 30–kilodalton gene product of tobacco mosaic virus potentiates virus movement. Science 337: 389–394 (1987).Google Scholar
  54. 54.
    Deom CM, Schubert KR, Wolf S, Holt C, Lucas WJ, Beachy RN: Molecular characterization and biological function of the movement protein of tobacco mosaic virus in transgenic plants. Proc Natl Acad Sci USA 87: 3284–3288 (1990).Google Scholar
  55. 55.
    Deom CM, Lapidot M, Beachy RN: Plant virus movement proteins. Cell 69: 221–224 (1992).Google Scholar
  56. 56.
    Derrick PM, Carter SA, Nelson RS: Mutation of the tobacco mosaic tobamovirus 126–and 183–kDa proteins: effects on phloem-dependent virus accumulation and synthesis of viral proteins. Mol Plant-Microbe Interact 10: 589–596 (1997).Google Scholar
  57. 57.
    Dickinson VJ, Halder J, Woolston CJ: The product of maize streak virus ORF V1 is associated with secondary plasmodesmata and is first detected with the onset of viral lesions. Virology 220: 51–59 (1996).Google Scholar
  58. 58.
    Di Franco A, Martelli GP, Russo M: An ultrastructural study of olive latent ringspot virus in Gomphrena globosa. J Submicrosc Cytol 15: 539–548 (1983).Google Scholar
  59. 59.
    Ding B, Parthasarathy MV, Niklas K, Turgeon R: A morphometric analysis of the phloem-unloading pathway in developing tobacco leaves. Planta 176: 307–318 (1988).Google Scholar
  60. 60.
    Ding B, Haudenshield JS, Hull RJ, Wolf S, Beachy RN, Lucas WJ: Secondary plasmodesmata are specific sites of localization of the tobacco mosaic virus movement protein in transgenic tobacco plants. Plant Cell 4: 915–928 (1992).Google Scholar
  61. 61.
    Ding B, Turgeon R, Parthasarathy MV: Substructure of freeze-substituted plasmodesmata. Protoplasma 169: 28–41 (1992).Google Scholar
  62. 62.
    Ding B, Haudenshield JS, Willmitzer L, Lucas WJ: Correlation between arrested secondary plasmodesmal development and onset of accelerated leaf senescence in yeast acid invertase transgenic tobacco plants. Plant J 4: 179–189 (1993).Google Scholar
  63. 63.
    Ding B, Li Q-b, Nguyen L, Palukaitis P, Lucas WJ: Cucumber mosaic virus 3a protein potentiates cell-to-cell trafficking of CMV vRNA in tobacco plants. Virology 207: 345–353 (1995).Google Scholar
  64. 64.
    Ding B, Kwon MO, Warnberg L: Evidence that actin filaments are involved in controlling the permeability of plasmodesmata in tobacco mesophyll. Plant J 10: 157–164 (1996).Google Scholar
  65. 65.
    Ding B, Lucas WJ: Secondary plasmodesmata: Biogenesis, special functions, and evolution. In: Smallwood M, Knox P, Bowles D (eds) Membranes: Specialized Functions in Plants, pp. 489–506. BIOS Scientific Publishers, Oxford (1996).Google Scholar
  66. 66.
    Ding B: Cell-to-cell transport of macromolecules through plasmodesmata: a novel signalling pathway in plants. Trends Cell Biol 7: 5–9 (1997).Google Scholar
  67. 67.
    Ding B: Tissue preparation and substructure of plasmodesmata. In: van Kesteren P, van Bel A (eds) Plasmodesmata: Nanochannels with Megatasks. Springer-Verlag, Berlin/Heidelberg/New York (in press).Google Scholar
  68. 68.
    Ding B, Itaya A, Woo Y-M: Plasmodesmata and cell-to-cell communication in plants. Int Rev Cytol (in press).Google Scholar
  69. 69.
    Ding XS, Shintaku MH, Arnold SA, Nelson RS: Accumulation of mild and severe strains of tobacco mosaic virus in minor veins of tobacco. Mol Plant-Microbe Interact 8: 32–40 (1995).Google Scholar
  70. 70.
    Ding XS, Shintaku MH, Carter SA, Nelson RS: Invasion of minor veins of tobacco leaves inoculated with tobacco mosaic virus mutants defective in phloem-dependent movement. Proc Natl Acad Sci USA 93: 11155–11160 (1996).Google Scholar
  71. 71.
    Ding XS, Carter SA, Deom CM, Nelson RS: Tobamovirus and potyvirus accumulation in minor veins of inoculated leaves from representatives of the Solanaceae and Fabaceae. Plant Physiol 116: 125–136 (1998).Google Scholar
  72. 72.
    Dingwall C, Sharnick SV, Laskey RA: A polypeptide domain that specifies migration of nucleoplasmin into the nucleus. Cell 30: 449–458 (1982).Google Scholar
  73. 73.
    Dolja VV, Haldeman R, Robertson NL, Dougherty WG, Carrington JC: Distinct functions of capsid protein in assembly and movement of tobacco etch potyvirus in plants. EMBO J 13: 1482–1491 (1994).Google Scholar
  74. 74.
    Dolja VV, Haldeman-Cahill R, Montgomery AE, Vanden-Bosch KA, Carrington JC: Capsid protein determinants involved in cell-to-cell and long distance movement of tobacco etch potyvirus. Virology 207: 1007–1016 (1995).Google Scholar
  75. 75.
    Donald RGK, Lawrence DM, Jackson AO: The barley stripe mosaic virus 58–kilodalton ßb protein is a multifunctional RNA binding protein. J Virol 71: 1538–1546 (1997).Google Scholar
  76. 76.
    Dorokhov YuL, Alexandrova NM, Miroshnichenko NA, Atabekov JG: The informosome-like virus-specific ribonucleoprotein (vRNP) may be involved in the transport of tobacco mosaic virus infection. Virology 137: 127–134 (1984).Google Scholar
  77. 77.
    Ehlers K, Kollmann R: Formation of branched plasmodesmata in regenerating Solanum nigrum-protoplasts. Planta 199: 126–138 (1996).Google Scholar
  78. 78.
    Endrizzi, Moussian B, Haecker A, Levin JZ, Laux T: The SHOOT MERISTEMLESS gene is required for maintenance of undifferentiated cells in Arabidopsis shoot and floral meristems and acts at a different regulatory level than the meristem genes WUSCHEL and ZWILLE. Plant J 10: 967–979 (1996).Google Scholar
  79. 79.
    Epel BL, van Lent JWM, Cohen L, Kotlozky G, Katz A, Yahalom A: A 41 kDa protein isolated from maize mesocotyl cell walls immunolocalizes to plasmodesmata. Protoplasma 191: 70–78 (1996).Google Scholar
  80. 80.
    Esau K, Cronshaw J, Hoefert LL: Relation of beet yellows virus to the phloem and to movement in the sieve tube. J Cell Biol 32: 71–87 (1967).Google Scholar
  81. 81.
    Esau K, Thorsch J: Sieve plate pores and plasmodesmata, the communication channels of the symplast: ultrastructural aspects and developmental relations. Am J Bot 72: 1641–1653 (1985).Google Scholar
  82. 82.
    Feldherr CM, Kallenbach E, Schultz N: Movement of karyophilic protein through the nuclear pores of oocytes. J Cell Biol 99: 2216–2222 (1984).Google Scholar
  83. 83.
    Fisher D, Wu Y, Ku MSB: Turnover of soluble proteins in the wheat sieve tube. Plant Physiol 100: 1433–1441 (1992).Google Scholar
  84. 84.
    Flanders DJ, Rawlins DJ, Shaw PJ, Lloyd CW: Nucleusassociated microtubules help determine the division plane of plant epidermal cells: avoidance of four-way junctions and the role of cell geometry. J Cell Biol 110: 1111–1122 (1990).Google Scholar
  85. 85.
    Forster RLS, Beck DL, Guilford PJ, Voot DM, Van Dolleweerd CJ, Andersen MT: The coat protein of white clover mosaic potexvirus has a role in facilitating cell-to-cell transport in plants. Virology 191: 480–484 (1992).Google Scholar
  86. 86.
    Franceschi VR, Ding B, Lucas WJ: Mechanism of plasmodesmata formation in characean algae in relation to evolution of intercellular communication in higher plants. Planta 192: 347–358 (1994).Google Scholar
  87. 87.
    Fujiwara T, Giesman-Cookmeyer D, Ding B, Lommel SA, Lucas WJ: Cell-to-cell trafficking of macromolecules through plasmodesmata potentiated by the red clover necrotic mosaic virus movement protein. Plant Cell 5: 1783–1794 (1993).Google Scholar
  88. 88.
    Gal-On A, Kaplan I, Roossinck MJ, Palukaitis P: The kinetics of infection of zucchini squash by cucumber mosaic virus indicate a function for RNA1 in virus movement. Virology 205: 280–289 (1994).Google Scholar
  89. 89.
    Gamalei YV, van Bel AJE, Pakhomova MV, Sjutkina A: Effects of temperature on the conformation of the endoplasmic reticulum and on starch accumulation in leaves with the symplasmic minor-vein configuration. Planta 194: 443–453 (1994).Google Scholar
  90. 90.
    Ghoshroy S, Lartley R, Sheng J, Citovsky V: Transport of proteins and nucleic acids through plasmodesmata. Annu Rev Plant Physiol Plant Mol Biol 48: 27–50 (1997).Google Scholar
  91. 91.
    Gibbs A: Viruses and plasmodesmata. In: Gunning BES, Robards RW (eds) Intercellular Communication in Plants: Studies on Plasmodesmata, pp. 149–164. Springer-Verlag, Berlin/Heidelberg/New York (1976).Google Scholar
  92. 92.
    Gilkey JC, Staehelin LA: Advances in ultrarapid freezing for the preservation of cellular ultrastructure. J Electron Microsc Techn 3: 177–210 (1986).Google Scholar
  93. 93.
    Giesman-Cookmeyer D, Lommel SA: Alanine scanning mutagenesis of a plant virus movement protein identifies three functional domains. Plant Cell 5: 973–982 (1993).Google Scholar
  94. 94.
    Giesman-Cookmeyer D, Silver S, Vaewhongs AA, Lommel SA, Deom CM: Tobamovirus and dianthovirus movement proteins are functionally homologous. Virology 213: 38–45 (1995).Google Scholar
  95. 95.
    Gilbertson RL, Lucas WJ: How do viruses traffic on the ‘vascular highway'? Trends Plant Sci 1: 260–268 (1996).Google Scholar
  96. 96.
    Gilmer D, Bouzoubaa S, Hein A, Guilley H, Richards K, Jonard G: Efficient cell-to-cell movement of beet necrotic yellow vein virus requires 30 proximal genes located on RNA2. Virology 189: 40–47 (1992).Google Scholar
  97. 97.
    Goodrick BJ, Kuhn CW, Hussey RS: Restricted systemic movement of cowpea chlorotic mottle virus in soybean with nonnecrotic resistance. Phytopathology 81: 1426–1431 (1991).Google Scholar
  98. 98.
    Goodwin PB: Molecular size limit for movement in the symplast of the Elodea leaf. Planta 157: 124–130 (1983).Google Scholar
  99. 99.
    Grabski S, de Feijter AW, Schindler M: Endoplasmic reticulum forms a dynamic continuum for lipid diffusion between contiguous soybean root cells. Plant Cell 5: 25–38 (1993).Google Scholar
  100. 100.
    Hake S, Freeling M: Analysis of genetic mosaics shows that the extra epidermal cell divisions in Knotted mutant maize plants are induced by adjacent mesophyll cells. Nature 320: 621–623 (1986).Google Scholar
  101. 101.
    Hake S, Char BR: Cell-to-cell interactions during plant development. Genes Devel 11: 1087–1097 (1997).Google Scholar
  102. 102.
    Haley A, Hunter T, Kiberstis P, Zimmern D: Multiple serine phosphorylation sites on the 30 kDa TMV cell-to-cell movement protein synthesized in tobacco protoplasts. Plant J 8: 715–724 (1995).Google Scholar
  103. 103.
    Hantke SS, Carpenter R, Coen, ES: Expression of floricaula in single cell layers of perichimeras activates downstream homeotic genes in all layers of floral meristems. Development 121: 27–35 (1995).Google Scholar
  104. 104.
    Hearon SS, Lawson RH: Effects of light intensity, photoperiod, and temperature on symptom expression and host and virus ultrastructure in Saponaria vaccaria infected with carnation etched ring virus. Phytopathology 71: 645–652 (1981).Google Scholar
  105. 105.
    Heese-Peck A, Raikhel NV: The nuclear pore complex. Plant Mol Biol (this issue).Google Scholar
  106. 106.
    Heinlein M, Epel BL, Padgett HS, Beachy RN: Interaction of tobamovirus movement proteins with the plant cytoskeleton. Science 270: 1983–1985 (1995).Google Scholar
  107. 107.
    Hensel W: Caffeine-induced alterations in the generation and cytodifferentiation of root cap cells from cress (Lepidium sativum L.). Euro J Cell Biol 43: 208–214 (1987).Google Scholar
  108. 108.
    Hepler PK: Endoplasmic reticulum in the formation of the cell plate and plasmodesmata. Protoplasma 111: 121–133 (1982).Google Scholar
  109. 109.
    Hepler PK, Cleary AL, Gunning BES, Wadsworth P, Wasteneys GO, Zhang DH: Cytoskeletal dynamics in living plant cells. Cell Biol Int 17: 127–142 (1993).Google Scholar
  110. 110.
    Hirokawa N: Kinesin and dynein superfamily proteins and the mechanism of organelle transport. Science 279: 519–526 (1998).Google Scholar
  111. 111.
    Howard EA, Zupan JR, Citovsky V, Zambryski PC: The VirD2 protein of A. tumefaciens contains a C-terminal bipartite nuclear localization signal: implications for nuclear uptake of DNA in plant cells. Cell 68: 109–118 (1992).Google Scholar
  112. 112.
    Ishiwatari Y, Honda C, Kawashima I, Nakamura S-i, Hirano H, Mori S, Fujiwara T, Hayashi H, Chino M: Thioredoxin h is one of the major proteins in rice phloem sap. Planta 195: 456–463 (1995).Google Scholar
  113. 113.
    Ishiwatari Y, Fujiwara T, McFarland KC, Nemoto K, Hayashi H, Chino M, Lucas WJ: Rice phloem thioredoxin h has the capacity to mediate its own cell-to-cell transport. Planta 205: 12–22 (1998).Google Scholar
  114. 114.
    Itaya A, Hickman H, Bao Y, Nelson R, Ding B: Cell-tocell trafficking of cucumber mosaic virus movement protein: green fluorescent protein fusion produced by biolistic gene bombardment in tobacco. Plant J 12: 1223–1230 (1997).Google Scholar
  115. 115.
    Ivanov KI, Ivanov PA, Timofeeva EK, Dorokhov YuriL, Atabekov JG: The immobilized movement proteins of two tobamoviruses form stable ribonucleoprotein complexes with full-length viral genomic RNA. FEBS Lett 346: 217–220 (1994).Google Scholar
  116. 116.
    Jacinto T, McGurl B, Franceschi V, Delano-Freier J, Ryan CA: Tomato prosystemin promoter confers wound-inducible, vascular bundle-specific expression of the β-glucuronidase gene in transgenic tomato plants. Planta 203: 406–412 (1997).Google Scholar
  117. 117.
    Jackson D, Veit B, Hake S: Expression of maize KNOTTED1 related homeobox genes in the shoot apical meristem predicts patterns of morphogenesis in the vegetative shoot. Development 120: 405–413 (1994).Google Scholar
  118. 118.
    Jackson D, Hake S: Morphogenesis on the move: cell-tocell trafficking of plant regulatory proteins. Curr Opin Genet Devel 7: 495–500 (1997).Google Scholar
  119. 119.
    Jones MGK: The origin and development of plasmodesmata. In: Gunning BES, Robards RW (eds) Intercellular Communication in Plants: Studies on Plasmodesmata, pp. 81–105. Springer-Verlag, Berlin/Heidelberg/New York (1976).Google Scholar
  120. 120.
    Jorgensen RA, Atkinson RG, Forster RLS, Lucas WJ: An RNA-based information superhighway in plants. Science 279: 1486–1487 (1998).Google Scholar
  121. 121.
    Kalderon D, Richardson WD, Markham AF, Smith AE: Sequence requirements for nuclear location of simian virus 40 large-T antigen. Nature 311: 33–38 (1984).Google Scholar
  122. 122.
    Kalinina NO, Fedorkin ON, Samuilova OV, Maiss E, Korpela T, Morozov SYu, Atabekov JG: Expression and biochemical analyses of the recombinant potato virus X 25K movement protein. FEBS Lett 397: 75–78 (1996).Google Scholar
  123. 123.
    Karpova OV, Ivanov KI, Rodionova NP, Dorokhov YuL, Atabekov JG: Nontranslatability and dissimilar behavior in plants and protoplasts of viral RNA and movement protein complexes formed in vitro. Virology 230: 11–21 (1997).Google Scholar
  124. 124.
    Kasschau KD, Cronin S, Carrington JC: Genome ampli-fication and long-distance movement functions associated with the central domain of tobacco etch potyvirus helper component-proteinase. Virology 228: 251–262 (1997).Google Scholar
  125. 125.
    Kasteel DTJ, Perbal M-C, Boyer J-C, Wellink J, Goldbach RW, Maule AJ, van Lent JWM: The movement proteins of cowpea mosaic virus and cauliflower mosaic virus induce tubular structures in plant and insect cells. J Gen Virol 77: 2857–2864 (1996).Google Scholar
  126. 126.
    Kasteel DTJ, Wellink J, Goldbach RW, van Lent JWM: Isolation and characterization of tubular structures of cowpea mosaic virus. J Gen Virol 78: 3167–3170 (1997).Google Scholar
  127. 127.
    Kasteel DTJ, van der Wel, Jansen KAJ, Goldbach RW, van Lent JWM: Tubule-forming capacity of the movement proteins of alfalfa mosaic virus and brome mosaic virus. J Gen Virol 78: 2089–2093 (1997).Google Scholar
  128. 128.
    Kempers R, van Bel AJE: Symplasmic connections between sieve element and companion cell in the stem phloem of Vicia faba L. have a molecular exclusion limit of at least 10 kDa. Planta 201: 195–201 (1997).Google Scholar
  129. 129.
    Kerstetter RA, Laudencia-Chingcuanco D, Smith L, Hake S: Loss of function mutations in the maize homeobox gene, knotted1, are defective in shoot meristem maintainence. Development 124: 3045–3054 (1997).Google Scholar
  130. 130.
    Kikkert M, van Poelwijk F, Storms M, Kassies W, Bloksma H, van Lent J, Kormelink R, Goldbach R: A protoplast system for studying tomato spotted wilt virus infection. J Gen Virol 78: 1755–1763 (1997).Google Scholar
  131. 131.
    Kim KS, Fulton JP: Tubules with virus like particles in leaf cells infected with bean pod mottle virus. Virology 43: 329–337 (1971).Google Scholar
  132. 132.
    Kim KS, Fulton JP, Scott HA: Osmiophilic globules and myelinic bodies in cells infected with two comoviruses. J Gen Virol 25: 445–452 (1974).Google Scholar
  133. 133.
    Kim KS, Lee KW: Geminivirus-induced macrotubules and their suggested role in cell-to-cell movement. Phytopathology 82: 664–669 (1992).Google Scholar
  134. 134.
    Kollmann R, Glockmann C: Studies on graft unions. I. Plasmodesmata between cells of plants belonging to different unrelated taxa. Protoplasma 124: 224–235 (1985).Google Scholar
  135. 135.
    Kollmann R, Glockmann C: Studies on graft unions. III. On the mechanism of secondary formation of plasmodesmata at the graft interface. Protoplasma 165: 71–85 (1991).Google Scholar
  136. 136.
    Koonin EV, Mushegian AR, Ryabov EV, Dolja VV: Diverse groups of plant RNA and DNA viruses share related movement proteins that may possess chaperone-like activity. J Gen Virol 72: 2895–2903 (1991).Google Scholar
  137. 137.
    Kormelink R, Storms M, van Lent J, Peters D, Goldbach R: Expression and subcellular location of the NSm protein of tomato spotted wilt virus (TSWV), a putative viral movement protein. Virology 200: 56–65 (1994).Google Scholar
  138. 138.
    Kragler F, Lucas WJ, Monzer J: Plasmodesmata: dynamics, domains and patterning. Ann Bot 81: 1–10 (1998).Google Scholar
  139. 139.
    Kubo S, Takanami Y: Infection of tobacco mesophyll protoplasts with tobacco necrotic dwarf virus, a phloem-limited virus. J Gen Virol 42: 387–398 (1979).Google Scholar
  140. 140.
    Kühn C, Franceschi VR, Schulz A, Lemoine R, Frommer WB: Macromolecular trafficking indicated by localization and turnover of sucrose transporters in enucleate sieve elements. Science 275: 1298–1300 (1997).Google Scholar
  141. 141.
    Langenberg WG: Virus protein association with cylindrical inclusions of two viruses that infect wheat. J Gen Virol 67: 1161–1168 (1986).Google Scholar
  142. 142.
    Lawson RH, Hearon SS: Ultrastructure of carnation etched ring virus-infected Saponaria vaccaria and Dianthus caryophyllus. J Ultrastruct Res 48: 201–215 (1973).Google Scholar
  143. 143.
    Li Q, Palukaitis P: Comparison of the nucleic acid-and NTP-binding properties of the movement protein of cucumber mosaic cucumovirus and tobacco mosaic tobamovirus. Virology 216: 71–79 (1996).Google Scholar
  144. 144.
    Linstead PJ, Hills GJ, Plaskitt KA, Wilson IG, Harker CL, Maule AJ: The subcellular location of the gene 1 product of cauliflower mosaic virus is consistent with a function associated with virus spread. J Gen Virol 69: 1809–1818 (1988).Google Scholar
  145. 145.
    Liu H, Boulton MI, Davies JW: Maize streak virus coat protein binds single-and double-stranded DNAin vitro. J Gen Virol 78: 1265–1270 (1997).Google Scholar
  146. 146.
    Long JA, Moan EI, Medford JI, Barton MK: A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379: 66–69 (1996).Google Scholar
  147. 147.
    Long RM, Singer RH, Meng X, Gonzalez I, Nasmyth K, Jansen R-P: Mating type switching in yeast controlled by asymmetric localization of ASH1 mRNA. Science 277: 383–387 (1997).Google Scholar
  148. 148.
    Lucas WJ, Ding B, van der Schoot C: Plasmodesmata and the supracellular nature of plants. New Phytol 125: 435–476 (1993).Google Scholar
  149. 149.
    Lucas WJ, Wolf S: Plasmodesmata: the intercellular organelles of green plants. Trends Cell Biol 3: 308–315 (1993).Google Scholar
  150. 150.
    Lucas WJ, Gilbertson RL: Plasmodesmata in relation to viral movement within leaf tissues. Annu Rev Phytopath 32: 387–411 (1994).Google Scholar
  151. 151.
    Lucas WJ: Plasmodesmata: intercellular channels for macromolecular transport in plants. Curr Opin Cell Biol 7: 673–680 (1995).Google Scholar
  152. 152.
    Lucas WJ, Bouché-Pillon S, Jackson DP, Nguyen L, Baker L, Ding B, Hake S: Selective trafficking of KNOTTED1 homeodomain protein and its mRNA through plasmodesmata. Science 270: 1980–1983 (1995).Google Scholar
  153. 153.
    Maia IG, Bernadi F: Nucleic acid-binding properties of a bacterially expressed potato virus Y helper componentproteinase. J Gen Virol 77: 869–877 (1996).Google Scholar
  154. 154.
    Malyshenko SI, Kondakova OA, Taliansky ME, Atabekov JG: Plant virus transport function: Complementation by helper viruses is non-specific. J Gen Virol 70: 2751–2757 (1989).Google Scholar
  155. 155.
    McGurl B, Pearce G, Orozco-Cardenas M, Ryan CA: Structure, expression, and antisense inhibition of the systemin precursor gene. Science 255: 1570–1573 (1992).Google Scholar
  156. 156.
    McLean BG, Zupan J, Zambryski PC: Tobacco mosaic virus movement protein associates with the cytoskeleton in tobacco cells. Plant Cell 7: 2101–2114 (1995).Google Scholar
  157. 157.
    McLean BG, Hempel FD, Zambryski PC: Plant intercellular communication via plasmodesmata. Plant Cell 9: 1043–1054 (1997).Google Scholar
  158. 158.
    Mehlin H, Daneholt B, Skoglund U: Translocation of a specific premessenger ribonucleoprotein particle through the nuclear pore studied with electron microscope tomography. Cell 69: 605–613 (1992).Google Scholar
  159. 159.
    Melcher U: Similarities between putative transport proteins of plant viruses. J Gen Virol 71: 1009–1018 (1990).Google Scholar
  160. 160.
    Mermall V, Post PL, Mooseker MS: Unconventional myosins in cell movement, membrane traffic, and signal transduction. Science 279: 527–533 (1998).Google Scholar
  161. 161.
    Meshi T, Watanabe Y, Saito T, Sugimoto A, Maeda T, Okada Y: Function of the 30 kd protein of tobacco mosaic virus: involvement in cell-to-cell movement and dispensability for replication. EMBO J 6: 2557–2563 (1987).Google Scholar
  162. 162.
    Mezitt LA, Lucas WJ: Plasmodesmal cell-to-cell transport of proteins and nucleic acids. Plant Mol Biol 32: 251–273 (1996).Google Scholar
  163. 163.
    Moore PJ, Fenczik CA, Deom CM, Beachy RN: Developmental changes in plasmodesmata in transgenic tobacco expressing the movement protein of tobacco mosaic virus. Protoplasma 170: 115–127 (1992).Google Scholar
  164. 164.
    Moreland RB, Nam HG, Hereford LM, Fried HM: Identifi-cation of a nuclear localization signal of a yeast ribosomal protein. Proc Natl Acad Sci USA 82: 6561–6565 (1985).Google Scholar
  165. 165.
    Morozov SYu, Dolja VV, Atabekov JG: Probable reassortment of genomic elements among elongated RNA-containing plant viruses. J Mol Evol 29: 52–62 (1989).Google Scholar
  166. 166.
    Morozov SYu, Fedorkin ON, Jüttner G, Schiemann J, Baulcombe DC, Atabekov JG: Complementation of a potato virus X mutant mediated by bombardment of plant tissues with cloned viral movement protein genes. J Gen Virol 78: 2077–2083 (1997).Google Scholar
  167. 167.
    Muench DG, Wu Y, Coughlan SJ, Okita TW: Evidence for a cytoskeleton-associated binding site involved in prolamine mRNA localization to the protein bodies in rice endosperm tissue. Plant Physiol 116: 559–569 (1998).Google Scholar
  168. 168.
    Murillo I, Cavallarin L, Segundo B San: The maize pathogenesis-related PRms protein localizes to plasmodesmata in maize radicles. Plant Cell 9: 145–156 (1997).Google Scholar
  169. 169.
    Nagano H, Okuno T, Mise K, Furusawa I: Deletion of the Cterminal 33 amino acids of cucumber mosaic virus movement protein enables a chimeric brome mosaic virus to move from cell to cell. J Virol 71: 2270–2276 (1997).Google Scholar
  170. 170.
    Nakamura S, Hayashi H, Mori S, Chino M: Protein phosphorylation in the sieve tubes of rice plants. Plant Cell Physiol 34: 927–933 (1993).Google Scholar
  171. 171.
    Narváez-Vásquez J, Pearce G, Orozco-Cardenas ML, Franceschi VR, Ryan CA: Autoradiographic and biochemical evidence for the systemic translocation of systemin in tomato plants. Planta 195: 593–600 (1995).Google Scholar
  172. 172.
    Nejidat A, Cellier F, Holt CA, Gafny R, Eggenberger AL, Beachy RN: Transfer of the movement protein gene between two tobamoviruses: influence on local lesion development. Virology 180: 318–326 (1991).Google Scholar
  173. 173.
    Nelson RS, van Bel AJE: The mystery of virus trafficking into, through and out of vascular tissue. Prog Bot 59: 476–533 (1998).Google Scholar
  174. 174.
    Newmeyer DD, Forbes DJ: Nuclear import can be separated into distinct steps in vitro: nuclear pore binding and translocation. Cell 52: 641–653 (1988).Google Scholar
  175. 175.
    Nguyen L, Lucas WJ, Ding B, Zaitlin M: Viral RNA traf-ficking is inhibited in replicase-mediated resistant transgenic tobacco plants. Proc Natl Acad Sci USA 93: 12643–12647 (1996).Google Scholar
  176. 176.
    Noueiry AO, Lucas WJ, Gilbertson RL: Two proteins of a plant DNA virus coordinate nuclear and plasmodesmal transport. Cell 76: 925–932 (1994).Google Scholar
  177. 177.
    Okita TW, Choi S-B, Ito H, Muench DG, Wu Y, Zhang F: Entry into the secretory system-the role of mRNA localization. J Exp Bot (in press).Google Scholar
  178. 178.
    Oparka KJ, Prior DAM: Direct evidence for pressuregenerated closure of plasmodesmata. Plant J 2: 741–750 (1992).Google Scholar
  179. 179.
    Oparka KJ, Roberts AG, Roberts IM, Prior DAM, Santa Cruz S: 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 (1996).Google Scholar
  180. 180.
    Oparka KJ, Prior DAM, Santa Cruz S, Padgett HS, Beachy RN: Gating of epidermal plasmodesmata is restricted to the leading edge of expanding infection sites of tobacco mosaic virus (TMV). Plant J 12: 781–789 (1997).Google Scholar
  181. 181.
    Osman TAM, Hayes RJ, Buck KW: Cooperative binding of the red clover necrotic mosaic virus movement protein to single-stranded nucleic acids. J Gen Virol 73: 223–227 (1992).Google Scholar
  182. 182.
    Overall RL, Blackman LM: A model for the macromolecular structure of plasmodesmata. Trends Plant Sci 1: 307–311 (1996).Google Scholar
  183. 183.
    Padgett HS, Epel BL, Kahn TW, Heinlein M, Watanabe Y, Beachy RN: Distribution of tobamovirus movement protein in infected cells and implications for cell-to-cell spread of infection. Plant J 10: 1079–1088 (1996).Google Scholar
  184. 184.
    Pante N, Aebi U: Sequential binding of import ligands to distinct nucleopore regions during their nuclear import. Science 273: 1729–1731 (1996).Google Scholar
  185. 185.
    Parthasarathy, MV: Sieve-element structure. In: Zimmermann MH, Milburn JA (eds) Encyclopedia of Plant Physiology, New Series: Transport in Plants I. Phloem Transport. Volume 1, pp. 3–38. Springer-Verlag, Berlin (1975).Google Scholar
  186. 186.
    Parthasarathy MV: F-actin architecture in coleoptile epidermal cells. Eur J Cell Biol 39: 1–12 (1985).Google Scholar
  187. 187.
    Parthasarathy MV, Perdue TD, Witztum A, Alvernaz J: Actin network as a normal component of the cytoskeleton in many vascular plant cells. Am J Bot 72: 1318–1323 (1985).Google Scholar
  188. 188.
    Pascal E, Sanderfoot AA, Ward BM, Medville R, Turgeon R, Lazarowitz SG: The geminivirus BR1 movement protein binds single-stranded DNA and localizes to the cell nucleus. Plant Cell 6: 995–1006 (1994).Google Scholar
  189. 189.
    Pearce G, Strydom D, Johnson S, Ryan CA: A polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins. Science 253: 895–898 (1991).Google Scholar
  190. 190.
    Pearce G, Johnson S, Ryan CA: Structure-activity of deleted and substituted systemin, an 18–amino acid polypeptide inducer of plant defensive genes. J Biol Chem 268: 212–216 (1993).Google Scholar
  191. 191.
    Pearce RH, Grimmer BJ: Calibration of agarose columns for gel chromatography with commercially available dextran fractions. J Chromatogr 150: 548–553 (1978).Google Scholar
  192. 192.
    Perbal M-C, Thomas CL, Maule AJ: Cauliflower mosaic virus gene I product (PI) forms tubular structures which extend from the surface of infected protoplasts. Virology 195: 281–285 (1993).Google Scholar
  193. 193.
    Perbal M-C, Haughn G, Saedler H, Schwarz-Sommer Z: Non-autonomous function of the Antirrhinum floral homeotic proteins DEFICIENS and GLOBOSA is exerted by their polar cell-to-cell trafficking. Development 122: 3433–3441 (1996).Google Scholar
  194. 194.
    Petty ITD, Jackson AO: Mutational analysis of barley stripe mosaic virus RNAâ. Virology 179: 712–718 (1990).Google Scholar
  195. 195.
    Picard D, Yamamoto KR: Two signals mediate hormonedependent nuclear localization of the glucocorticoid receptor. EMBO J 6: 3333–3340 (1987).Google Scholar
  196. 196.
    Radford JE, White RG: Localisation of a myosin-like protein to plasmodesmata. Plant J (in press).Google Scholar
  197. 197.
    Rao ALN: Molecular studies on bromovirus capsid protein. III. Analysis of cell-to-cell movement competence of coat protein defective variants of cowpea chlorotic mottle virus. Virology 232: 385–395 (1997).Google Scholar
  198. 198.
    Raven JA: Long-term functioning of enucleate sieve elements: possible mechanisms of damage avoidance and damage repair. Plant Cell Environ 14: 139–146 (1991).Google Scholar
  199. 199.
    Richardson WD, Mills AD, Dilworth SM, Laskey RA, Dingwall C: Nuclear protein migration involves two steps: rapid binding at the nuclear envelope followed by slower translocation through nuclear pores. Cell 52: 655–644 (1988).Google Scholar
  200. 200.
    Ritzenthaler C, Schmit A-C, Michler P, Stussi-Garaud C, Pinck L: Grapevine fanleaf nepovirus p38 putative movement protein is located on tubules in vivo. Mol Plant-Microbe Interact 8: 379–387 (1995).Google Scholar
  201. 201.
    Robards AW, Lucas WJ: Plasmodesmata. Annu Rev Plant Physiol Plant Mol Biol 41: 369–419 (1990).Google Scholar
  202. 202.
    Roberts IM, Harrison BD: Inclusion bodies and tubular structures in Chenopodium amaranticolor plants infected with strawberry latent ringspot virus. J Gen Virol 7: 47–54 (1970).Google Scholar
  203. 203.
    Rojas MR, Zerbini FM, Allison RF, Gilbertson RL, Lucas WJ: Capsid protein and helper component-proteinase function as potyvirus cell-to-cell movement proteins. Virology 237: 283–295 (1997).Google Scholar
  204. 204.
    Rouleau M, Smith RJ, Bancroft JB, Mackie GA: Purification, properties, and subcellular localization of foxtail mosaic potexvirus 26–kDa protein. Virology 204: 254–265 (1994).Google Scholar
  205. 205.
    Rouleau M, Smith RJ, Bancroft JB, Mackie GA: Subcellular immunolocalization of the coat protein of two potexviruses in infected Chenopodium quinoa. Virology 214: 314–318 (1995).Google Scholar
  206. 206.
    Rupasov VV, Morozov SYu, Kanyuka KV, Zavriev SK: Partial nucleotide sequence of potato virus M RNA shows similarities to potexviruses in gene arrangement and the encoded amino acid sequences. J Gen Virol 70: 1861–1869 (1989).Google Scholar
  207. 207.
    Russin WA, Evert RF, Vanderveer PJ, Sharkey TD, Briggs SP: Modification of a specific class of plasmodesmata and loss of sucrose export ability in the sucrose export defective1 maize mutant. Plant Cell 8: 645–658 (1996).Google Scholar
  208. 208.
    Russo M, Castellano MA, Martelli GP: The ultrastructure of broad bean stain and broad bean true mosaic virus infections. J Submicrosc Cytol 14: 149–160 (1982).Google Scholar
  209. 209.
    Sack FD, Kiss JZ: Root-cap structure in wild type and in a starchless mutant of Arabidopsis. Am J Bot 76: 454–464 (1989).Google Scholar
  210. 210.
    Sakuth T, Schobert C, Pecsvaradi A, Eichholz A, Komor E, Orlich G: Specific proteins in the sieve-tube exudate of Ricinus communis L. seedlings: separation, characterization and in vivo labelling. Planta 191: 207–213 (1993).Google Scholar
  211. 211.
    Sanderfoot AA, Lazararowitz SG: 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 (1995).Google Scholar
  212. 212.
    Sanderfoot AA, Ingham DJ, Lazarowitz SG: 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 (1996).Google Scholar
  213. 213.
    Sanderfoot AA, Lazarowitz SG: Getting it together in plant virus movement: cooperative interactions between bipartite geminivirus movement proteins. Trends Cell Biol 6: 353–358 (1996).Google Scholar
  214. 214.
    Sanger M, Passmore B, Falk BW, Bruening G, Ding B, Lucas WJ: Symptom severity of beet western yellows virus strain ST9 is conferred by the ST9–associated RNA and is not associated with virus release from the phloem. Virology 200: 48–55 (1994).Google Scholar
  215. 215.
    Santos B, Snyder M: Targeting of chitin synthase 3 to polarized growth sites in yeast requires Chs5p and Myo2p. J Cell Biol 136: 95–110 (1997).Google Scholar
  216. 216.
    Satina S, Blakeslee AF, Avery AG: Demonstrations of the three germ layers in the shoot apex of Datura by means of induced polyploidy in periclinal chimeras. Am J Bot 27: 895–905 (1940).Google Scholar
  217. 217.
    Schaller A, Ryan CA: Systemin: a polypeptide defense signal in plants. BioEssays 18: 27–33 (1995).Google Scholar
  218. 218.
    Schmitz I, Rao ALN: Molecular studies on bromovirus capsid protein. I. Characterization of cell-to-cell movementdefective RNA3 variants of brome mosaic virus. Virology 226: 281–293 (1996).Google Scholar
  219. 219.
    Schmitz J, Stussi-Garaud C, Tacke E, Prüfer D, Rohde W, Rohfritsch O: In situ localization of the putative movement protein (pr17) from potato leafroll luteovirus (PLRV) in infected and transgenic potato plants. Virology 235: 311–322 (1997).Google Scholar
  220. 220.
    Schobert C, Großmann P, Gottschalk M, Komor E, Pecsvaradi A, Nieden Uz: Sieve-tube exudate from Ricinus communis L. seedlings contains ubiquitin and chaperones. Planta 196: 205–210 (1995).Google Scholar
  221. 221.
    Schobert C, Baker L, Szederkényi J, Großmann P, Komor E, Hayashi H, Chino M, Lucas WJ: Identification of immunologically related proteins in sieve-tube exudate collected from monocotyledonous and dicotyledonous plants. Planta (in press).Google Scholar
  222. 222.
    Schoumacher F, Erny C, Berna A, Godefroy-Colburn T, Stussi-Garaud C: Nucleic acid-binding properties of the alfalfa mosaic virus movement protein produced in yeast. Virology 188: 896–899 (1992).Google Scholar
  223. 223.
    Schoumacher F, Giovane C, Maira M, Poirson A, Godefroy-Colburn T, Berna A: Mapping of the RNA-binding domain of the alfalfa mosaic virus movement proteins. J Gen Virol 75: 3199–3202 (1994).Google Scholar
  224. 224.
    Schwartz-Sommer Z, Hue I, Huijser P, Flor PJ, Hansen R, Tetens F, Lönnig, WE, Saedler H, Sommer H: Characterization of the Antirrhinum floral homeotic MADS-box gene deficiens: evidence for DNA binding and autoregulation of its persistent expression throughout flower development. EMBO J 11: 251–263 (1992).Google Scholar
  225. 225.
    Scott KP, Kashiwazaki S, Reavy B, Harrison BD: The nucleotide sequence of potato mop-top virus RNA2: a novel type of genome organization for a furovirus. J Gen Virol 75: 3561–3568 (1994).Google Scholar
  226. 226.
    Seagull RW, Falconer MM, Weerdenburg CA: Microfilaments: dynamic arrays in higher plant cells. J Cell Biol 104: 995–1004 (1987).Google Scholar
  227. 227.
    Shieh MW, Wessler SR, Raikhel NV: Nuclear targeting of the maize R protein requires two nuclear localization sequences. Plant Physiol 101: 353–361 (1993).Google Scholar
  228. 228.
    Singer RH: RNA traffic report. Trends Cell Biol 6: 486–489 (1996).Google Scholar
  229. 229.
    Sinha N, Hake S: Mutant characters of Knotted maize leaves are determined in the innermost tissue layers. Devel Biol 141: 203–210 (1990).Google Scholar
  230. 230.
    Sinha NR, Williams RE, Hake S: Overexpression of the maize homeobox gene, KNOTTED-1, causes a switch from determinate to indeterminate cell fates. Genes Devel 7: 787–795 (1993).Google Scholar
  231. 231.
    Sjölund RD: The phloem sieve element: a river runs through it. Plant Cell 9: 1137–1146 (1997).Google Scholar
  232. 232.
    Smirnova EA, Bajer AS: Microtubule converging centers and reorganization of the interphase cytoskeleton and the mitotic spindle in higher plant Haemanthus. Cell Motil Cytoskel 27: 219–233 (1994).Google Scholar
  233. 233.
    Smith LG, Greene B, Veit B, Hake S: A dominant mutation in the maize homeobox gene, Knotted-1, causes its ectopic expression in leaf cells with altered fates. Development 116: 21–30 (1992).Google Scholar
  234. 234.
    Snapp EL, Landfear SM: Cytoskeletal association is important for differential targeting of glucose transporter isoform in Leishmania. J Cell Biol 139: 1775–1783 (1997).Google Scholar
  235. 235.
    Sokolova M, Prüfer D, Tacke E, Rohde W: The potato leafroll virus 17K movement protein is phosphorylated by a membrane-associated protein kinase from potato with biochemical features of protein kinase C. FEBS Lett 400: 201–205 (1997).Google Scholar
  236. 236.
    Solovyev AG, Zelenina DA, Savenkov EI, Grdzelishvili VZ, Morozov SYu, Lesemann D-E, Maiss E, Casper R, Atabekov JG: Movement of a barley stripe mosaic virus chimera with a tobacco mosaic virus mvoement protein. Virology 217: 435–441 (1996).Google Scholar
  237. 237.
    Solovyev AG, Zelenina DA, Savenkov EI, Grdzelishvili VZ, Morozov SYu, Lesemann D-E, Maiss E, Casper R, Atabekov JG: Host controlled cell-to-cell movement of a hybrid barley stripe mosaic virus expressing a dianthovirus movement protein. Intervirology 40: 1–6 (1997).Google Scholar
  238. 238.
    Sommer H, Beltran JP, Huijser P, Pape H, Lönnig WE, Saedler H, Schwartz-Sommer Z: Deficiens, a homeotic gene involved in the control of flower morphogenesis in Antirrhinum majus: the protein shows homology to transcription factors. EMBO J 9: 605–613 (1990).Google Scholar
  239. 239.
    Squire PG: Calculation of hydrodynamic parameters of random coil polymers from size exclusion chromatography and comparison with parameters by conventional methods. J Chromotogr 210: 433–442 (1981).Google Scholar
  240. 240.
    Steinberg G, Kollmann R: A quantitative analysis of the interspecific plasmodesmata in the non-division walls of the plant chimera Laburnocytis adamii (Poit.) Schneid. Planta 192: 75–83 (1994).Google Scholar
  241. 241.
    St Johnston D: The intracellular localization of messenger RNAs. Cell 81: 161–170 (1995).Google Scholar
  242. 242.
    Storms MMH, Kormelink R, Peters D, van Lent JWM, Goldbach RW: The nonstructural NSm protein of tomato spotted wilt virus induces tubular structures in plant and insect cells. Virology 214: 485–493 (1995).Google Scholar
  243. 243.
    Storms MMH, van der Schoot C, Prins M, Kormelink R, van Lent JWW, Goldbach RW: A comparison of two methods of microinjection for assessing altered plasmodesmal gating in tissues expressing viral movement proteins. Plant J 13: 131–140 (1998).Google Scholar
  244. 244.
    Sussex IM: Developmental programming of the shoot meristem. Cell 56: 225–229 (1989).Google Scholar
  245. 245.
    Suzuki M, Kuwata S, Kataoka J, Masuta C, Nitta N, Takanami Y: Functional analysis of deletion mutants of cucumber mosaic virus RNA3 using an in vitro transcription system. Virology 183: 106–113 (1991).Google Scholar
  246. 246.
    Szederkényi J, Komor E, Schobert C: Cloning of the cDNA for glutaredoxin, an abundant sieve-tube exudate protein from Ricinus communis L. and characterisation of the glutathione-dependent thiol-reduction system in sieve tubes. Planta 202: 349–356 (1997).Google Scholar
  247. 247.
    Szymkowiak EJ, Sussex IM: The internal meristem layer (L3) determines floral meristem size and carpel number in tomato periclinal chimeras. Plant Cell 4: 1089–1100 (1992).Google Scholar
  248. 248.
    Szymkowiak EJ, Sussex IM: Effect of lateral suppressor on petal initiation in tomato. Plant J 4: 1–7 (1993).Google Scholar
  249. 249.
    Tacke E, Prüfer D, Schmitz J, Rohde W: The potato leafroll luteovirus 17K protein is a single-stranded nucleic acidbinding protein. J Gen Virol 72: 2035–2038 (1991).Google Scholar
  250. 250.
    Takizawa PA, Sil A, Swedlow JR, Herskowitz I, Vale RD: Actin-dependent localization of an RNA encoding a cell-fate determinant in yeast. Nature 389: 90–93 (1997).Google Scholar
  251. 251.
    Terry BR, Robards AW: Hydrodynamic radius alone governs the mobility of molecules through plasmodesmata. Planta 171: 145–157 (1987).Google Scholar
  252. 252.
    Theurkauf W, Alberts B, Jan YN, Jongens TA: A central role for microtubules in the differentiation of Drosophila oocytes. Development 118: 1169–1180 (1993).Google Scholar
  253. 253.
    Thomas CL, Maule AJ: Identification of the cauliflower mosaic virus movement protein RNA-binding domain. Virology 206: 1145–1149 (1995).Google Scholar
  254. 254.
    Thompson JR, García-Arenal F: The bundle sheath-phloem interface of Cucumis sativus is a boundary to systemic infection by tomato aspermy virus. Mol Plant-Microbe Interact 11: 109–114 (1998).Google Scholar
  255. 255.
    Tilney LG, Cooke TJ, Connelly PS, Tilney MS: The structure of plasmodesmata as revealed by plasmolysis, detergent extraction, and protease digestion. J Cell Biol 122: 739–747 (1991).Google Scholar
  256. 256.
    Tomenius K, Clapham D, Meshi T: Localization by immunogold cytochemistry of the virus-coded 30K protein in plasmodesmata of leaves infected with tobacco mosaic virus. Virology 160: 363–371 (1987).Google Scholar
  257. 257.
    Trass JA, Doonan JH, Rawlins DJ, Shaw PJ, Watts J, Lloyd CW: An actin network is present in the cytoplasm throughout the cell cycle of carrot cells and associates with the dividing nucleus. J Cell Biol 105: 387–395 (1987).Google Scholar
  258. 258.
    Tröbner W, Ramirez L, Motte P, Hue I, Huijser P, Lönnig W-K, Saedler H, Sommer H, Schwarz-Sommer Z: GLOBOSA: a homeotic gene which interacts with DEFICIENS in the control of Antirrinum floral organogenesis. EMBO J 11: 4693–4704 (1992).Google Scholar
  259. 259.
    Tucker EB: Translocation in the staminal hairs of Setcreasea purpurea. I. Study of cell ultrastructure and cell-to-cell passage of molecular probes. Protoplasma 113: 193–201 (1982).Google Scholar
  260. 260.
    Turner A, Wells B, Roberts K: Plasmodesmata of maize root tips: Structure and composition. J Cell Sci 107: 3351–3361 (1994).Google Scholar
  261. 261.
    van den Berg C, Willemsen V, Hage W, Weisbeek P, Scheres B: Cell fate in the Arabidopsis root meristem determined by directional signalling. Nature 378: 62–65 (1995).Google Scholar
  262. 262.
    van der Krol AR, Chua N-H: The basic domain of plant BZIP proteins facilitates import of a reporter protein into plant nuclei. Plant Cell 3: 667–675 (1991).Google Scholar
  263. 263.
    van Lent J, Wellink J, Goldbach R: Evidence for the involvement of the 58K and 48K proteins in the intercellular movement of cowpea mosaic virus. J Gen Virol 71: 219–223 (1990).Google Scholar
  264. 264.
    van Lent J, Storms M, van der Meer F, Wellink J, Goldbach R: Tubular structures involved in movement of cowpea mosaic virus are also formed in infected cowpea protoplasts. J Gen Virol 72: 2615–2623 (1991).Google Scholar
  265. 265.
    van Loon LC, Pierpoint WS, Boller Th, Conejero V: Recommendations for naming plant pathogenesis-related proteins. Plant Mol Biol Rep 12: 245–264 (1994).Google Scholar
  266. 266.
    Vaquero C, Turner AP, Demangeat G, Sanz A, Serra MT, Roberts K, García-Luque I: The 3a protein from cucumber mosaic virus increases the gating capacity of plasmodesmata in transgenic tobacco plants. J Gen Virol 75: 3193–3197 (1994).Google Scholar
  267. 267.
    Vaquero C, Liao Y-C, Nähring J, Fischer R: Mapping of the RNA-binding domain of the cucumber mosaic virus movement protein. J Gen Virol 78: 2095–2099 (1997).Google Scholar
  268. 268.
    Varagona MJ, Schmidt RJ, Raikhel NV: Nuclear localization signal(s) required for nuclear targeting of the maize regulatory protein Opaque-2. Plant Cell 4: 1213–1227 (1992).Google Scholar
  269. 269.
    Varogana MJ, Raikhel NV: The basic domain in the bZIP regulatory protein Opaque2 serves two independent functions: DNA binding and nuclear localization. Plant J 5: 207–214 (1994).Google Scholar
  270. 270.
    Volk GM, Turgeon R, Beebe DU: Secondary plasmodesmata formation in the minor-vein phloem of Cucumis melo L. and Cucurbita pepo L. Planta 199: 425–432 (1996).Google Scholar
  271. 271.
    Waigmann E, Lucas WJ, Citovsky V, Zambryski P: Direct functional assay for tobacco mosaic virus cell-to-cell movement protein and identification of a domain involved in increasing plasmodesmal permeability. Proc Natl Acad Sci USA 91: 1433–1437 (1994).Google Scholar
  272. 272.
    Waigmann E, Zambryski P: Tobacco mosaic virus movement protein-mediated protein transport between trichome cells. Plant Cell 7: 2069–2079 (1995).Google Scholar
  273. 273.
    Waigmann E, Turner A, Peart J, Roberts K, Zambryski P: Ultrastructural analysis of leaf trichome plasmodesmata reveals major differences from mesophyll plasmodesmata. Planta 203: 75–84 (1997).Google Scholar
  274. 274.
    Wang S, Hazelrigg T: Implications for bcd mRNA localization from spatial distribution of exu protein in Drosophila oogenesis. Nature 369: 400–403 (1994).Google Scholar
  275. 275.
    Ward BM, Medville R, Lazarowitz SG, Turgeon R: The geminivirus BL1 movement protein is associated with endoplasmic reticulum-derived tubules in developing phloem cells. J Virol 71: 3726–3733 (1997).Google Scholar
  276. 276.
    Ward JM, Kühn C, Tegeder M, Frommer WB: Sucrose transport in higher plants. Int Rev Cytol 178: 41–71 (1998).Google Scholar
  277. 277.
    Weigel D, Alvarez J, Smyth DR, Yanofsky MF, Meyerowitz EM: LEAFY controls floral meristem identity in Arabidopsis. Cell 69: 843–859 (1992).Google Scholar
  278. 278.
    Wellink J, van Kammen AB: Cell-to-cell transport of cowpea mosaic virus requires both the 58/48 K proteins and the capsid proteins. J Gen Virol 70: 2279–2286 (1989).Google Scholar
  279. 279.
    Wellink J, van Lent JWM, Verver J, Sijen T, Goldbach RW, van Kammen AB: The cowpea mosaic virus M RNAencoded 48–kiladalton protein is responsible for induction of tubular structures in protoplasts. J Virol 67: 3660–3664 (1993).Google Scholar
  280. 280.
    Whaley WG, Mollenhauer HH, Leech JH: The ultrastructure of the meristematic cells. Am J Bot 47: 401–449 (1960).Google Scholar
  281. 281.
    White RG, Badelt K, Overall RL, Vesk M: Actin associated with plasmodesmata. Protoplasma 180: 169–184 (1994).Google Scholar
  282. 282.
    Wieczorek A, Sanfaçon H: Characterization and subcellular localization of tomato ringspot nepovirus putative movement protein. Virology 194: 734–742 (1993).Google Scholar
  283. 283.
    Wilhelm JE, Vale RD: RNA on the move: the mRNA localization pathway. J Cell Biol 123: 269–274 (1993).Google Scholar
  284. 284.
    Williams W: The effect of selection on the manifold expression of the 'suppressed lateral’ gene in the tomato. Heredity 14: 285–296 (1960).Google Scholar
  285. 285.
    Wintermantel WM, Banerjee N, Oliver JC, Paolillo DJ, Zaitlin M: Cucumber mosaic virus is restricted from entering minor veins in transgenic tobacco exhibiting replicasemediated resistance. Virology 231: 248–257 (1997).Google Scholar
  286. 286.
    Wolf S, Deom CM, Beachy RN, Lucas WJ: Movement protein of tobacco mosaic virus modifies plasmodesmatal size exclusion limit. Science 246: 377–379 (1989).Google Scholar
  287. 287.
    Zhao L-j, Padamanabhan R: Nuclear transport of adenovirus DNA polymerase is facilitated by interaction with preterminal protein. Cell 55: 1005–1015 (1988).Google Scholar
  288. 288.
    Zheng H, Wang G, Zhang L: Alfalfa mosaic virus movement protein induces tubules in plant protoplasts. Mol Plant Microbe Inteact 10: 1010–1014 (1997).Google Scholar
  289. 289.
    Ziegler-Graff V, Guilford PJ, Baulcombe DC: Tobacco rattle virus RNA-1 29K gene product potentiates viral movement and also affects symptom induction in tobacco. Virology 182: 145–155 (1991).Google Scholar

Copyright information

© Kluwer Academic Publishers 1998

Authors and Affiliations

  • Biao Ding
    • 1
  1. 1.Department of BotanyOklahoma State UniversityStillwaterUSA (e-mail

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