RNA as a long-distance information macromolecule in plants

Nature Reviews Molecular Cell Biology

Volumn 2, Issue 11, 2001, Pages 849-857

  Lucas, William J ^a   Yoo, Byung Chun ^a   Kragler, Friedrich ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EMBRYOPHYTA;

RNA;

BIOLOGICAL MODEL; GENE; METABOLISM; PHYSIOLOGY; PLANT; PLANT PHYSIOLOGY; REVIEW; TRANSPORT AT THE CELLULAR LEVEL;

BIOLOGICAL TRANSPORT; GENES, PLANT; MODELS, BIOLOGICAL; PLANT PHYSIOLOGY; PLANTS; RNA; SUPPORT, U.S. GOV'T, NON-P.H.S.;

EID: 0035513830     PISSN: 14710072     EISSN: None     Source Type: Journal    
DOI: 10.1038/35099096     Document Type: Article

References (100)

1. Lehmann, R. Cell-cell signalling, microtubules, and the loss of symmetry in the Drosophila oocyte. Cell 83, 353-356 (1995).
2. Grünert, S. & St Johnston, D. RNA localization and the development of asymmetry during Drosophila oogenesis. Curr. Opin. Genet. Dev. 6, 395-402 (1996).
3. Schnapp, B. J., Am, E. A., Deshler, J. O. & Highett, M. I. RNA localization in Xenopus oocytes. Semin. Cell Dev. Biol. 8, 529-540 (1997).
4. Jorgensen, R. A., Atkinson, R. G., Forster, R. L. S. & Lucas, W. J. An RNA-based information superhighway in plants. Science 279, 1486-1487 (1998).
5. Waterhouse, P., Wang, M.-B. & Lough, T. Gene silencing as an adaptive defence against viruses. Nature 411, 834-842 (2001).
6. Falke, J. J., Bass, R. B., Butler, S. L., Chervitz, S. A. & Danielson, M. A. The two-component signalling pathway of bacterial chemotaxis: a molecular view of signal transduction by receptors, kinases, and adaptation enzymes. Annu. Rev. Cell Dev. Biol. 13, 457-512 (1997).
7. Goudreau, P. N. & Stock, A. M. Signal transduction in bacteria: molecular mechanisms of stimulus-response coupling. Curr. Opin. Microbiol. 1, 160-169 (1998).
8. Stock, A. M., Robinson, V. L. & Goudreau, P. N. Two-component signal transduction. Annu. Rev. Biochem. 69, 183-215 (2000).
9. Artavanis-Tsakonas, S., Rand, M. D. & Lake, R. J. Notch signalling: cell fate control and signal integration in development. Science 284, 770-776 (1999).
10. Gurdon, J. B., Dyson, S. & St Johnson, D. Cells' perception of position in a concentration gradient. Cell 95, 159-162 (1998).
11. Clark, S. E. Cell signalling at the shoot meristem. Nature Reviews Mol. Cell Biol. 2, 276-284 (2001).
12. Goodenough, D. A., Goliger, J. A. & Paul, D. L. Connexins, connexons, and intercellular communication. Annu. Rev. Biochem. 65, 475-502 (1996).
13. Lucas, W. J., Ding, B. & van der School, C. Plasmodesmata and the supracellular nature of plants. New Phytol. 125, 435-476 (1993).
14. Lucas, W. J. Plasmodesmata: intercellular channels for macromolecular transport in plants. Curr. Opin. Cell Biol. 7, 673-680 (1995).
15. Robards, A. W. & Lucas, W. J. Plasmodesmata. Annu. Rev. Plant Physiol. Plant Mol. Biol. 41, 369-419 (1990).
16. Lee, J.-Y., Yoo, B.-C. & Lucas, W. J. Parallels between nuclear-pore and plasmodesmal trafficking of information molecules. Planta 210, 177-187 (2000).
17. Jackson, D. & Hake, S. Morphogenesis on the move: cell-to-cell trafficking of plant regulatory proteins. Curr. Opin. Genet. Dev. 7, 495-500 (1997).
18. Zambryski, P. & Crawford, K. Plasmodesmata: gatekeepers for cell-to-cell transport of developmental signals in plants. Annu. Rev. Cell Dev. Biol. 16, 393-421 (2000).
19. Fujiwara, T., Giesman-Cookmeyer, D., Ding, B., Lommel, S. A. & Lucas, W. J. Cell-to-cell trafficking of macromolecules through plasmodesmata potentiated by the red clover necrotic mosaic virus movement protein. Plant Cell 5, 1783-1794 (1993).
20. Noueiry, A. O., Lucas, W. J. & Gilbertson, R. L. Two proteins of a plant DNA virus coordinate nuclear and plasmodesmal transport. Cell 76, 925-932 (1994).
21. Waigmann, E., Lucas, W. J., 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).
22. Fukuda, H. Tracheary element differentiation. Plant Cell 9, 1147-1156 (1997).
23. Schulz, A. Phloem: structure related to function. Prog. Bot. 59, 429-475 (1998).
24. Sjölund, R. T. The phloem sieve element: a river runs through it. Plant Cell 9, 1137-1146 (1997).
25. van Bel, A. J. E. & Knoblauch, M. Sieve element and companion cell: the story of the comatose patient and the hyperactive nurse. Aust. J. Plant Physiol. 27, 477-487 (2000).
26. Knoblauch, M., & van Bel, A. J. E. Sieve tubes in action. Plant Cell 10, 35-50 (1998).
27. Turgeon, R. Phloem loading and plasmodesmata. Trends Plant Sci. 1, 418-423 (1995).
28. Ziegler, H. Encyclopedia of Plant Physiology Vol. 1 (eds Zimmermann, M. H. & Milbum, J. A.) 59-100 (Springer, Berlin, 1975).
29. Kollmann, R. & Kleinig, H. Protein filaments - structural components of the phloem exudate. Planta 95, 86-94 (1970).
30. Kühn, C., Franceschi, V. R., Schulz, A., Lemoine, R. & Frommer, W. B. Macromolecular trafficking indicated by localization and turnover of sucrose transporters in enucleate sieve elements. Science 275, 1298-1300 (1997).
31. Ruiz-Medrano, R., Xoconostle-Cazares, B. & Lucas, W. J. Phloem long-distance transport of CmNACP mRNA: implications for supracellular regulation in plants. Development 126, 4405-4419 (1999).
32. Sasaki, T. Chino, M., Hayashi, H. & Fujiwara, T. Detection of several mRNA species in rice phloem sap. Plant Cell Physiol. 39, 895-897 (1998).
33. Xoconostle-Cazares, B. et al. Plant paralog to viral movement protein that potentiates transport of mRNA into the phloem. Science 283, 94-98 (1999).
34. Kim, M., Canio, W., Kessler, S. & Sinha, N. Developmental changes due to long-distance movement of a homeobox fusion transcript in tomato. Science 293, 287-289 (2001).
35. Ruiz-Medrano, R., Xoconostle-Cazares, B. & Lucas, W. J. The phloem as a conduit for inter-organ communication. Curr. Opin. Plant Biol. 4, 202-209 (2001).
36. Jorgensen, R. A. Cosuppression, flower color patterns, and metastable gene expression states. Science 268, 686-691 (1995).
37. Palauqui, J. C., et al. Frequencies, timing, and spatial patterns of co-suppression of nitrate reductase and nitrite reductase in transgenic tobacco plants. Plant Physiol. 112, 1447-1456 (1996).
38. Palauqui, J. C., Elmayan, T., Pollen, J. M. & Vaucheret, H. Systemic acquired silencing: transgene-specific post-transcriptional silencing is transmitted by grafting from silenced stocks to non-silenced scions. EMBO J. 16, 4733-4745 (1997).
39. Voinnet, O. & Baulcombe, D. C. Systemic signalling in gene silencing. Nature 389, 553 (1997).
40. Voinnet, O., Vain, P., Angell, S. & Baulcombe, D. C. Systemic spread of sequence-specific transgene RNA degradation in plants is initiated by localized introduction of ectopic promoterless DNA. Cell 95, 177-187 (1998).
41. Hull, R. The movement of viruses in plants. Annu. Rev. Phytopathol. 24, 213-240 (1989).
42. Gilbertson, R. L. & Lucas, W. J. How do viruses traffic on the vascular highway? Trends Plant Sci. 1, 260-268 (1996).
43. Carrington, J. C.. Kasschau, K. D., Mahajan, S. K. & Schaad, M. C. Cell-to-cell and long-distance transport of viruses in plants. Plant Cell 8, 1669-1681 (1996).
44. Dolja, V. V., McBride, H. J. & Carrington, J. C. Tagging of plant potyvirus replication and movement by insertion of β-glucuronidase into the viral polyprotein. Proc. Natl Acad. Sci. USA 89, 10208-10212 (1992).
45. Oparka, K. J., Boevink, P. & Santa Cruz, S. Studying the movement of plant viruses using green fluorescent protein. Trends Plant Sci. 1, 412-418 (1996).
46. Roberts, A. G. et al. Phloem unloading in sink leaves of Nicotiana benthamiana: comparison of a fluorescent solute with a fluorescent virus. Plant Cell 9, 1381-1396 (1997).
47. Wang, H. L., Sudarshana, M. R., Gilbertson, R. L. & Lucas, W. J. Analysis of cell-to-cell and long-distance movement of a bean dwarf mosaic geminivirus-green fluorescent protein reporter in host and non-host species: identification of sites of resistance. Mol. Plant Microbe Interact. 12, 345-355 (1999).
48. Lindbo, J. A., Silva-Rosales, L., Proebsting, W. M. & Dougherty, W. G. Induction of a highly specific antiviral state in transgenic plants: implications for regulation of gene expression and virus resistance. Plant Cell 5, 1749-1759 (1993).
49. Ratcliff, R. Harrison, B. D. & Baulcombe, D. C. A similarity between viral defence and gene silencing in plants. Science 276, 1558-1560 (1997).
50. Jones, A. L. Thomas, C. L. & Maule, A. J. De novo methylation and co-suppression induced by a cytoplasmically replicating plant RNA virus. EMBO J. 17, 6385-6393 (1998).
51. Brigneti, G. et al. Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana. EMBO J. 17, 6739-6746 (1998).
52. Beclin, C., Berthome, R., Palauqui, J. C., Tepfer, M. & Vaucheret, H. Infection of tobacco or Arabidopsis plants by CMV counteracts systemic post-transcriptional silencing of non-viral (trans)genes. Virology 252, 313-317 (1998).
53. Anandalakshmi, R. et al. A viral suppressor of gene silencing in plants. Proc. Natl Acad. Sci. USA 95, 13079-13084 (1998).
54. Voinnet, O., Lederer, C. & Baulcombe, D. C. A viral movement protein prevents spread of the gene silencing signal in Nicotiana benthamiana. Cell 103, 157-167 (2000).
55. Lucy, A. P., Guo, H.-S., Li, W.-X. & Ding, S.-W. Suppression of post-transcriptional gene silencing by a plant viral protein localized in the nucleus. EMBO J. 19, 1672-1680 (2000).
56. Mallory, A. C. et al. HC-Pro suppression of transgene silencing eliminates the small RNAs but not transgene methylation or the mobile signal. Plant Cell 13, 571-583 (2001).
57. Lachaud, S., Catesson, A. M. & Bonnemain, J. L. Structure and functions of the vascular cambium. C. R. Acad. Sci. III 322, 633-650 (1999).
58. Chaffey, N. Cambium: old challenges-new opportunities. Trees Struct. Funct. 13, 138-151 (1999).
59. Jansen, R.-P. mRNA localization: messages on the move. Nature Rev Mol. Cell Biol. 2, 247-256 (2001).
60. Bassell, G. J., Oleynikov, Y. & Singer, R. H. The travels of mRNAs through all cells large and small. FASEB J. 13, 447-454 (1999).
61. Schnorrer, F., Bohmann, K. & Nusslein-Volhard, C. The molecular motor dynein is involved in targeting Swallow and bicoid RNA to the anterior pole of Drosophila oocytes. Nature Cell Biol. 2, 185-190 (2000).
62. Heinlein, M., Epel, B. L., Padgett, H. S. & Beachy, R. N. Interaction of tobamovirus movement proteins with the plant cytoskeleton. Science 270, 1983-1985 (1995).
63. McLean, B. G., Zupan, J. & Zambryski, P. C. Tobacco mosaic virus movement protein associates with the cytoskeleton in tobacco cells. Plant Cell 7, 2101-2114 (1995).
64. Boyko, V. Ferralli, J., Ashby, J., Schellenbaum, P. & Heinlein, M. Function of microtubules in intercellular transport of plant virus RNA. Nature Cell Biol. 2, 826-832 (2000).
65. Oparka, K. J. & Santa Cruz, S. The great escape: phloem transport and unloading of macromolecules. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51, 323-347 (2000).
66. Fisher, D. B., Wu, Y. & Ku, M. S. B. Turnover of soluble proteins in the wheat sieve tube. Plant Physiol. 100, 1433-1441 (1992).
67. Golecki, B., Schulz, A., Carstens-Behrens, U. & Kollmann, R. Evidence for graft transmission of structural phloem proteins or their precursors in heterografts of Cucurbitaceae. Planta 206, 630-640 (1998).
68. Golecki, B., Schulz, A. & Thompson, G. A. Translocation of structural P proteins in the phloem. Plant Cell 11, 127-140 (1999).
69. Kende, H. & Zeevaart, J. A. D. The five "classical" plant hormones. Plant Cell 9, 1197-1210 (1997).
70. Ryan, C. A. & Pearce, G. Polypeptide hormones. Plant Physiol. 125, 65-68 (2001).
71. Coruzzi, G. M. & Zhou, L. Carbon and nitrogen sensing and signalling in plants: emerging 'matrix effects'. Curr. Opin. Plant Biol. 4, 247-253 (2001).
72. Jang, J. C. & Sheen, J. Sugar sensing in higher plants. Trends Plant Sci. 2, 208-214 (1997).
73. Matzke, M. A., Matzke, A. J., Pruss, G. J. & Vance, V. B. RNA-based silencing strategies in plants. Curr. Opin. Genet. Dev. 11, 221-227 (2001).
74. Meins, F. Jr. RNA degradation and models for post-transcriptional gene-silencing. Plant Mol. Biol. 43, 261-273 (2000).
75. Baulcombe, D. C. Gene silencing: RNA makes RNA makes no protein. Curr. Biol. 9, R599-R601 (1999).
76. Vaucheret, H. & Fagard, M. Transcriptional gene silencing in plants: targets, inducers and regulators. Trends Genet. 17, 29-35 (2001).
77. Fire, A. RNA-triggered gene silencing. Trends Genet. 15, 358-363 (1999).
78. Eddy, S. R. Noncoding RNA genes. Curr. Opin. Genet. Dev. 9, 695-699 (1999).
79. Pasquinelli, A. E. et al. Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature 408, 86-89 (2000).
80. Slack, F. J. et al. The lin-41 RBCC gene acts in the C. elegans heterochronic pathway between the let-7 regulatory RNA and the LIN-29 transcription factor. Mol. Cell 5, 659-669 (2000).
81. Reinhart, B. J. et al. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403, 901-906 (2000).
82. Rinne, P. L. H. & van der School, C. Symplasmic fields in the tunica of the shoot apical meristem coordinate morphogenetic events. Development 125, 1477-1485 (1998).
83. van der School, C. & Rinne, P. L. Networks for shoot design. Trends Plant Sci. 4, 31-37 (1999).
84. Lucas, W. J. et al. Selective trafficking of KNOTTED1 homeodomain protein and its mRNA through plasmodesmata. Science 270, 1980-1983 (1995).
85. Carpenter, R. & Coen, E. S. Transposon induced chimeras show that FLOPICAULA, a meristem identity gene, acts non-autonomously between cell-layers. Development 121, 19-26 (1995).
86. Hantke, S. S., Carpenter, R. & Coen, E. S. Expression of FLORICAULA in single-cell layers of periclinal chimeras activates downstream homeotic genes in all layers of floral meristems. Development 121, 27-35 (1995).
87. Perbal, M. C., Haughn, G., Saedler, H. & Schwarz-Sommer, Z. Non-cell-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).
88. Kragler, F., Monzer, J., Xoconostle-Cazares, B. & Lucas, W. J. Peptide antagonists of the plasmodesmal macromolecular trafficking pathway. EMBO J. 19, 2856-2868 (2000).
89. Kragler, F., Monzer, J., Shash, K., Xoconostle-Cazares, B. & Lucas, W. J. Cell-to-cell transport of proteins: requirement for unfolding and characterization of binding to a putative plasmodesmal receptor. Plant J. 15, 367-381 (1998).
90. Sessions, A., Yanofsky, M. F. & Weigel, D. Cell-cell signalling and movement by the floral transcription factors LEAFY and APETALA1. Science 289, 779-781 (2000).
91. Zeevaart, J. A. D. Physiology of flowering. Science 137, 723-731 (1962).
92. Colasanti, J. & Sundaresan, V. 'Florigen' enters the molecular age: long-distance signals that cause plants to flower. Trends Biochem. Sci. 25, 236-240 (2000).
93. Aukerman, M. J. & Amasino, R. M. Floral induction and florigen. Cell 93, 491-494 (1998).
94. Mezitt, L. A. & Lucas, W. J. Plasmodesmal cell-to-cell transport of proteins and nucleic acids. Plant Mol. Biol. 32, 251-273 (1996).
95. Lake, J. A., Quick, W. P., Beerling, D. J. & Woodward, F. I. Signals from mature to new leaves. Nature 411, 154 (2001).
96. Mette, M. F., Aufsatz, W., van der Winden, J., Matzke, M. A. & Matzke A. J. M. Transcriptional silencing and promoter methylation triggered by double-stranded RNA. EMBO. J. 19, 5194-5201 (2000).
97. Jones, L., Ratcliff, F. & Baulcombe, D. C. RNA-directed transcriptional gene silencing in plants can be inherited independently of the RNA trigger and requires Met1 for maintenance. Curr. Biol. 11, 747-757 (2001).
98. Amedeo, P., Habu, Y., Afsar, K., Mittelsten Scheid, O. & Paszkowski, J. Disruption of the plant gene MOM releases transcriptional silencing of methylated genes. Nature 405, 203-206 (2000).
99. Matzke, M., Matzke, A. & Kooter, J. M. RNA: guiding gene silencing. Science 293, 1080-1083 (2001).
100. Wolf, S., Deom, C. M., Beachy, R. N. & Lucas, W. J. Movement protein of tobacco mosaic virus modifies plasmodesmatal size exclusion limit. Science 246, 377-379 (1989).