Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Opinion
  • Published:

RNA as a long-distance information macromolecule in plants

Nature Reviews Molecular Cell Biology volume 2, pages 849–857 (2001)Cite this article

Abstract

A role for RNA as a non-cell-autonomous information macromolecule is emerging as a new model in biology. Studies on higher plants have shown the operation of cell-to-cell and long-distance communication networks that mediate the selective transport of RNA. The evolution and function of these systems are discussed in terms of an RNA-based signalling network that potentiates control over gene expression at the whole-plant level.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Model of protein/ribonucleoprotein transport through the microchannels of higher plant plasmodesmata.
Figure 2: The plant vascular network and the development of the phloem sieve-tube system.
Figure 3: Phloem-mediated long-distance delivery of a sequence-specific signal activates systemic silencing of the targeted transgene.
Figure 4: Potential mechanism for regulating the transport of non-cell-autonomous RNA into the phloem translocation stream.
Figure 5: Selective transport of non-cell-autonomous ribonucleoprotein complexes (RNPs) over long distances through the non-circulatory phloem translocation pathway.
Figure 6: Selective entry and exit of long-distance RNA-based signalling molecules.

Similar content being viewed by others

References

  1. Lehmann, R. Cell–cell signalling, microtubules, and the loss of symmetry in the Drosophila oocyte. Cell 83, 353–356 (1995).

    Article  CAS  PubMed  Google Scholar 

  2. Grünert, S. & St Johnston, D. RNA localization and the development of asymmetry during Drosophila oogenesis. Curr. Opin. Genet. Dev. 6, 395–402 (1996).

    Article  PubMed  Google Scholar 

  3. Schnapp, B. J., Arn, E. A., Deshler, J. O. & Highett, M. I. RNA localization in Xenopus oocytes. Semin. Cell Dev. Biol. 8, 529–540 (1997).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  5. Waterhouse, P., Wang, M.-B. & Lough, T. Gene silencing as an adaptive defence against viruses. Nature 411, 834–842 (2001).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Goudreau, P. N. & Stock, A. M. Signal transduction in bacteria: molecular mechanisms of stimulus-response coupling. Curr. Opin. Microbiol. 1, 160–169 (1998).

    Article  CAS  PubMed  Google Scholar 

  8. Stock, A. M., Robinson, V. L. & Goudreau, P. N. Two-component signal transduction. Annu. Rev. Biochem. 69, 183–215 (2000).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  10. Gurdon, J. B., Dyson, S. & St Johnson, D. Cells' perception of position in a concentration gradient. Cell 95, 159–162 (1998).

    Article  CAS  PubMed  Google Scholar 

  11. Clark, S. E. Cell signalling at the shoot meristem. Nature Reviews Mol. Cell Biol. 2, 276–284 (2001).

    Article  CAS  Google Scholar 

  12. Goodenough, D. A., Goliger, J. A. & Paul, D. L. Connexins, connexons, and intercellular communication. Annu. Rev. Biochem. 65, 475–502 (1996).

    Article  CAS  PubMed  Google Scholar 

  13. Lucas, W. J., Ding, B. & van der Schoot, C. Plasmodesmata and the supracellular nature of plants. New Phytol. 125, 435–476 (1993).

    Article  PubMed  Google Scholar 

  14. Lucas, W. J. Plasmodesmata: intercellular channels for macromolecular transport in plants. Curr. Opin. Cell Biol. 7, 673–680 (1995).

    Article  CAS  PubMed  Google Scholar 

  15. Robards, A. W. & Lucas, W. J. Plasmodesmata. Annu. Rev. Plant Physiol. Plant Mol. Biol. 41, 369–419 (1990).

    Article  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Fukuda, H. Tracheary element differentiation. Plant Cell 9, 1147–1156 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Schulz, A. Phloem: structure related to function. Prog. Bot. 59, 429–475 (1998).

    Article  Google Scholar 

  24. Sjölund, R. T. The phloem sieve element: a river runs through it. Plant Cell 9, 1137–1146 (1997).

    Article  PubMed  PubMed Central  Google Scholar 

  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).

    CAS  Google Scholar 

  26. Knoblauch, M., & van Bel, A. J. E. Sieve tubes in action. Plant Cell 10, 35–50 (1998).

    Article  CAS  PubMed Central  Google Scholar 

  27. Turgeon, R. Phloem loading and plasmodesmata. Trends Plant Sci. 1, 418–423 (1996).

    Article  Google Scholar 

  28. Ziegler, H. Encyclopedia of Plant Physiology Vol. 1 (eds Zimmermann, M. H. & Milburn, J. A.) 59–100 (Springer, Berlin, 1975).

    Google Scholar 

  29. Kollmann, R. & Kleinig, H. Protein filaments — structural components of the phloem exudate. Planta 95, 86–94 (1970).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  36. Jorgensen, R. A. Cosuppression, flower color patterns, and metastable gene expression states. Science 268, 686–691 (1995).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Palauqui, J. C., Elmayan, T., Pollien, 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, 4738–4745 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Voinnet, O. & Baulcombe, D. C. Systemic signalling in gene silencing. Nature 389, 553 (1997).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  41. Hull, R. The movement of viruses in plants. Annu. Rev. Phytopathol. 24, 213–240 (1989).

    Article  Google Scholar 

  42. Gilbertson, R. L. & Lucas, W. J. How do viruses traffic on the vascular highway? Trends Plant Sci. 1, 260–268 (1996).

    Article  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Ratcliff, F., Harrison, B. D. & Baulcombe, D. C. A similarity between viral defence and gene silencing in plants. Science 276, 1558–1560 (1997).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Brigneti, G. et al. Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana. EMBO J. 17, 6739–6746 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  53. Anandalakshmi, R. et al. A viral suppressor of gene silencing in plants. Proc. Natl Acad. Sci. USA 95, 13079–13084 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  58. Chaffey, N. Cambium: old challenges-new opportunities. Trees Struct. Funct. 13, 138–151 (1999).

    Article  Google Scholar 

  59. Jansen, R.-P. mRNA localization: messages on the move. Nature Rev Mol. Cell Biol. 2, 247–256 (2001).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  68. Golecki, B., Schulz, A. & Thompson, G. A. Translocation of structural P proteins in the phloem. Plant Cell 11, 127–140 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Kende, H. & Zeevaart, J. A. D. The five “classical” plant hormones. Plant Cell 9, 1197–1210 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Ryan, C. A. & Pearce, G. Polypeptide hormones. Plant Physiol. 125, 65–68 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  72. Jang, J. C. & Sheen, J. Sugar sensing in higher plants. Trends Plant Sci. 2, 208–214 (1997).

    Article  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  74. Meins, F. Jr. RNA degradation and models for post-transcriptional gene-silencing. Plant Mol. Biol. 43, 261–273 (2000).

    Article  CAS  PubMed  Google Scholar 

  75. Baulcombe, D. C. Gene silencing: RNA makes RNA makes no protein. Curr. Biol. 9, R599–R601 (1999).

    Article  CAS  PubMed  Google Scholar 

  76. Vaucheret, H. & Fagard, M. Transcriptional gene silencing in plants: targets, inducers and regulators. Trends Genet. 17, 29–35 (2001).

    Article  CAS  PubMed  Google Scholar 

  77. Fire, A. RNA-triggered gene silencing. Trends Genet. 15, 358–363 (1999).

    Article  CAS  PubMed  Google Scholar 

  78. Eddy, S. R. Noncoding RNA genes. Curr. Opin. Genet. Dev. 9, 695–699 (1999).

    Article  CAS  PubMed  Google Scholar 

  79. Pasquinelli, A. E. et al. Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature 408, 86–89 (2000).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  81. Reinhart, B. J. et al. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403, 901–906 (2000).

    Article  CAS  PubMed  Google Scholar 

  82. Rinne, P. L. H. & van der Schoot, C. Symplasmic fields in the tunica of the shoot apical meristem coordinate morphogenetic events. Development 125, 1477–1485 (1998).

    Article  CAS  PubMed  Google Scholar 

  83. van der Schoot, C. & Rinne, P. L. Networks for shoot design. Trends Plant Sci. 4, 31–37 (1999).

    Article  CAS  PubMed  Google Scholar 

  84. Lucas, W. J. et al. Selective trafficking of KNOTTED1 homeodomain protein and its mRNA through plasmodesmata. Science 270, 1980–1983 (1995).

    Article  CAS  PubMed  Google Scholar 

  85. Carpenter, R. & Coen, E. S. Transposon induced chimeras show that FLORICAULA, a meristem identity gene, acts non-autonomously between cell-layers. Development 121, 19–26 (1995).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  91. Zeevaart, J. A. D. Physiology of flowering. Science 137, 723–731 (1962).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  93. Aukerman, M. J. & Amasino, R. M. Floral induction and florigen. Cell 93, 491–494 (1998).

    Article  CAS  PubMed  Google Scholar 

  94. Mezitt, L. A. & Lucas, W. J. Plasmodesmal cell-to-cell transport of proteins and nucleic acids. Plant Mol. Biol. 32, 251–273 (1996).

    Article  CAS  PubMed  Google Scholar 

  95. Lake, J. A., Quick, W. P., Beerling, D. J. & Woodward, F. I. Signals from mature to new leaves. Nature 411, 154 (2001).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  99. Matzke, M., Matzke, A. & Kooter, J. M. RNA: guiding gene silencing. Science 293, 1080–1083 (2001).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We apologize to all of our colleagues whose work was not properly discussed due to space limitations. Work in our laboratory on plasmodesmata and the supracellular nature of plants was supported by grants from the National Science Foundation and the Department of Energy Office of Basic Energy Sciences.

Author information

Authors and Affiliations

  1. the Division of Biological Sciences, Section of Plant Biology, University of California, One Shields Ave., Davis, 95616, California

    William J. Lucas, Byung-Chun Yoo & Friedrich Kragler

Authors
  1. William J. Lucas
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Byung-Chun Yoo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Friedrich Kragler
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to William J. Lucas.

Related links

Related links

DATABASES

Swiss-Prot:

CmPP16-1

CmPP16-2

sucrose transporter 1

FURTHER INFORMATION

Encyclopaedia of Life Sciences:

Phloem structure and function

William J. Lucas' homepage

Glossary

ALLOPOLYPLOIDY

The fusion of two distinct parental species to form a hybrid, the genome of which is the sum of the two parental genomes.

ANGIOSPERMS

Any flowering vascular plant with seeds that are covered and protected by a carpel. Non-angiosperms include gymnosperms (for example, pine and cycads), ferns and mosses.

CAMBIUM

A meristem that gives rise to radial rows of cells.

COMPANION CELLS

These are specialized parenchymal cells that are associated with sieve-tube elements in angiosperm phloem. These cells arise from the same mother cell as the sieve-tube elements.

ENDOREDUPLICATION

Repeated rounds of DNA replication in the absence of intervening mitoses, which lead to polyploidy.

EPIGENETIC PROCESS

Any heritable influence (in the progeny of cells or of individuals) on gene activity, which is unaccompanied by a change in DNA sequence.

GAP JUNCTION

A communicating junction (permeant to molecules up to 1 kDa) between adjacent animal cells, which is composed of 12 connexin protein subunits, six of which form a connexon or hemichannel contributed by each of the coupled cells.

NON-CELL-AUTONOMOUS

A gene whose product (either RNA or protein) affects cells that are distant from the site of production.

RIBONUCLEOPROTEIN

A conjugated protein that contains RNA as the non-protein component.

SIEVE ELEMENTS

The cells of the phloem that are involved in the long-distance transport of nutrients.

TRACHEID

An elongated, thick-walled cell of xylem, which conducts and supports, and is found in most vascular plants. In contrast to vessel elements, tracheids have tapering ends and pitted walls without perforations.

VASCULAR MERISTEM

A cylindrical sheath of undifferentiated cells, which divide to produce secondary phloem and secondary xylem.

VEGETATIVE STATE

The state relating to, or involving propagation by, asexual processes.

VESSEL MEMBER

A constituent cell of a vessel.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lucas, W., Yoo, BC. & Kragler, F. RNA as a long-distance information macromolecule in plants. Nat Rev Mol Cell Biol 2, 849–857 (2001). https://doi.org/10.1038/35099096

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1038/35099096

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing