Skip to main content
The Plant Cell logoLink to The Plant Cell
. 1993 Dec;5(12):1783–1794. doi: 10.1105/tpc.5.12.1783

Cell-to-Cell Trafficking of Macromolecules through Plasmodesmata Potentiated by the Red Clover Necrotic Mosaic Virus Movement Protein.

T Fujiwara 1, D Giesman-Cookmeyer 1, B Ding 1, SA Lommel 1, WJ Lucas 1
PMCID: PMC160404  PMID: 12271056

Abstract

Direct evidence is presented for cell-to-cell trafficking of macromolecules via plasmodesmata in higher plants. The fluorescently labeled 35-kD movement protein of red clover necrotic mosaic virus (RCNMV) trafficked rapidly from cell to cell when microinjected into cowpea leaf mesophyll cells. Furthermore, this protein potentiated rapid cell-to-cell trafficking of RCNMV RNA, but not DNA. Electron microscopic studies demonstrated that the 35-kD movement protein does not unfold the RCNMV RNA molecules. Thus, if unfolding of RNA is necessary for cell-to-cell trafficking, it may well involve participation of endogenous cellular factors. These findings support the hypothesis that trafficking of macromolecules is a normal plasmodesmal function, which has been usurped by plant viruses for their cell-to-cell spread.

Full Text

The Full Text of this article is available as a PDF (3.0 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Akey C. W., Goldfarb D. S. Protein import through the nuclear pore complex is a multistep process. J Cell Biol. 1989 Sep;109(3):971–982. doi: 10.1083/jcb.109.3.971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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. 1990 Feb 23;60(4):637–647. doi: 10.1016/0092-8674(90)90667-4. [DOI] [PubMed] [Google Scholar]
  3. Citovsky V., Knorr D., Zambryski P. Gene I, a potential cell-to-cell movement locus of cauliflower mosaic virus, encodes an RNA-binding protein. Proc Natl Acad Sci U S A. 1991 Mar 15;88(6):2476–2480. doi: 10.1073/pnas.88.6.2476. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Citovsky V. Probing Plasmodesmal Transport with Plant Viruses. Plant Physiol. 1993 Aug;102(4):1071–1076. doi: 10.1104/pp.102.4.1071. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Citovsky V., Wong M. L., Shaw A. L., Prasad B. V., Zambryski P. Visualization and characterization of tobacco mosaic virus movement protein binding to single-stranded nucleic acids. Plant Cell. 1992 Apr;4(4):397–411. doi: 10.1105/tpc.4.4.397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Citovsky V., Zambryski P. How do plant virus nucleic acids move through intercellular connections? Bioessays. 1991 Aug;13(8):373–379. doi: 10.1002/bies.950130802. [DOI] [PubMed] [Google Scholar]
  7. Comai L., Dietrich R. A., Maslyar D. J., Baden C. S., Harada J. J. Coordinate expression of transcriptionally regulated isocitrate lyase and malate synthase genes in Brassica napus L. Plant Cell. 1989 Mar;1(3):293–300. doi: 10.1105/tpc.1.3.293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dalmay T., Rubino L., Burgyán J., Russo M. Replication and movement of a coat protein mutant of cymbidium ringspot tombusvirus. Mol Plant Microbe Interact. 1992 Sep-Oct;5(5):379–383. doi: 10.1094/mpmi-5-379. [DOI] [PubMed] [Google Scholar]
  9. Ding B., Haudenshield J. S., Hull R. J., Wolf S., Beachy R. N., Lucas W. J. Secondary plasmodesmata are specific sites of localization of the tobacco mosaic virus movement protein in transgenic tobacco plants. Plant Cell. 1992 Aug;4(8):915–928. doi: 10.1105/tpc.4.8.915. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Ding B., Haudenshield J. S., Willmitzer L., Lucas W. J. Correlation between arrested secondary plasmodesmal development and onset of accelerated leaf senescence in yeast acid invertase transgenic tobacco plants. Plant J. 1993 Jul;4(1):179–189. doi: 10.1046/j.1365-313x.1993.04010179.x. [DOI] [PubMed] [Google Scholar]
  11. Fisher D. B., Wu Y., Ku M. S. Turnover of soluble proteins in the wheat sieve tube. Plant Physiol. 1992 Nov;100(3):1433–1441. doi: 10.1104/pp.100.3.1433. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Giesman-Cookmeyer D., Lommel S. A. Alanine scanning mutagenesis of a plant virus movement protein identifies three functional domains. Plant Cell. 1993 Aug;5(8):973–982. doi: 10.1105/tpc.5.8.973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Lommel S. A., Weston-Fina M., Xiong Z., Lomonossoff G. P. The nucleotide sequence and gene organization of red clover necrotic mosaic virus RNA-2. Nucleic Acids Res. 1988 Sep 12;16(17):8587–8602. doi: 10.1093/nar/16.17.8587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Lůcas W. J., Wolf S. Plasmodesmata: the intercellular organelles of green plants. Trends Cell Biol. 1993 Sep;3(9):308–315. doi: 10.1016/0962-8924(93)90013-q. [DOI] [PubMed] [Google Scholar]
  15. Osman T. A., Hayes R. J., Buck K. W. Cooperative binding of the red clover necrotic mosaic virus movement protein to single-stranded nucleic acids. J Gen Virol. 1992 Feb;73(Pt 2):223–227. doi: 10.1099/0022-1317-73-2-223. [DOI] [PubMed] [Google Scholar]
  16. Petty I. T., Jackson A. O. Mutational analysis of barley stripe mosaic virus RNA beta. Virology. 1990 Dec;179(2):712–718. doi: 10.1016/0042-6822(90)90138-h. [DOI] [PubMed] [Google Scholar]
  17. Silver P. A. How proteins enter the nucleus. Cell. 1991 Feb 8;64(3):489–497. doi: 10.1016/0092-8674(91)90233-o. [DOI] [PubMed] [Google Scholar]
  18. Wolf S., Deom C. M., Beachy R. N., Lucas W. J. Movement protein of tobacco mosaic virus modifies plasmodesmatal size exclusion limit. Science. 1989 Oct 20;246(4928):377–379. doi: 10.1126/science.246.4928.377. [DOI] [PubMed] [Google Scholar]
  19. Xiong Z. G., Lommel S. A. Red clover necrotic mosaic virus infectious transcripts synthesized in vitro. Virology. 1991 May;182(1):388–392. doi: 10.1016/0042-6822(91)90687-7. [DOI] [PubMed] [Google Scholar]
  20. Ziegler-Graff V., Guilford P. J., Baulcombe D. C. Tobacco rattle virus RNA-1 29K gene product potentiates viral movement and also affects symptom induction in tobacco. Virology. 1991 May;182(1):145–155. doi: 10.1016/0042-6822(91)90658-x. [DOI] [PubMed] [Google Scholar]

Articles from The Plant Cell are provided here courtesy of Oxford University Press

RESOURCES