Skip to main content
The Plant Cell logoLink to The Plant Cell
. 1995 Dec;7(12):2069–2079. doi: 10.1105/tpc.7.12.2069

Tobacco mosaic virus movement protein-mediated protein transport between trichome cells.

E Waigmann 1, P Zambryski 1
PMCID: PMC161062  PMID: 8718620

Abstract

Tobacco mosaic virus movement protein (TMV MP) is required to mediate viral spread between plant cells via plasmodesmata. Plasmodesmata are cytoplasmic bridges that connect individual plant cells and ordinarily limit molecular diffusion to small molecules and metabolites with a molecular mass up to 1 kD. Here, we characterize functional properties of Nicotiana clevelandii trichome plasmodesmata and analyze their interaction with TMV MP. Trichomes constitute a linear cellular system and provide a predictable pathway of movement. Their plasmodesmata are functionally distinct from plasmodesmata in other plant cel types; they allow cell-to-cell diffusion of dextrans with a molecular mass up to 7 kD, and TMV MP does not increase this size exclusion limit for dextrans. In contrast, the 30-kD TMV MP itself moves between trichome cells and specifically mediates the translocation of a 90-kD beta-glucuronidase (GUS) reporter protein as a GUS::TMV MP fusion. Neither GUS by itself nor GUS in the presence of TMV MP moves between cells. These data imply that a plasmodesmal transport signal resides within TMV MP and is essential for movement. This signal confers selectivity to the translocated protein and cannot function in trans to support movement of other molecules.

Full Text

The Full Text of this article is available as a PDF (2.7 MB).

Selected References

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

  1. Angell S. M., Baulcombe D. C. Cell-to-cell movement of potato virus X revealed by micro-injection of a viral vector tagged with the beta-glucuronidase gene. Plant J. 1995 Jan;7(1):135–140. doi: 10.1046/j.1365-313x.1995.07010135.x. [DOI] [PubMed] [Google Scholar]
  2. Bostwick D. E., Dannenhoffer J. M., Skaggs M. I., Lister R. M., Larkins B. A., Thompson G. A. Pumpkin phloem lectin genes are specifically expressed in companion cells. Plant Cell. 1992 Dec;4(12):1539–1548. doi: 10.1105/tpc.4.12.1539. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. 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]
  4. 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]
  5. Citovsky V., McLean B. G., Zupan J. R., Zambryski P. Phosphorylation of tobacco mosaic virus cell-to-cell movement protein by a developmentally regulated plant cell wall-associated protein kinase. Genes Dev. 1993 May;7(5):904–910. doi: 10.1101/gad.7.5.904. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. 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]
  8. Deom C. M., Oliver M. J., Beachy R. N. The 30-kilodalton gene product of tobacco mosaic virus potentiates virus movement. Science. 1987 Jul 24;237(4813):389–394. doi: 10.1126/science.237.4813.389. [DOI] [PubMed] [Google Scholar]
  9. Derrick P. M., Barker H., Oparka K. J. Increase in Plasmodesmatal Permeability during Cell-to-Cell Spread of Tobacco Rattle Virus from Individually Inoculated Cells. Plant Cell. 1992 Nov;4(11):1405–1412. doi: 10.1105/tpc.4.11.1405. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  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. 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. 1993 Dec;5(12):1783–1794. doi: 10.1105/tpc.5.12.1783. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Grabski S., De Feijter A. W., Schindler M. Endoplasmic Reticulum Forms a Dynamic Continuum for Lipid Diffusion between Contiguous Soybean Root Cells. Plant Cell. 1993 Jan;5(1):25–38. doi: 10.1105/tpc.5.1.25. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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. 1987 Sep;6(9):2557–2563. doi: 10.1002/j.1460-2075.1987.tb02544.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Mushegian A. R., Koonin E. V. Cell-to-cell movement of plant viruses. Insights from amino acid sequence comparisons of movement proteins and from analogies with cellular transport systems. Arch Virol. 1993;133(3-4):239–257. doi: 10.1007/BF01313766. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Noueiry A. O., Lucas W. J., Gilbertson R. L. Two proteins of a plant DNA virus coordinate nuclear and plasmodesmal transport. Cell. 1994 Mar 11;76(5):925–932. doi: 10.1016/0092-8674(94)90366-2. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. Pascal E., Sanderfoot A. A., Ward B. M., Medville R., Turgeon R., Lazarowitz S. G. The geminivirus BR1 movement protein binds single-stranded DNA and localizes to the cell nucleus. Plant Cell. 1994 Jul;6(7):995–1006. doi: 10.1105/tpc.6.7.995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Restrepo M. A., Freed D. D., Carrington J. C. Nuclear transport of plant potyviral proteins. Plant Cell. 1990 Oct;2(10):987–998. doi: 10.1105/tpc.2.10.987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Rouleau M., Smith R. J., Bancroft J. B., Mackie G. A. Purification, properties, and subcellular localization of foxtail mosaic potexvirus 26-kDa protein. Virology. 1994 Oct;204(1):254–265. doi: 10.1006/viro.1994.1530. [DOI] [PubMed] [Google Scholar]
  21. Smith L. G., 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. 1992 Sep;116(1):21–30. doi: 10.1242/dev.116.1.21. [DOI] [PubMed] [Google Scholar]
  22. Tautz D., Pfeifle C. A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma. 1989 Aug;98(2):81–85. doi: 10.1007/BF00291041. [DOI] [PubMed] [Google Scholar]
  23. Vaquero C., Turner A. P., Demangeat G., Sanz A., Serra M. T., 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. 1994 Nov;75(Pt 11):3193–3197. doi: 10.1099/0022-1317-75-11-3193. [DOI] [PubMed] [Google Scholar]
  24. 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 U S A. 1994 Feb 15;91(4):1433–1437. doi: 10.1073/pnas.91.4.1433. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Waigmann E., Zambryski P. Plasmodesmata. Gateways for rapid information transfer. Curr Biol. 1994 Aug 1;4(8):713–716. doi: 10.1016/s0960-9822(00)00157-3. [DOI] [PubMed] [Google Scholar]
  26. Wieczorek A., Sanfaçon H. Characterization and subcellular localization of tomato ringspot nepovirus putative movement protein. Virology. 1993 Jun;194(2):734–742. doi: 10.1006/viro.1993.1314. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. 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