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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1996 Oct 1;93(20):11155–11160. doi: 10.1073/pnas.93.20.11155

Invasion of minor veins of tobacco leaves inoculated with tobacco mosaic virus mutants defective in phloem-dependent movement.

X Ding 1, M H Shintaku 1, S A Carter 1, R S Nelson 1
PMCID: PMC38300  PMID: 8855325

Abstract

To fully understand vascular transport of plant viruses, the viral and host proteins, their structures and functions, and the specific vascular cells in which these factors function must be determined. We report here on the ability of various cDNA-derived coat protein (CP) mutants of tobacco mosaic virus (TMV) to invade vascular cells in minor veins of Nicotiana tabacum L. cv. Xanthi nn. The mutant viruses we studied, TMV CP-O, U1mCP15-17, and SNC015, respectively, encode a CP from a different tobamovirus (i.e., from odontoglossum ringspot virus) resulting in the formation of non-native capsids, a mutant CP that accumulates in aggregates but does not encapsidate the viral RNA, or no CP. TMV CP-O is impaired in phloem-dependent movement, whereas U1mCP15-17 and SNC015 do not accumulate by phloem-dependent movement. In developmentally-defined studies using immunocytochemical analyses we determined that all of these mutants invaded vascular parenchyma cells within minor veins in inoculated leaves. In addition, we determined that the CPs of TMV CP-O and U1mCP15-17 were present in companion (C) cells of minor veins in inoculated leaves, although more rarely than CP of wild-type virus. These results indicate that the movement of TMV into minor veins does not require the CP, and an encapsidation-competent CP is not required for, but may increase the efficiency of, movement into the conducting complex of the phloem (i.e., the C cell/sieve element complex). Also, a host factor(s) functions at or beyond the C cell/sieve element interface with other cells to allow efficient phloem-dependent accumulation of TMV CP-O.

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Selected References

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  1. Allison R., Thompson C., Ahlquist P. Regeneration of a functional RNA virus genome by recombination between deletion mutants and requirement for cowpea chlorotic mottle virus 3a and coat genes for systemic infection. Proc Natl Acad Sci U S A. 1990 Mar;87(5):1820–1824. doi: 10.1073/pnas.87.5.1820. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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]
  3. Cronin S., Verchot J., Haldeman-Cahill R., Schaad M. C., Carrington J. C. Long-distance movement factor: a transport function of the potyvirus helper component proteinase. Plant Cell. 1995 May;7(5):549–559. doi: 10.1105/tpc.7.5.549. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Culver J. N., Dawson W. O., Plonk K., Stubbs G. Site-directed mutagenesis confirms the involvement of carboxylate groups in the disassembly of tobacco mosaic virus. Virology. 1995 Jan 10;206(1):724–730. doi: 10.1016/s0042-6822(95)80096-4. [DOI] [PubMed] [Google Scholar]
  5. Culver J. N., Dawson W. O. Tobacco mosaic virus coat protein: an elicitor of the hypersensitive reaction but not required for the development of mosaic symptoms in Nicotiana sylvestris. Virology. 1989 Dec;173(2):755–758. doi: 10.1016/0042-6822(89)90592-8. [DOI] [PubMed] [Google Scholar]
  6. Das P., Hari V. Intracellular distribution of the 126K/183K and capsid proteins in cells infected by some tobamoviruses. J Gen Virol. 1992 Nov;73(Pt 11):3039–3043. doi: 10.1099/0022-1317-73-11-3039. [DOI] [PubMed] [Google Scholar]
  7. Deom C. M., Lapidot M., Beachy R. N. Plant virus movement proteins. Cell. 1992 Apr 17;69(2):221–224. doi: 10.1016/0092-8674(92)90403-y. [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. 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 X. S., Carter S. A., Nelson R. S. Enhanced cytochemical detection of viral proteins and RNAs using double-sided labeling and light microscopy. Biotechniques. 1996 Jan;20(1):111–115. doi: 10.2144/96201st06. [DOI] [PubMed] [Google Scholar]
  11. Dolja V. V., Haldeman-Cahill R., Montgomery A. E., Vandenbosch K. A., Carrington J. C. Capsid protein determinants involved in cell-to-cell and long distance movement of tobacco etch potyvirus. Virology. 1995 Feb 1;206(2):1007–1016. doi: 10.1006/viro.1995.1023. [DOI] [PubMed] [Google Scholar]
  12. Dolja V. V., Haldeman R., Robertson N. L., Dougherty W. G., Carrington J. C. Distinct functions of capsid protein in assembly and movement of tobacco etch potyvirus in plants. EMBO J. 1994 Mar 15;13(6):1482–1491. doi: 10.1002/j.1460-2075.1994.tb06403.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gal-On A., Kaplan I., Roossinck M. J., Palukaitis P. The kinetics of infection of zucchini squash by cucumber mosaic virus indicate a function for RNA 1 in virus movement. Virology. 1994 Nov 15;205(1):280–289. doi: 10.1006/viro.1994.1644. [DOI] [PubMed] [Google Scholar]
  14. Hilf M. E., Dawson W. O. The tobamovirus capsid protein functions as a host-specific determinant of long-distance movement. Virology. 1993 Mar;193(1):106–114. doi: 10.1006/viro.1993.1107. [DOI] [PubMed] [Google Scholar]
  15. Hills G. J., Plaskitt K. A., Young N. D., Dunigan D. D., Watts J. W., Wilson T. M., Zaitlin M. Immunogold localization of the intracellular sites of structural and nonstructural tobacco mosaic virus proteins. Virology. 1987 Dec;161(2):488–496. doi: 10.1016/0042-6822(87)90143-7. [DOI] [PubMed] [Google Scholar]
  16. Holt C. A., Beachy R. N. In vivo complementation of infectious transcripts from mutant tobacco mosaic virus cDNAs in transgenic plants. Virology. 1991 Mar;181(1):109–117. doi: 10.1016/0042-6822(91)90475-q. [DOI] [PubMed] [Google Scholar]
  17. Holt C. A., Hodgson R. A., Coker F. A., Beachy R. N., Nelson R. S. Characterization of the masked strain of tobacco mosaic virus: identification of the region responsible for symptom attenuation by analysis of an infectious cDNA clone. Mol Plant Microbe Interact. 1990 Nov-Dec;3(6):417–423. doi: 10.1094/mpmi-3-417. [DOI] [PubMed] [Google Scholar]
  18. Ishikawa M., Meshi T., Motoyoshi F., Takamatsu N., Okada Y. In vitro mutagenesis of the putative replicase genes of tobacco mosaic virus. Nucleic Acids Res. 1986 Nov 11;14(21):8291–8305. doi: 10.1093/nar/14.21.8291. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Leisner S. M., Turgeon R. Movement of virus and photoassimilate in the phloem: a comparative analysis. Bioessays. 1993 Nov;15(11):741–748. doi: 10.1002/bies.950151107. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. 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]
  22. Mise K., Ahlquist P. Host-specificity restriction by bromovirus cell-to-cell movement protein occurs after initial cell-to-cell spread of infection in nonhost plants. Virology. 1995 Jan 10;206(1):276–286. doi: 10.1016/s0042-6822(95)80043-3. [DOI] [PubMed] [Google Scholar]
  23. Nathanson S. D., Nelson L. T., Lee M. A spontaneous subcutaneous tumor in C57BL/6 mice that metastasizes to the liver. Clin Exp Metastasis. 1993 Jan;11(1):45–54. doi: 10.1007/BF00880065. [DOI] [PubMed] [Google Scholar]
  24. Pacha R. F., Allison R. F., Ahlquist P. cis-acting sequences required for in vivo amplification of genomic RNA3 are organized differently in related bromoviruses. Virology. 1990 Feb;174(2):436–443. doi: 10.1016/0042-6822(90)90097-b. [DOI] [PubMed] [Google Scholar]
  25. Qiu S. G., Schoelz J. E. Three regions of cauliflower mosaic virus strain W260 are involved in systemic infection of solanaceous hosts. Virology. 1992 Oct;190(2):773–782. doi: 10.1016/0042-6822(92)90915-c. [DOI] [PubMed] [Google Scholar]
  26. Quillet L., Guilley H., Jonard G., Richards K. In vitro synthesis of biologically active beet necrotic yellow vein virus RNA. Virology. 1989 Sep;172(1):293–301. doi: 10.1016/0042-6822(89)90131-1. [DOI] [PubMed] [Google Scholar]
  27. SIEGEL A., ZAITLIN M., SEHGAL O. P. The isolation of defective tobacco mosaic virus strains. Proc Natl Acad Sci U S A. 1962 Oct 15;48:1845–1851. doi: 10.1073/pnas.48.10.1845. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Saito T., Yamanaka K., Okada Y. Long-distance movement and viral assembly of tobacco mosaic virus mutants. Virology. 1990 Jun;176(2):329–336. doi: 10.1016/0042-6822(90)90002-9. [DOI] [PubMed] [Google Scholar]
  29. Shintaku M. H., Carter S. A., Bao Y., Nelson R. S. Mapping nucleotides in the 126-kDa protein gene that control the differential symptoms induced by two strains of tobacco mosaic virus. Virology. 1996 Jul 1;221(1):218–225. doi: 10.1006/viro.1996.0368. [DOI] [PubMed] [Google Scholar]
  30. Takamatsu N., Ishikawa M., Meshi T., Okada Y. Expression of bacterial chloramphenicol acetyltransferase gene in tobacco plants mediated by TMV-RNA. EMBO J. 1987 Feb;6(2):307–311. doi: 10.1002/j.1460-2075.1987.tb04755.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Taliansky M. E., García-Arenal F. Role of cucumovirus capsid protein in long-distance movement within the infected plant. J Virol. 1995 Feb;69(2):916–922. doi: 10.1128/jvi.69.2.916-922.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Vaewhongs A. A., Lommel S. A. Virion formation is required for the long-distance movement of red clover necrotic mosaic virus in movement protein transgenic plants. Virology. 1995 Oct 1;212(2):607–613. doi: 10.1006/viro.1995.1518. [DOI] [PubMed] [Google Scholar]
  33. Weiland J. J., Edwards M. C. Evidence that the alpha a gene of barley stripe mosaic virus encodes determinants of pathogenicity to oat (Avena sativa). Virology. 1994 May 15;201(1):116–126. doi: 10.1006/viro.1994.1271. [DOI] [PubMed] [Google Scholar]
  34. Wijdeveld M. M., Goldbach R. W., Verduin B. J., van Loon L. C. Association of viral 126 kDa protein-containing X-bodies with nuclei in mosaic-diseased tobacco leaves. Arch Virol. 1989;104(3-4):225–239. doi: 10.1007/BF01315545. [DOI] [PubMed] [Google Scholar]
  35. 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]
  36. de Zoeten G. A., Gaard G. Mechanisms underlying systemic invasion of pea plants by pea enation mosaic virus. Intervirology. 1983;19(2):85–94. doi: 10.1159/000149342. [DOI] [PubMed] [Google Scholar]

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