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. 1995 Feb;69(2):916–922. doi: 10.1128/jvi.69.2.916-922.1995

Role of cucumovirus capsid protein in long-distance movement within the infected plant.

M E Taliansky 1, F García-Arenal 1
PMCID: PMC188660  PMID: 7815560

Abstract

Direct evidence is presented for a host-specific role of the cucumovirus capsid protein in long-distance movement within infected plants. Cucumber (Cucumis sativus L.) is a systemic host for cucumber mosaic cucumovirus (CMV). Tomato aspermy cucumovirus, strain 1 (1-TAV), multiplied to the levels of CMV (i.e., replicated, moved from cell to cell, and formed infectious particles) in the inoculated leaves of cucumbers but was completely unable to spread systemically. The defective long-distance systemic movement of 1-TAV was complemented by CMV in mixed infections. Coinfection of cucumbers with 1-TAV RNA with various combinations of transcripts from full-length cDNA clones of CMV genomic RNA 1, RNA2, and RNA3 showed that CMV RNA3 alone complemented 1-TAV long-distance movement. We obtained mutants containing mutations in the two open reading frames in CMV RNA3 encoding the 3a protein and the capsid protein (CP), both of which are necessary for cell-to-cell movement of CMV. Complementation experiments with mutant CMV RNA3 showed that only 3a protein mutants, i.e., those with an intact CP, complemented the long-distance movement of 1-TAV in cucumbers. Since CMV and TAV have common systemic host plants, the results presented here are strong evidence for an active, host-specific function of the CPs of these two cucumoviruses for long-distance spread in the phloem. The results also suggest that the plasmodesmata in the vascular system and/or at the boundary between the mesophyll and the vascular system, involved in long-distance movement through the phloem, and those in the mesophyll, involved in cell-to-cell movement, differ functionally.

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Selected References

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  1. Atabekov J. G., Taliansky M. E. Expression of a plant virus-coded transport function by different viral genomes. Adv Virus Res. 1990;38:201–248. doi: 10.1016/s0065-3527(08)60863-5. [DOI] [PubMed] [Google Scholar]
  2. Atkins D., Hull R., Wells B., Roberts K., Moore P., Beachy R. N. The tobacco mosaic virus 30K movement protein in transgenic tobacco plants is localized to plasmodesmata. J Gen Virol. 1991 Jan;72(Pt 1):209–211. doi: 10.1099/0022-1317-72-1-209. [DOI] [PubMed] [Google Scholar]
  3. Bernal J. J., Moriones E., García-Arenal F. Evolutionary relationships in the cucumoviruses: nucleotide sequence of tomato aspermy virus RNA 1. J Gen Virol. 1991 Sep;72(Pt 9):2191–2195. doi: 10.1099/0022-1317-72-9-2191. [DOI] [PubMed] [Google Scholar]
  4. Boccard F., Baulcombe D. C. Infectious in vitro transcripts from amplified cDNAs of the Y and Kin strains of cucumber mosaic virus. Gene. 1992 May 15;114(2):223–227. doi: 10.1016/0378-1119(92)90578-d. [DOI] [PubMed] [Google Scholar]
  5. Boccard F., Baulcombe D. Mutational analysis of cis-acting sequences and gene function in RNA3 of cucumber mosaic virus. Virology. 1993 Apr;193(2):563–578. doi: 10.1006/viro.1993.1165. [DOI] [PubMed] [Google Scholar]
  6. Chapman S., Hills G., Watts J., Baulcombe D. Mutational analysis of the coat protein gene of potato virus X: effects on virion morphology and viral pathogenicity. Virology. 1992 Nov;191(1):223–230. doi: 10.1016/0042-6822(92)90183-p. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. 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]
  9. 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]
  10. 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]
  11. 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]
  12. 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]
  13. Deom C. M., Schubert K. R., Wolf S., Holt C. A., Lucas W. J., Beachy R. N. Molecular characterization and biological function of the movement protein of tobacco mosaic virus in transgenic plants. Proc Natl Acad Sci U S A. 1990 May;87(9):3284–3288. doi: 10.1073/pnas.87.9.3284. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. 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]
  16. Habili N., Francki R. I. Comparative studies on tomato aspermy and cucumber mosaic viruses. I. Physical and chemical properties. Virology. 1974 Feb;57(2):392–401. doi: 10.1016/0042-6822(74)90179-2. [DOI] [PubMed] [Google Scholar]
  17. Hacker D. L., Petty I. T., Wei N., Morris T. J. Turnip crinkle virus genes required for RNA replication and virus movement. Virology. 1992 Jan;186(1):1–8. doi: 10.1016/0042-6822(92)90055-t. [DOI] [PubMed] [Google Scholar]
  18. Heaton L. A., Lee T. C., Wei N., Morris T. J. Point mutations in the turnip crinkle virus capsid protein affect the symptoms expressed by Nicotiana benthamiana. Virology. 1991 Jul;183(1):143–150. doi: 10.1016/0042-6822(91)90127-w. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. Lot H., Marchoux G., Marrou J., Kaper J. M., West C. K., van Vloten-Doting L., Hull R. Evidence for three functional RNA species in several strains of cucumber mosaic virus. J Gen Virol. 1974 Jan;22(1):81–93. doi: 10.1099/0022-1317-22-1-81. [DOI] [PubMed] [Google Scholar]
  21. Moriones E., Diaz I., Rodriguez-Cerezo E., Fraile A., Garcia-Arenal F. Differential interactions among strains of tomato aspermy virus and satellite RNAs of cucumber mosaic virus. Virology. 1992 Feb;186(2):475–480. doi: 10.1016/0042-6822(92)90012-e. [DOI] [PubMed] [Google Scholar]
  22. Moriones E., Roossinck M. J., García-Arenal F. Nucleotide sequence of tomato aspermy virus RNA 2. J Gen Virol. 1991 Apr;72(Pt 4):779–783. doi: 10.1099/0022-1317-72-4-779. [DOI] [PubMed] [Google Scholar]
  23. Murphy G., Kavanagh T. Speeding-up the sequencing of double-stranded DNA. Nucleic Acids Res. 1988 Jun 10;16(11):5198–5198. doi: 10.1093/nar/16.11.5198. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. O'Reilly D., Thomas C. J., Coutts R. H. Tomato aspermy virus has an evolutionary relationship with other tripartite RNA plant viruses. J Gen Virol. 1991 Jan;72(Pt 1):1–7. doi: 10.1099/0022-1317-72-1-1. [DOI] [PubMed] [Google Scholar]
  26. Palukaitis P., Roossinck M. J., Dietzgen R. G., Francki R. I. Cucumber mosaic virus. Adv Virus Res. 1992;41:281–348. doi: 10.1016/s0065-3527(08)60039-1. [DOI] [PubMed] [Google Scholar]
  27. Petty I. T., Edwards M. C., Jackson A. O. Systemic movement of an RNA plant virus determined by a point substitution in a 5' leader sequence. Proc Natl Acad Sci U S A. 1990 Nov;87(22):8894–8897. doi: 10.1073/pnas.87.22.8894. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. 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]
  29. 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]
  30. Rizzo T. M., Palukaitis P. Nucleotide sequence and evolutionary relationships of cucumber mosaic virus (CMV) strains: CMV RNA 1. J Gen Virol. 1989 Jan;70(Pt 1):1–11. doi: 10.1099/0022-1317-70-1-1. [DOI] [PubMed] [Google Scholar]
  31. Rizzo T. M., Palukaitis P. Nucleotide sequence and evolutionary relationships of cucumber mosaic virus (CMV) strains: CMV RNA 2. J Gen Virol. 1988 Aug;69(Pt 8):1777–1787. doi: 10.1099/0022-1317-69-8-1777. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. Salánki K., Balázs E., Burgyán J. Nucleotide sequence and infectious in vitro transcripts of RNA 3 of tomato aspermy virus pepper isolate. Virus Res. 1994 Sep;33(3):281–289. doi: 10.1016/0168-1702(94)90109-0. [DOI] [PubMed] [Google Scholar]
  34. Salánki K., Thole V., Balázs E., Burgyán J. Complete nucleotide sequence of the RNA 3 from subgroup II of cucumber mosaic virus (CMV) strain: Trk7. Virus Res. 1994 Mar;31(3):379–384. doi: 10.1016/0168-1702(94)90030-2. [DOI] [PubMed] [Google Scholar]
  35. Suzuki M., Kuwata S., Kataoka J., Masuta C., Nitta N., Takanami Y. Functional analysis of deletion mutants of cucumber mosaic virus RNA3 using an in vitro transcription system. Virology. 1991 Jul;183(1):106–113. doi: 10.1016/0042-6822(91)90123-s. [DOI] [PubMed] [Google Scholar]
  36. Traynor P., Young B. M., Ahlquist P. Deletion analysis of brome mosaic virus 2a protein: effects on RNA replication and systemic spread. J Virol. 1991 Jun;65(6):2807–2815. doi: 10.1128/jvi.65.6.2807-2815.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. 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]
  38. 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]
  39. Xiong Z., Kim K. H., Giesman-Cookmeyer D., Lommel S. A. The roles of the red clover necrotic mosaic virus capsid and cell-to-cell movement proteins in systemic infection. Virology. 1993 Jan;192(1):27–32. doi: 10.1006/viro.1993.1004. [DOI] [PubMed] [Google Scholar]
  40. Young M. J., Kelly L., Larkin P. J., Waterhouse P. M., Gerlach W. L. Infectious in vitro transcripts from a cloned cDNA of barley yellow dwarf virus. Virology. 1991 Jan;180(1):372–379. doi: 10.1016/0042-6822(91)90042-a. [DOI] [PubMed] [Google Scholar]
  41. van Lent J., Storms M., van der Meer F., Wellink J., Goldbach R. Tubular structures involved in movement of cowpea mosaic virus are also formed in infected cowpea protoplasts. J Gen Virol. 1991 Nov;72(Pt 11):2615–2623. doi: 10.1099/0022-1317-72-11-2615. [DOI] [PubMed] [Google Scholar]

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