Natural isolates of with the ability to move from cell to cell independently of coat protein Free

Abstract

(BMV) requires encapsidation-competent coat protein (CP) for cell-to-cell movement and the 3a movement protein (MP) is involved in determining the CP requirement for BMV movement. However, these conclusions have been drawn by using BMV strain M1 (BMV-M1) and a related strain. Here, the ability of the MPs of five other natural BMV strains to mediate the movement of BMV-M1 in the absence of CP was tested. The MP of BMV M2 strain (BMV-M2) efficiently mediated the movement of CP-deficient BMV-M1 and the MPs of two other strains functioned similarly to some extent. Furthermore, BMV-M2 itself moved between cells independently of CP, demonstrating that BMV-M1 and -M2 use different movement modes. Reassortment between CP-deficient BMV-M1 and -M2 showed the involvement of RNA3 in determining the CP requirement for cell-to-cell movement and the involvement of RNAs 1 and 2 in movement efficiency and symptom induction in the absence of CP. Spontaneous BMV MP mutants generated that exhibited CP-independent movement were also isolated and analysed. Comparison of the nucleotide differences of the MP genes of BMV-M1, the natural strains and mutants capable of CP-independent movement, together with further mutational analysis of BMV-M1 MP, revealed that single amino acid differences at the C terminus of MP are sufficient to alter the requirement for CP in the movement of BMV-M1. Based on these findings, a possible virus strategy in which a movement mode is selected in plant viruses to optimize viral infectivity in plants is discussed.

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2005-04-01
2024-03-29
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References

  1. Ahlquist P. 1999; Bromoviruses ( Bromoviridae ). In Encyclopedia of Virology . , 2nd edn. vol 1 pp  198–204 Edited by Granoff A., Webster R. G. San Diego, CA: Academic Press;
  2. Ahlquist P., French R., Janda M., Loesch-Fries L. S. 1984; Multicomponent RNA plant virus infection derived from cloned viral cDNA. Proc Natl Acad Sci U S A 81:7066–7070 [CrossRef]
    [Google Scholar]
  3. Andreev I. A., Kim S. H., Kalinina N. O., Rakitina D. V., Fitzgerald A. G., Palukaitis P., Taliansky M. E. 2004; Molecular interactions between a plant virus movement protein and RNA: force spectroscopy investigation. J Mol Biol 339:1041–1047 [CrossRef]
    [Google Scholar]
  4. Blackman L. M., Boevink P., Santa Cruz S., Palukaitis P., Oparka K. J. 1998; The movement protein of Cucumber mosaic virus traffics into sieve elements in minor veins of Nicotiana clevelandii . Plant Cell 10:525–537 [CrossRef]
    [Google Scholar]
  5. Callaway A., Giesman-Cookmeyer D., Gillock E. T., Sit T. L., Lommel S. A. 2001; The multifunctional capsid proteins of plant RNA viruses. Annu Rev Phytopathol 39:419–460 [CrossRef]
    [Google Scholar]
  6. Canto T., Prior D. A. M., Hellwald K.-H., Oparka K. J., Palukaitis P. 1997; Characterization of cucumber mosaic virus. IV. Movement protein and coat protein are both essential for cell-to-cell movement of cucumber mosaic virus. Virology 237:237–248 [CrossRef]
    [Google Scholar]
  7. Carrington J. C., Kasschau K. D., Mahajan S. K., Schaad M. C. 1996; Cell-to-cell and long-distance transport of viruses in plants. Plant Cell 8:1669–1681 [CrossRef]
    [Google Scholar]
  8. Carvalho C. M., Wellink J., Ribeiro S. G., Goldbach R. W., van Lent J. W. M. 2003; The C-terminal region of the movement protein of Cowpea mosaic virus is involved in binding to the large but not to the small coat protein. J Gen Virol 84:2271–2277 [CrossRef]
    [Google Scholar]
  9. Citovsky V., Knorr D., Schuster G., Zambryski P. 1990; The P30 movement protein of tobacco mosaic virus is a single-stranded nucleic acid binding protein. Cell 60:637–647 [CrossRef]
    [Google Scholar]
  10. De Jong W., Ahlquist P. 1995; Host-specific alterations in viral RNA accumulation and infection spread in a brome mosaic virus isolate with an expanded host range. J Virol 69:1485–1492
    [Google Scholar]
  11. De Jong W., Chu A., Ahlquist P. 1995; Coding changes in the 3a cell-to-cell movement gene can extend the host range of brome mosaic virus systemic infection. Virology 214:464–474 [CrossRef]
    [Google Scholar]
  12. Dreher T. W., Rao A. L. N., Hall T. C. 1989; Replication in vivo of mutant brome mosaic virus RNAs defective in aminoacylation. J Mol Biol 206:425–438 [CrossRef]
    [Google Scholar]
  13. Fujisaki K., Hagihara H., Kaido M., Mise K., Okuno T. 2003; Complete nucleotide sequence of spring beauty latent virus, a bromovirus infectious to Arabidopsis thaliana . Arch Virol 148:165–175 [CrossRef]
    [Google Scholar]
  14. Fujita Y., Mise K., Okuno T., Ahlquist P., Furusawa I. 1996; A single codon change in a conserved motif of a bromovirus movement protein gene confers compatibility with a new host. Virology 223:283–291 [CrossRef]
    [Google Scholar]
  15. Fujita M., Mise K., Furusawa I. 1999; Expression and characterization of the 3a movement protein of cowpea chlorotic mottle bromovirus. Arch Virol 144:2449–2456 [CrossRef]
    [Google Scholar]
  16. Janda M., French R., Ahlquist P. 1987; High efficiency T7 polymerase synthesis of infectious RNA from cloned brome mosaic virus cDNA and effects of 5′ extensions on transcript infectivity. Virology 158:259–262 [CrossRef]
    [Google Scholar]
  17. Kaplan I. B., Zhang L., Palukaitis P. 1998; Characterization of cucumber mosaic virus. V. Cell-to-cell movement requires capsid protein but not virions. Virology 246:221–231 [CrossRef]
    [Google Scholar]
  18. Kasteel D. T. J., van der Wel N. N., Jansen K. A. J., Goldbach R. W., van Lent J. W. M. 1997; Tubule-forming capacity of the movement proteins of alfalfa mosaic virus and brome mosaic virus. J Gen Virol 78:2089–2093
    [Google Scholar]
  19. Kim S. H., Kalinina N. O., Andreev I., Ryabov E. V., Fitzgerald A. G., Taliansky M. E., Palukaitis P. 2004; The C-terminal 33 amino acids of the cucumber mosaic virus 3a protein affect virus movement, RNA binding and inhibition of infection and translation. J Gen Virol 85:221–230 [CrossRef]
    [Google Scholar]
  20. Kroner P., Ahlquist P. 1992; RNA-based viruses. In Molecular Plant Pathology: a Practical Approach vol 1 pp  23–34 Edited by Gurr S. J., McPherson M. J., Bowles D. J. Oxford: Oxford University Press;
    [Google Scholar]
  21. Kroner P., Richards D., Traynor P., Ahlquist P. 1989; Defined mutations in a small region of the brome mosaic virus 2a gene cause diverse temperature-sensitive RNA replication phenotypes. J Virol 63:5302–5309
    [Google Scholar]
  22. Kroner P. A., Young B. M., Ahlquist P. 1990; Analysis of the role of brome mosaic virus 1a protein domains in RNA replication, using linker insertion mutagenesis. J Virol 64:6110–6120
    [Google Scholar]
  23. Lane L. C. 1974; The bromoviruses. Adv Virus Res 19:151–220
    [Google Scholar]
  24. Lane L. C. 1981; Bromoviruses. In Handbook of Plant Virus Infections: Comparative Diagnosis pp  333–376 Edited by Kurstak E. Amsterdam: Elsevier;
    [Google Scholar]
  25. Lazarowitz S. G., Beachy R. N. 1999; Viral movement proteins as probes for intracellular and intercellular trafficking in plants. Plant Cell 11:535–548 [CrossRef]
    [Google Scholar]
  26. Mise K., Allison R. F., Janda M., Ahlquist P. 1993; Bromovirus movement protein genes play a crucial role in host specificity. J Virol 67:2815–2823
    [Google Scholar]
  27. Mise K., Mori M., Nakayashiki H., Koyama T., Okuno T., Furusawa I. 1994; Nucleotide sequence of a set of cDNA clones derived from the brome mosaic virus ATCC66 strain and comparison with the Russian strain genome. Ann Phytopath Soc Jpn 60:454–462 [CrossRef]
    [Google Scholar]
  28. Mori M., Zhang G.-H., Kaido M., Okuno T., Furusawa I. 1993; Efficient production of human gamma interferon in tobacco protoplasts by genetically engineered brome mosaic virus RNAs. J Gen Virol 74:1255–1260 [CrossRef]
    [Google Scholar]
  29. Nagano H., Mise K., Okuno T., Furusawa I. 1999; The cognate coat protein is required for cell-to-cell movement of a chimeric brome mosaic virus mediated by the cucumber mosaic virus movement protein. Virology 265:226–234 [CrossRef]
    [Google Scholar]
  30. Nagano H., Mise K., Furusawa I., Okuno T. 2001; Conversion in the requirement of coat protein in cell-to-cell movement mediated by the cucumber mosaic virus movement protein. J Virol 75:8045–8053 [CrossRef]
    [Google Scholar]
  31. Okinaka Y., Mise K., Suzuki E., Okuno T., Furusawa I. 2001; The C terminus of brome mosaic virus coat protein controls viral cell-to-cell and long-distance movement. J Virol 75:5385–5390 [CrossRef]
    [Google Scholar]
  32. Osman T. A. M., Hayes R. J., Buck K. W. 1992; Cooperative binding of the red clover necrotic mosaic virus movement protein to single-stranded nucleic acids. J Gen Virol 73:223–227 [CrossRef]
    [Google Scholar]
  33. Osman F., Schmitz I., Rao A. L. N. 1999; Effect of C-terminal deletions in the movement protein of cowpea chlorotic mottle virus on cell-to-cell and long-distance movement. J Gen Virol 80:1357–1365
    [Google Scholar]
  34. Rao A. L. N. 1997; Molecular studies on bromovirus capsid protein. III. Analysis of cell-to-cell movement competence of coat protein defective variants of cowpea chlorotic mottle virus. Virology 232:385–395 [CrossRef]
    [Google Scholar]
  35. Rao A. L. N., Grantham G. L. 1995; Biological significance of the seven amino-terminal basic residues of brome mosaic virus coat protein. Virology 211:42–52 [CrossRef]
    [Google Scholar]
  36. Rao A. L. N., Grantham G. L. 1996; Molecular studies on bromovirus capsid protein. II. Functional analysis of the amino-terminal arginine-rich motif and its role in encapsidation, movement, and pathology. Virology 226:294–305 [CrossRef]
    [Google Scholar]
  37. Sánchez-Navarro J. A., Bol J. F. 2001; Role of the Alfalfa mosaic virus movement protein and coat protein in virus transport. Mol Plant Microbe Interact 14:1051–1062 [CrossRef]
    [Google Scholar]
  38. Sasaki N., Fujita Y., Mise K., Furusawa I. 2001; Site-specific single amino acid changes to Lys or Arg in the central region of the movement protein of a hybrid bromovirus are required for adaptation to a nonhost. Virology 279:47–57 [CrossRef]
    [Google Scholar]
  39. Sasaki N., Arimoto M., Nagano H., Mori M., Kaido M., Mise K., Okuno T. 2003; The movement protein gene is involved in the virus-specific requirement of the coat protein in cell-to-cell movement of bromoviruses. Arch Virol 148:803–812 [CrossRef]
    [Google Scholar]
  40. Sasaki N., Kaido M., Okuno T., Mise K. 2005; Coat protein-independent cell-to-cell movement of bromoviruses expressing brome mosaic virus movement protein with an adaptation-related amino acid change in the central region. Arch Virol (in press
    [Google Scholar]
  41. Schmitz I., Rao A. L. N. 1996; Molecular studies on bromovirus capsid protein. I. Characterization of cell-to-cell movement-defective RNA3 variants of brome mosaic virus. Virology 226:281–293 [CrossRef]
    [Google Scholar]
  42. Schmitz I., Rao A. L. N. 1998; Deletions in the conserved amino-terminal basic arm of cucumber mosaic virus coat protein disrupt virion assembly but do not abolish infectivity and cell-to-cell movement. Virology 248:323–331 [CrossRef]
    [Google Scholar]
  43. Suzuki M., Kuwata S., Kataoka J., Masuta C., Nitta N., Takanami Y. 1991; Functional analysis of deletion mutants of cucumber mosaic virus RNA3 using an in vitro transcription system. Virology 183:106–113 [CrossRef]
    [Google Scholar]
  44. Takamatsu K., Ishikawa M., Meshi T., Okada Y. 1987; Expression of bacterial chloramphenicol acetyltransferase gene in tobacco plants mediated by TMV-RNA. EMBO J 6:307–311
    [Google Scholar]
  45. Takeda A., Kaido M., Okuno T., Mise K. 2004; The C terminus of the movement protein of Brome mosaic virus controls the requirement for coat protein in cell-to-cell movement and plays a role in long-distance movement. J Gen Virol 85:1751–1761 [CrossRef]
    [Google Scholar]
  46. Valverde R. A. 1987; Systemic infection of cowpea by two isolates of brome mosaic virus. Plant Dis 71:557
    [Google Scholar]
  47. van Lent J., Wellink J., Goldbach R. 1990; Evidence for the involvement of the 58K and 48K proteins in the intercellular movement of cowpea mosaic virus. J Gen Virol 71:219–223 [CrossRef]
    [Google Scholar]
  48. Wieczorek A., Sanfaçon H. 1993; Characterization and subcellular localization of tomato ringspot nepovirus putative movement protein. Virology 194:734–743 [CrossRef]
    [Google Scholar]
  49. Xiong Z., Kim K. H., Giesman-Cookmeyer D., Lommel S. A. 1993; The roles of the red clover necrotic mosaic virus capsid and cell-to-cell movement proteins in systemic infection. Virology 192:27–32 [CrossRef]
    [Google Scholar]
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