1887

Journal of General Virology header logo

Volume 86, Issue 4

2a polymerase and 3a movement proteins independently affect both virus movement and the timing of symptom development in zucchini squash Free

Abstract

The basis for differences in the timing of systemic symptom elicitation in zucchini squash between a pepper strain of (Pf-CMV) and a cucurbit strain (Fny-CMV) was analysed. The difference in timing of appearance of systemic symptoms was shown to map to both RNA 2 and RNA 3 of Pf-CMV, with pseudorecombinant viruses containing either RNA 2 or RNA 3 from Pf-CMV showing an intermediate rate of systemic symptom development compared with those containing both or neither Pf-CMV RNAs. Symptom phenotype was shown to map to two single-nucleotide changes, both in codons for Ile at aa 267 and 168 (in Fny-CMV RNAs 2 and 3, respectively) to Thr (in Pf-CMV RNAs 2 and 3). The differential rate of symptom development was shown to be due to differences in the rates of cell-to-cell movement in the inoculated cotyledons, as well as differences in the rate of egress of the virus from the inoculated leaves. These data indicate that both the CMV 3a movement protein and the CMV 2a polymerase protein affect the rate of movement of CMV in zucchini squash and that these two proteins function independently of each other in their interactions with the host, facilitating virus movement.

  • Received:
  • Accepted:
  • Published Online:
SGM
Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.80744-0
2005-04-01
2024-04-16
Loading full text...

Full text loading...

/deliver/fulltext/jgv/86/4/vir861213.html?itemId=/content/journal/jgv/10.1099/vir.0.80744-0&mimeType=html&fmt=ahah

References

  1. Canto T., Palukaitis P. 1998; Transgenically expressed cucumber mosaic virus RNA 1 simultaneously complements replication of cucumber mosaic viruses RNA 2 and 3 and confers resistance to systemic infection. Virology 250:325–336 [CrossRef]
     [Google Scholar]
  2. Canto T., Palukaitis P. 1999a; The hypersensitive response to cucumber mosaic virus in Chenopodium amaranticolor requires virus movement outside the initially infected cell. Virology 265:74–82 [CrossRef]
     [Google Scholar]
  3. Canto T., Palukaitis P. 1999b; Are tubules generated by the 3a protein necessary for cucumber mosaic virus movement?. Mol Plant Microbe Interact 12:985–993 [CrossRef]
     [Google Scholar]
  4. Canto T., Choi S. K., Palukaitis P. 2001; A subpopulation of RNA 1 Cucumber mosaic virus contains 3′ termini originating from RNAs 2 or 3. J Gen Virol 82:941–945
     [Google Scholar]
  5. Chen J., Watanabe Y., Sako N., Ohshima K., Okada Y. 1996; Mapping of host range restriction of the Rakkyo strain of tobacco mosaic virus in Nicotiana tabacum cv. bright yellow. Virology 226:198–204 [CrossRef]
     [Google Scholar]
  6. Choi S. K., Choi J. K., Park W. M., Ryu K. H. 1999; RT-PCR detection and identification of three species of cucumoviruses with a single pair of primers. J Virol Methods 83:67–73 [CrossRef]
     [Google Scholar]
  7. Choi S. K., Yoon J. Y., Ryu K. H., Choi J. K., Palukaitis P., Park W. M. 2002; Systemic movement of a movement-deficient strain of Cucumber mosaic virus in zucchini squash is facilitated by a cucurbit-infecting potyvirus. J Gen Virol 83:3173–3178
     [Google Scholar]
  8. De Jong W., Chou 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]
  9. Deom C. M., Quan S., He X. Z. 1997; Replicase proteins as determinants of phloem-dependent long-distance movement of tobamoviruses in tobacco. Protoplasma 199:1–8 [CrossRef]
     [Google Scholar]
  10. Edwards M. C., Gonsalves D., Provvidenti R. 1983; Genetic analysis of cucumber mosaic virus in relation to host resistance: location of determinants for pathogenicity to certain legumes and Lactuca saligna . Phytopathology 73:269–273 [CrossRef]
     [Google Scholar]
  11. 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]
  12. Gal-On A., Kaplan I. B., Roossinck M. J., Palukaitis P. 1994; The kinetics of infection of zucchini squash by cucumber mosaic virus indicate a function for RNA 1 in virus movement. Virology 205:280–289 [CrossRef]
     [Google Scholar]
  13. Gal-On A., Kaplan I. B., Palukaitis P. 1996; Characterization of cucumber mosaic virus. II. Identification of movement protein sequences that influence its accumulation and systemic infection in tobacco. Virology 226:354–361 [CrossRef]
     [Google Scholar]
  14. Hayes R. J., Buck K. W. 1990; Complete replication of a eukaryotic virus RNA in vitro by a purified RNA-dependent RNA polymerase. Cell 63:363–368 [CrossRef]
     [Google Scholar]
  15. Higuchi R., Krummel B., Saiki R. K. 1988; A general method of in vitro preparation and specific mutagenesis of DNA fragments: study of protein and DNA interactions. Nucleic Acids Res 16:7351–7367 [CrossRef]
     [Google Scholar]
  16. Hirashima K., Watanabe Y. 2001; Tobamovirus replicase coding region is involved in cell-to-cell movement. J Virol 75:8831–8836 [CrossRef]
     [Google Scholar]
  17. Hirashima K., Watanabe Y. 2003; RNA helicase domain of tobamovirus replicase executes cell-to-cell movement possibly through collaboration with its nonconserved region. J Virol 77:12357–12362 [CrossRef]
     [Google Scholar]
  18. Hull R. 2002 Matthews' Plant Virology , 4th edn. San Diego: Academic Press;
     [Google Scholar]
  19. Kaplan I. B., Gal-On A., Palukaitis P. 1997; Characterization of cucumber mosaic virus. III. Localization of sequence in the movement protein controlling systemic infection in cucurbits. Virology 230:343–349 [CrossRef]
     [Google Scholar]
  20. Kim C. H., Palukaitis P. 1997; The plant defense response to cucumber mosaic virus in cowpea is elicited by viral polymerase gene and affects virus accumulation in single cells. EMBO J 16:4060–4068 [CrossRef]
     [Google Scholar]
  21. Kim S. H., Palukaitis P., Park Y. I. 2002; Phosphorylation of cucumber mosaic virus RNA polymerase 2a protein inhibits formation of replicase complex. EMBO J 21:2292–2300 [CrossRef]
     [Google Scholar]
  22. Lee K. C., Koh A., Loh C. S., Wong S. M. 2001; Cucurbita protoplast isolation for the study of plant virus replication. J Virol Methods 91:21–27 [CrossRef]
     [Google Scholar]
  23. Li Q., Ryu K. H., Palukaitis P. 2001; Cucumber mosaic virus–plant interactions: identification of 3a protein sequences affecting infectivity, cell-to-cell movement, and long-distance movement. Mol Plant Microbe Interact 14:378–385 [CrossRef]
     [Google Scholar]
  24. Nelson R. S., van Bel A. J. E. 1997; The mystery of virus trafficking into, through and out of vascular tissue. Prog Bot 59:477–533
     [Google Scholar]
  25. Owen J., Palukaitis P. 1988; Characterization of cucumber mosaic virus. I. Molecular heterogeneity mapping of RNA 3 in eight CMV strains. Virology 166:495–502 [CrossRef]
     [Google Scholar]
  26. Palukaitis P., García-Arenal F. 2003; Cucumoviruses. Adv Virus Res 62:241–323
     [Google Scholar]
  27. Peden K. W. C., Symons R. H. 1973; Cucumber mosaic virus contains a functionally divided genome. Virology 53:487–492 [CrossRef]
     [Google Scholar]
  28. Rao A. L. N., Francki R. I. B. 1982; Distribution of determinants for symptom production and host range in the three RNA components of cucumber mosaic virus. J Gen Virol 61:197–205 [CrossRef]
     [Google Scholar]
  29. Rizzo T. M., Palukaitis P. 1990; Construction of full-length cDNA clones of cucumber mosaic virus RNAs 1, 2, and 3: generation of infectious RNA transcripts. Mol Gen Genet 222:249–256 [CrossRef]
     [Google Scholar]
  30. Roossinck M. J. 1991; Temperature-sensitive replication of cucumber mosaic virus in muskmelon ( Cucumis melo cv. Iroquois), maps to RNA 1 of a slow strain. J Gen Virol 72:1747–1750 [CrossRef]
     [Google Scholar]
  31. Roossinck M. J., Palukaitis P. 1990; Rapid induction and severity of symptoms in zucchini squash ( Cucurbita pepo ) map to RNA 1 of cucumber mosaic virus. Mol Plant Microbe Interact 3:188–192 [CrossRef]
     [Google Scholar]
  32. Ryu K. H., Kim C. H., Palukaitis P. 1998; The coat protein of cucumber mosaic virus is a host range determinant for infection of maize. Mol Plant Microbe Interact 11:351–357 [CrossRef]
     [Google Scholar]
  33. Saitoh H., Fujiwara M., Ohki S. T., Osaki T. 1999; The coat protein gene is essential for the systemic infection of cucumber mosaic virus in Cucumis figarei at a high temperature. Ann Phytopathol Soc Jpn 65:248–253 [CrossRef]
     [Google Scholar]
  34. Sambrook J., Fritsch E. F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual , 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
     [Google Scholar]
  35. Simon J. N. 1957; Three strains of cucumber mosaic virus affecting bell pepper in the Everglades area in South Florida. Phytopathology 47:145–150
     [Google Scholar]
  36. Takeshita M., Suzuki M., Kuwata S., Takanami Y. 1998; Involvement of cucumber mosaic cucumovirus RNA 2 and RNA 3 in viral systemic spread in radish plant. Arch Virol 143:1109–1117 [CrossRef]
     [Google Scholar]
  37. Takeshita M., Suzuki M., Takanami Y. 2001; Combination of amino acids in the 3a protein and the coat protein of Cucumber mosaic virus determines symptom expression and viral spread in bottle gourd. Arch Virol 146:697–711 [CrossRef]
     [Google Scholar]
  38. Valkonen J. P. T., Slack S. A., Watanabe K. N. 1995; Resistance to cucumber mosaic virus in potato. Ann Appl Biol 126:143–151 [CrossRef]
     [Google Scholar]
  39. Wang Y., Tzfira T., Gaba V., Citovsky V., Palukaitis P., Gal-On A. 2004; Functional analysis of the Cucumber mosaic virus 2b protein: pathogenicity and nuclear localization. J Gen Virol 85:3135–3147 [CrossRef]
     [Google Scholar]
  40. Wong S. M., Thio S. S. C., Shintaku M. H., Palukaitis P. 1999; The rate of cell-to-cell movement in squash of cucumber mosaic virus is affected by sequences of the capsid protein. Mol Plant Microbe Interact 12:628–632 [CrossRef]
     [Google Scholar]
  41. Yoon J. Y., Min B. E., Choi J. K., Ryu K. H. 2002; Genome structure and production of biologically active in vitro transcripts of cucurbit-infecting Zucchini green mottle mosaic virus . Phytopathology 92:156–163 [CrossRef]
     [Google Scholar]
  42. Zaitlin M., Anderson J. M., Perry K. L., Zhang L., Palukaitis P. 1994; Specificity of replicase-mediated resistance to cucumber mosaic virus. Virology 201:200–205 [CrossRef]
     [Google Scholar]
  43. Zhang L., Hanada K., Palukaitis P. 1994; Mapping local and systemic symptom determinants of cucumber mosaic cucumovirus in tobacco. J Gen Virol 75:3185–3195 [CrossRef]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.80744-0
Loading
Cucumber mosaic virus 2a polymerase and 3a movement proteins independently affect both virus movement and the timing of symptom development in zucchini squash
J. Gen. Virol. 86, 1213 (2005); https://doi.org/10.1099/vir.0.80744-0
/content/journal/jgv/10.1099/vir.0.80744-0
/content/journal/jgv/10.1099/vir.0.80744-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error