1887

Journal of General Virology header logo

Volume 91, Issue 1

Pathogenicity of Alternanthera mosaic virus is affected by determinants in RNA-dependent RNA polymerase and by reduced efficacy of silencing suppression in a movement-competent TGB1 Free

Abstract

Four biologically active cDNA clones were derived from the Alternanthera mosaic virus (AltMV; genus ) isolate, AltMV-SP, which differ in symptoms in infected plants. Two clones induced necrosis and plant death; a mixture of all four clones induced milder symptoms than AltMV-SP. Replication of all clones was enhanced by a minimum of fourfold at 15 °C. A mixture of clones 4-7 (severe) and 3-1 (mild) was indistinguishable from AltMV-SP, but the ratio of 4-7 to 3-1 differed at 25 and 15 °C. RNA copy numbers of mixed infections were always below those of 4-7 alone. Determinants of symptom severity were identified in both Pol and TGB1; the mildest (4-1) and most severe (3-7) clones differed at three residues in the ‘core’ Pol domain [R(1110)P, K(1121)R, R(1255)K] and one [S(1535)P] in the C-terminal Pol domain of RNA-dependent RNA polymerase, and one in TGB1 [P(88)L]. Pol [P,R,K]+TGB1] always induced systemic necrosis at 15 °C. Gene exchanges of Pol and TGB1 each affected replication and symptom expression, with TGB1 significantly reducing silencing suppression. The difference in silencing suppression between TGB1 and TGB1 was confirmed by an agroinfiltration assay. Further, co-expression of TGB1 and TGB1 resulted in interference in the suppression of silencing by TGB1. Yeast two-hybrid analysis confirmed that TGB1 and TGB1 interact. These results identify a TGB1 residue that significantly affects replication and silencing suppression, but maintains full movement functions.

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

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.014977-0
2010-01-01
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/jgv/91/1/277.html?itemId=/content/journal/jgv/10.1099/vir.0.014977-0&mimeType=html&fmt=ahah

References

  1. Aldaoud, R., Dawson, W. O. & Jones, G. E.(1989). Rapid, random evolution of the genetic structure of replicating tobacco mosaic virus populations. Intervirology 30, 227–233. [Google Scholar]
  2. Bae, H., Kim, M. S., Sicher, R. C., Bae, H. J. & Bailey, B. A.(2006). Necrosis- and ethylene-inducing peptide from Fusarium oxysporum induces a complex cascade of transcripts associated with signal transduction and cell death in Arabidopsis. Plant Physiol 141, 1056–1067.[CrossRef] [Google Scholar]
  3. Bayne, E. H., Rakitina, D. V., Morozov, S. Y. & Baulcombe, D. C.(2005). Cell-to-cell movement of potato potexvirus X is dependent on suppression of RNA silencing. Plant J 44, 471–482.[CrossRef] [Google Scholar]
  4. Becker, D. M., Fikes, J. D. & Guarente, L.(1991). A cDNA encoding a human CCAAT-binding protein cloned by functional complementation in yeast. Proc Natl Acad Sci U S A 88, 1968–1972.[CrossRef] [Google Scholar]
  5. Bragg, J. N. & Jackson, A. O.(2004). The C-terminal region of the Barley stripe mosaic virusγb protein participates in homologous interactions and is required for suppression of RNA silencing. Mol Plant Pathol 5, 465–481.[CrossRef] [Google Scholar]
  6. Chellappan, P., Vanitharani, R., Ogbe, F. & Fauquet, C. M.(2005). Effect of temperature on geminivirus-induced RNA silencing in plants. Plant Physiol 138, 1828–1841.[CrossRef] [Google Scholar]
  7. Garcia-Arenal, F., Fraile, A. & Malpica, J. M.(2001). Variability and genetic structure of plant virus populations. Annu Rev Phytopathol 39, 157–186.[CrossRef] [Google Scholar]
  8. Geering, A. D. & Thomas, J. E.(1999). Characterisation of a virus from Australia that is closely related to papaya mosaic potexvirus. Arch Virol 144, 577–592.[CrossRef] [Google Scholar]
  9. Goodin, M. M., Dietzgen, R. G., Schichnes, D., Ruzin, S. & Jackson, A. O.(2002). pGD vectors: versatile tools for the expression of green and red fluorescent protein fusions in agroinfiltrated plant leaves. Plant J 31, 375–383.[CrossRef] [Google Scholar]
  10. Hagiwara, K., Ichiki, T. U., Ogawa, Y., Omura, T. & Tsuda, S.(2002). A single amino acid substitution in 126kDa protein of Pepper mild mottle virus associates with symptom attenuation in pepper; the complete nucleotide sequence of an attenuated strain, C-1421. Arch Virol 147, 833–840.[CrossRef] [Google Scholar]
  11. Hammond, J., Reinsel, M. D. & Maroon-Lango, C. J.(2006). Identification and full sequence of an isolate of Alternanthera mosaic potexvirus infecting Phlox stolonifera. Arch Virol 151, 477–493.[CrossRef] [Google Scholar]
  12. James, P., Halladay, J. & Craig, E. A.(1996). Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics 144, 1425–1436. [Google Scholar]
  13. Jovel, J., Walker, M. & Sanfacon, H.(2007). Recovery of Nicotiana benthamiana plants from a necrotic response induced by a nepovirus is associated with RNA silencing but not with reduced virus titer. J Virol 81, 12285–12297.[CrossRef] [Google Scholar]
  14. Kagiwada, S., Yamaji, Y., Komatsu, K., Takahashi, S., Mori, T., Hirata, H., Suzuki, M., Ugaki, M. & Namba, S.(2005). A single amino acid residue of RNA-dependent RNA polymerase in the Potato virus X genome determines the symptoms in Nicotiana plants. Virus Res 110, 177–182.[CrossRef] [Google Scholar]
  15. Kaper, J. M., Geletka, L. M., Wu, G. S. & Tousignant, M. E.(1995). Effect of temperature on cucumber mosaic virus satellite-induced lethal tomato necrosis is helper virus strain dependent. Arch Virol 140, 65–74.[CrossRef] [Google Scholar]
  16. Komatsu, K., Yamaji, Y., Ozeki, J., Hashimoto, M., Kagiwada, S., Takahashi, S. & Namba, S.(2008). Nucleotide sequence analysis of seven Japanese isolates of Plantago asiatica mosaic virus (PlAMV): a unique potexvirus with significantly high genomic and biological variability within the species. Arch Virol 153, 193–198.[CrossRef] [Google Scholar]
  17. Lewandowski, D. J. & Dawson, W. O.(1993). A single amino acid change in Tobacco mosaic virus replicase prevents symptom production. Mol Plant Microbe Interact 6, 157–160.[CrossRef] [Google Scholar]
  18. Liang, X. Z., Lee, B. T. & Wong, S. M.(2002). Covariation in the capsid protein of hibiscus chlorotic ringspot virus induced by serial passaging in a host that restricts movement leads to avirulence in its systemic host. J Virol 76, 12320–12324.[CrossRef] [Google Scholar]
  19. Lim, H. S., Ko, T. S., Lambert, K. N., Kim, H. G., Korban, S. S., Hartman, G. L. & Domier, L. L.(2005). Soybean mosaic virus helper component-protease enhances somatic embryo production and stabilizes transgene expression in soybean. Plant Physiol Biochem 43, 1014–1021.[CrossRef] [Google Scholar]
  20. Malcuit, I., Marano, M. R., Kavanagh, T. A., De Jong, W., Forsyth, A. & Baulcombe, D. C.(1999). The 25-kDa movement protein of PVX elicits Nb-mediated hypersensitive cell death in potato. Mol Plant Microbe Interact 12, 536–543.[CrossRef] [Google Scholar]
  21. Ozeki, J., Takahashi, S., Komatsu, K., Kagiwada, S., Yamashita, K., Mori, T., Hirata, H., Yamaji, Y., Ugaki, M. & Namba, S.(2006). A single amino acid in the RNA-dependent RNA polymerase of Plantago asiatica mosaic virus contributes to systemic necrosis. Arch Virol 151, 2067–2075.[CrossRef] [Google Scholar]
  22. Petty, I. T., Hunter, B. G., Wei, N. & Jackson, A. O.(1989). Infectious barley stripe mosaic virus RNA transcribed in vitro from full-length genomic cDNA clones. Virology 171, 342–349.[CrossRef] [Google Scholar]
  23. Qiu, W., Park, J. W. & Scholthof, H. B.(2002). Tombusvirus P19-mediated suppression of virus-induced gene silencing is controlled by genetic and dosage features that influence pathogenicity. Mol Plant Microbe Interact 15, 269–280.[CrossRef] [Google Scholar]
  24. Qu, F., Ye, X., Hou, G., Sato, S., Clemente, T. E. & Morris, T. J.(2005). RDR6 has a broad-spectrum but temperature-dependent antiviral defense role in Nicotiana benthamiana. J Virol 79, 15209–15217.[CrossRef] [Google Scholar]
  25. Rico, P., Ivars, P., Elena, S. F. & Hernandez, C.(2006). Insights into the selective pressures restricting Pelargonium flower break virus genome variability: evidence for host adaptation. J Virol 80, 8124–8132.[CrossRef] [Google Scholar]
  26. Schneider, W. L. & Roossinck, M. J.(2001). Genetic diversity in RNA virus quasispecies is controlled by host-virus interactions. J Virol 75, 6566–6571.[CrossRef] [Google Scholar]
  27. Shiboleth, Y. M., Haronsky, E., Leibman, D., Arazi, T., Wassenegger, M., Whitham, S. A., Gaba, V. & Gal-On, A.(2007). The conserved FRNK box in HC-Pro, a plant viral suppressor of gene silencing, is required for small RNA binding and mediates symptom development. J Virol 81, 13135–13148.[CrossRef] [Google Scholar]
  28. Siddiqui, S. A., Sarmiento, C., Kiisma, M., Koivumaki, S., Lemmetty, A., Truve, E. & Lehto, K.(2008). Effects of viral silencing suppressors on tobacco ringspot virus infection in two Nicotiana species. J Gen Virol 89, 1502–1508.[CrossRef] [Google Scholar]
  29. Silhavy, D. & Burgyán, J.(2004). Effects and side-effects of viral RNA silencing suppressors on short RNAs. Trends Plant Sci 9, 76–83. [Google Scholar]
  30. Simón, O., Williams, T., López-Ferber, M. & Caballero, P.(2005). Functional importance of deletion mutant genotypes in an insect nucleopolyhedrovirus population. Appl Environ Microbiol 71, 4254–4262.[CrossRef] [Google Scholar]
  31. Verchot-Lubicz, J., Ye, C. M. & Bamunusinghe, D.(2007). Molecular biology of potexviruses: recent advances. J Gen Virol 88, 1643–1655.[CrossRef] [Google Scholar]
  32. Voinnet, O., Lederer, C. & Baulcombe, D. C.(2000). A viral movement protein prevents spread of the gene silencing signal in Nicotiana benthamiana. Cell 103, 157–167.[CrossRef] [Google Scholar]
  33. Wurch, T., Lestienne, F. & Pauwels, P.(1998). A modified overlap extension PCR method to create chimeric genes in the absence of restriction enzymes. Biotechnol Tech 12, 653–657.[CrossRef] [Google Scholar]
  34. Yu, H. H. & Wong, S. M.(1998). Synthesis of biologically active cDNA clones of cymbidium mosaic potexvirus using a population cloning strategy. Arch Virol 143, 1617–1620.[CrossRef] [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.014977-0
Loading
Pathogenicity of Alternanthera mosaic virus is affected by determinants in RNA-dependent RNA polymerase and by reduced efficacy of silencing suppression in a movement-competent TGB1
J. Gen. Virol. 91, 277 (2010); https://doi.org/10.1099/vir.0.014977-0
/content/journal/jgv/10.1099/vir.0.014977-0
/content/journal/jgv/10.1099/vir.0.014977-0
Loading

Data & Media loading...

Supplements

vol. , part 1, pp. 277 - 287

Primers used in this study [PDF](46 KB)

PDF

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