The Library
The role of the Cucumber mosaic virus 2b protein in viral movement and symptom induction
Tools
Lewsey, Mathew, Surette, Monique, Robertson, Fiona C. , Ziebell, Heiko, Choi, Sun Hee , Ryu, Ki Hyun , Canto, Tomas, Palukaitis, Peter, Payne, Tina, Walsh, John A. and Carr, John P.. (2009) The role of the Cucumber mosaic virus 2b protein in viral movement and symptom induction. Molecular Plant - Microbe Interactions, Vol.22 (No.6). pp. 642-654. ISSN 0894-0282
|
PDF
WRAP_Lewsey__0170657-270509-wrap_lewsey_mgl_30708_final_draft_pdf.pdf - Draft Version - Requires a PDF viewer such as GSview, Xpdf or Adobe Acrobat Reader Download (209Kb) |
Official URL: http://dx.doi.org/10.1094/MPMI-22-6-0642
Abstract
The Cucumber mosaic virus (CMV) 2b protein is a counter-defense factor and symptom determinant. Conserved domains in the 2b protein sequence were mutated in the 2b gene of strain Fny-CMV. The effects of these mutations were assessed by infection of Nicotiana tabacum, N. benthamiana, and Arabidopsis thaliana (ecotype Col-0) with mutant viruses and by expression of mutant 2b transgenes in A. thaliana. We confirmed that two nuclear localization signals were required for symptom induction and found that the N-terminal domain was essential for symptom induction. The C-terminal domain and two serine residues within a putative phosphorylation domain modulated symptom severity. Further infection studies were conducted using Fny-CMVΔ2b, a mutant that cannot express the 2b protein and that induces no symptoms in N. tabacum, N. benthamiana, or A. thaliana ecotype Col-0. Surprisingly, in plants of A. thaliana ecotype C24, Fny-CMVΔ2b induced severe symptoms similar to those induced by the wild-type virus. However, C24 plants infected with the mutant virus recovered from disease while those infected with the wild-type virus did not. Expression of 2b transgenes from either Fny-CMV or from LS-CMV (a mild strain) in Col-0 plants enhanced systemic movement of Fny-CMVΔ2b and permitted symptom induction by Fny-CMVΔ2b. Taken together, the results indicate that the 2b protein itself is an important symptom determinant in certain hosts. However, they also suggest that the protein may somehow synergize symptom induction by other CMV-encoded factors.
| Item Type: | Journal Article |
|---|---|
| Subjects: | Q Science > QR Microbiology > QR355 Virology Q Science > QR Microbiology |
| Divisions: | Faculty of Science > Life Sciences (2010- ) > Warwick HRI (2004-2010) |
| Library of Congress Subject Headings (LCSH): | Cucumber mosaic virus, Viral proteins, Virus diseases of plants -- Genetic aspects, Arabidopsis thaliana -- Diseases and pests, Tobacco -- Diseases and pests |
| Journal or Publication Title: | Molecular Plant - Microbe Interactions |
| Publisher: | American Phytopathological Society |
| ISSN: | 0894-0282 |
| Date: | June 2009 |
| Volume: | Vol.22 |
| Number: | No.6 |
| Page Range: | pp. 642-654 |
| Identification Number: | 10.1094/MPMI-22-6-0642 |
| Status: | Peer Reviewed |
| Access rights to Published version: | Open Access |
| Funder: | Biotechnology and Biological Sciences Research Council (Great Britain) (BBSRC), Great Britain. Dept. for Environment, Food & Rural Affairs (DEFRA), Scotland. Rural and Environment Research and Analysis Directorate (RERAD), Plant Signaling Network Research Center (Korea University) (PSNRC), Korean Science and Engineering Fund (KOSEF), Gatsby Charitable Foundation (GCF), Fondation Baxter et Alma Ricard (FBAR), Trinity Hall (University of Cambridge) |
| Grant number: | HH3205SFV (DEFRA), BB/D008204/1 (BBSRC), R11-2003-008-02002-0 (PSNRC), KRF-2005-214-C00156 (KOSEF) |
| References: | Brigneti, G., Voinnet, O., Li, W-X., Ji, L.-H., Ding, S.-W., and Baulcombe, D. C. 1998. Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana. EMBO (Eur. Mol. Biol. Organ.) J. 17:6739-6746. Chapman, E. J., Prokhnevsky, A. I., Gopinath, K., Dolja, V. V., and Carrington, J. C. 2004. Viral RNA silencing suppressors inhibit the microRNA pathway at an intermediate step. Genes Dev. 18:1179-1186. Chen, H.-Y., Yang, J., Lin, C., and Yuan, Y. A. 2008. Structural basis for RNA silencing suppression by Tomato aspermy virus protein 2b. EMBO (Eur. Mol. Biol. Organ.) Rep. 9:754-760. Clough, S. J., and Bent, A. 1998. Floral dip: A simplified method for Agrobacterium- mediated transformation of Arabidopsis thaliana. Plant J. 16:735-743. Deleris, A., Gallego-Bartolome, J., Bao, J., Kasschau, K. D., Carrington, J. C., and Voinnet, O. 2006. Hierarchical action and inhibition of plant Dicer-like proteins in antiviral defense. Science 313:68-71. Diaz-Pendon, J. A., Li, F., Li, W.-X., and Ding, S.-W. 2007. Suppression of antiviral silencing by cucumber mosaic virus 2b protein in Arabidopsis is associated with drastically reduced accumulation of three classes of viral small interfering RNAs. Plant Cell 19:2053-2063. Ding, S.-W., Anderson, B. J., Haase, H. R., and Symons, R. H. 1994. New overlapping gene encoded by the cucumber mosaic virus genome. Virology 198:593-601. Ding, S.-W., Li, W.-X., and Symons, R. H. 1995. A novel naturally occurring hybrid gene encoded by a plant RNA virus facilitates long distance virus movement. EMBO (Eur. Mol. Biol. Organ.) J. 14:5762-5772. Du, Z.-Y., Chen, F.-F., Liao, Q.-S., Zhang, H.-R., Chen, Y.-F., and Chen, J.-S. 2007. 2b ORFs encoded by subgroup IB strains of cucumber mosaic virus induce differential virulence on Nicotiana species. J. Gen. Virol. 88:2596-2604. Du, Z., Chen, F., Zhao, Z., Liao, Q., Palukaitis, P., and Chen, J. 2008. The 2b protein and the C-terminus of the 2a protein of cucumber mosaic virus subgroup I strains both play a role in viral RNA accumulation and induction of symptoms. Virology 380:363-370. Guo, H.-S., Xie, Q., Fei, J.-F., and Chua, N.-H. 2005. MicroRNA directs mRNA cleavage of the transcription factor NAC1 to down regulate auxin signals for Arabidopsis lateral root development. Plant Cell 17:1376-1386. Ham, B.-K., Lee, T.-H., You, J.-S., Nam Y.-W., Kim, J.-K., and Paek, K.-H. 1999. Isolation of a putative tobacco host factor interacting with cucumber mosaic virus-encoded 2b protein by yeast two-hybrid screening. Mol. Cells 9:548-555. Ji, L.-H., and Ding, S.-H. 2001. The suppressor of transgene RNA silencing encoded by Cucumber mosaic virus interferes with salicylic acidmediated virus resistance. Mol. Plant-Microbe Interact. 14:715-724. Jovel, J., Walker, M., and Sanfaçon, 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. Lewsey, M., Robertson, F. C., Canto, T, Palukaitis, P., and Carr, J. P. 2007. Selective targeting of miRNA-regulated plant development by a viral counter-silencing protein. Plant J. 50:240-252. Li, H. W., Lucy, A. P., Guo, H. S., Li, W-X., Wong, S. M., and Ding, S.-W. 1999. Strong host resistance targeted against a viral suppressor of the plant gene silencing defence mechanism. EMBO (Eur. Mol. Biol. Organ.) J. 18:2683-2691. Lot, H., Marrou, J., Quiot, J. B., and Esvan, C. 1972. Contribution á l’étude de virus de la mosaïque du concombre (CMV). II. Méthode de purification rapide du virus. Ann. Phytopathol. 4:25-38. Lucy, A. P., Guo, H.-S., Li, W.-X., and Ding, S.-W. 2000. Suppression of 654 / Molecular Plant-Microbe Interactions post-transcriptional gene silencing by a plant viral protein localized in the nucleus. EMBO (Eur. Mol. Biol. Organ.) J. 19:1672-1680. Mayers, C. N., Palukaitis, P., and Carr, J. P. 2000. Subcellular distribution analysis of the cucumber mosaic virus 2b protein. J. Gen. Virol. 81:219-226. Mourrain, P., Béclin, C., Elmayan, T., Feuerbach, F., Godon, C., Morel, J.-B., Jouette, D., Lacombe, A.-M., Nikic, S., Picault, N., Rémoué, K., Sanial, M., Vo, T.-A., and Vaucheret, H. 2000. Arabidopsis SGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance. Cell 101:533-542. Naylor, M., Murphy, A. M., Berry, J. O., and Carr, J. P. 1998. Salicylic acid can induce resistance to plant virus movement. Mol. Plant-Microbe Interact. 11:860-868. Palukaitis, P., and García-Arenal, F. 2003. Cucumoviruses. Adv. Virus Res. 62:242-323. Praveen, S., Mangrauthia, S. K., Singh, P., and Mishra, A. K. 2008. Behaviour of RNAi suppressor 2b of Cucumber mosaic virus in planta in presence and absence of virus. Virus Genes 37:96-102. Rizzo, T. M., and 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. Roossinck, M. J. 2001. Cucumber mosaic virus, a model for RNA virus evolution. Mol. Plant Pathol. 2:59-63. Roossinck, M. J., Zhang, L., and Hellewald, K. H. 1999. Rearrangements in the 5′ nontranslated region and phylogenetic analyses of cucumber mosaic virus RNA 3 indicate radial evolution of three subgroups. J. Gen. Virol. 73:6752-6758. Ryabov, E. V., Roberts, I. M., Palukaitis, P., and Taliansky, M. 2001. Umbravirus gene expression helps Potato leafroll virus to invade mesophyll tissues and to be transmitted mechanically between plants. Virology 286:363-372. Shi, B.-J., Palukaitis, P., and Symons, R. H. 2002. Differential virulence by strains of Cucumber mosaic virus is mediated by the 2b gene. Mol. Plant-Microbe Interact. 15:947-955. Shi, B.-J., Miller, J., Symons, R. H., and Palukaitis, P. 2003. The 2b protein of cucumoviruses has a role in promoting the cell-to-cell movement of pseudorecombinant viruses. Mol. Plant-Microbe Interact. 16:261-267. Siddiqui, S. A., Sarmiento, C., Truve, E., Lehto, H., and Lehto, K. 2008. Phenotypes and functional effects caused by various viral RNA silencing suppressors in transgenic Nicotiana benthamiana and N. tabacum. Mol. Plant-Microbe Interact. 21:178-187. Soards, A. J. 2003. The Cucumber mosaic virus 2b protein: Influences on the plant-virus interaction. Ph.D. thesis. Cambridge University. Soards, A. J., Murphy, A. M., Palukaitis, P., and Carr, J. P. 2002. Virulence and differential local and systemic spread of Cucumber mosaic virus in tobacco are affected by the CMV 2b protein. Mol. Plant-Microbe Interact. 15:647-653. Taliansky, M., Kim, S. H., Mayo, M. A., Kalinina, N. O., Fraser, G., McGeachy, K. D., and Barker, H. 2004. Escape of a plant virus from amplicon-mediated RNA silencing is associated with biotic or abiotic stress. Plant J. 39:194-205. Wang, Y., Tzfira, T., Gaba, V., Citovsky, V., Palukaitis, P., and Gal-On, A. 2004. Functional analysis of the Cucumber mosaic virus 2b protein: Pathogenicity and nuclear localization. J. Gen. Virol. 85:3135-3147. Ziebell, H., Payne, T., Berry, J. O., Walsh, J. A., and Carr, J. P. 2007. A cucumber mosaic virus mutant lacking the 2b counter-defence protein gene provides protection against wild-type strains. J. Gen. Virol. 88:2862-2861. Zhang, L., Hanada, K., and Palukaitis, P. 1994. Mapping local and systemic symptom determinants of cucumber mosaic cucumovirus in tobacco. J. Gen. Virol. 75:3185-3191. Zhang, X., Yuan, Y. R., Pei, Y., Lin, S.-S., Tuschl, T., Patel, D. J., and Chua, N.-H. 2006. Cucumber mosaic virus-encoded 2b suppressor inhibits Arabidopsis Argonaute1 cleavage activity to counter plant defense. Genes Dev. 20:3255-3268. |
| URI: | http://wrap.warwick.ac.uk/id/eprint/731 |
Data sourced from Thomson Reuters' Web of Knowledge
Actions (login required)
![]() |
View Item |
Tools
Tools

