Interference with jasmonic acid-regulated gene expression is a general property of viral suppressors of RNA silencing but only partly explains virus-induced changes in plant-aphid interactions

Journal of General Virology

Volumn 95, Issue PART3, 2014, Pages 733-739

  Westwood, Jack H ^a   Lewsey, Mathew G ^a,b   Murphy, Alex M ^a   Tungadi, Trisna ^a   Bates, Anne ^a   Gilligan, Christopher A ^a   Carr, John P ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; APHIDS; CUCUMOVIRUS; CYCLOPENTANES; HOST-PARASITE INTERACTIONS; OXYLIPINS; PLANT DISEASES; POTEXVIRUS; RNA, VIRAL; SUPPRESSION, GENETIC; TOBACCO;

EID: 84894083683     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.060624-0     Document Type: Article

References (36)

1. Anandalakshmi, R., Pruss, G. J., Ge, X., Marathe, R., Mallory, A. C., Smith, T. H. & Vance, V. B. (1998). A viral suppressor of gene silencing in plants. Proc Natl Acad Sci U S A 95, 13079-13084.
2. Bari, R. & Jones, J. D. (2009). Role of plant hormones in plant defence responses. Plant Mol Biol 69, 473-488.
3. Brigneti, G., Voinnet, O., Li, W. X., Ji, L. H., Ding, S. W. & Baulcombe, D. C. (1998). Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana. EMBO J 17, 6739-6746.
4. Chen, H. Y., Yang, J., Lin, C. & Yuan, Y. A. (2008). Structural basis for RNA-silencing suppression by Tomato aspermy virus protein 2b. EMBO Rep 9, 754-760.
5. Chiu, M.-H., Chen, I. H., Baulcombe, D. C. & Tsai, C.-H. (2010). The silencing suppressor P25 of Potato virus X interacts with Argonaute1 and mediates its degradation through the proteasome pathway. Mol Plant Pathol 11, 641-649.
6. Cillo, F., Mascia, T., Pasciuto, M. M. & Gallitelli, D. (2009). Differential effects of mild and severe Cucumber mosaic virus strains in the perturbation of microRNA-regulated gene expression in tomato map to the 39 sequence of RNA 2. Mol Plant Microbe Interact 22, 1239-1249.
7. Devonshire, A. L. & Sawicki, R. M. (1979). Insecticide-resistant Myzus persicae as an example of evolution by gene duplication. Nature 280, 140-141.
8. Eigenbrode, S. D., Ding, H., Shiel, P. & Berger, P. H. (2002). Volatiles from potato plants infected with potato leafroll virus attract and arrest the virus vector, Myzus persicae (Homoptera: Aphididae). Proc Biol Sci 269, 455-460.
9. Ellis, C., Karafyllidis, I. & Turner, J. G. (2002). Constitutive activation of jasmonate signaling in an Arabidopsis mutant correlates with enhanced resistance to Erysiphe cichoracearum, Pseudomonas syringae, and Myzus persicae. Mol Plant Microbe Interact 15, 1025-1030.
10. Endres, M. W., Gregory, B. D., Gao, Z., Foreman, A. W., Mlotshwa, S., Ge, X., Pruss, G. J., Ecker, J. R., Bowman, L. H. & Vance, V. (2010). Two plant viral suppressors of silencing require the ethyleneinducible host transcription factor RAV2 to block RNA silencing. PLoS Pathog 6, e1000729.
11. González, I., Martínez, L., Rakitina, D. V., Lewsey, M. G., Atencio, F. A., Llave, C., Kalinina, N. O., Carr, J. P., Palukaitis, P. & Canto, T. (2010). Cucumber mosaic virus 2b protein subcellular targets and interactions: their significance to RNA silencing suppressor activity. Mol Plant Microbe Interact 23, 294-303.
12. González, I., Rakitina, D., Semashko, M., Taliansky, M., Praveen, S., Palukaitis, P., Carr, J. P., Kalinina, N. & Canto, T. (2012). RNA binding is more critical to the suppression of silencing function of Cucumber mosaic virus 2b protein than nuclear localization. RNA 18, 771-782.
13. Goto, K., Kobori, T., Kosaka, Y., Natsuaki, T. & Masuta, C. (2007). Characterization of silencing suppressor 2b of cucumber mosaic virus based on examination of its small RNA-binding abilities. Plant Cell Physiol 48, 1050-1060.
14. Harries, P. A., Palanichelvam, K., Bhat, S. & Nelson, R. S. (2008). Tobacco mosaic virus 126-kDa protein increases the susceptibility of Nicotiana tabacum to other viruses and its dosage affects virusinduced gene silencing. Mol Plant Microbe Interact 21, 1539-1548.
15. Harvey, J. J. W., Lewsey, M. G., Patel, K., Westwood, J., Heimstädt, S., Carr, J. P. & Baulcombe, D. C. (2011). An antiviral defense role of AGO2 in plants. PLoS ONE 6, e14639.
16. Ji, L. H. & Ding, S. W. (2001). The suppressor of transgene RNA silencing encoded by Cucumber mosaic virus interferes with salicylic acid-mediated virus resistance. Mol Plant Microbe Interact 14, 715-724.
17. Kovač, M., Müller, A., Milovanovič Jarh, D., Milavec, M., Düchting, P. & Ravnikar, M. (2009). Multiple hormone analysis indicates involvement of jasmonate signalling in the early defence of potato to potato virus YNTN. Biol Plant 53, 195-199.
18. Kurihara, Y., Inaba, N., Kutsuna, N., Takeda, A., Tagami, Y. & Watanabe, Y. (2007). Binding of tobamovirus replication protein with small RNA duplexes. J Gen Virol 88, 2347-2352.
19. Leather, S. R. & Dixon, A. F. G. (1984). Aphid growth and reproductive rates. Entomol Exp Appl 35, 137-140.
20. Lewsey, M., Robertson, F. C., Canto, T., Palukaitis, P. & Carr, J. P. (2007). Selective targeting of miRNA-regulated plant development by a viral counter-silencing protein. Plant J 50, 240-252.
21. Lewsey, M. G., Murphy, A. M., Maclean, D., Dalchau, N., Westwood, J. H., Macaulay, K., Bennett, M. H., Moulin, M., Hanke, D. E. & other authors (2010). Disruption of two defensive signaling pathways by a viral RNA silencing suppressor. Mol Plant Microbe Interact 23, 835-845.
22. Love, A. J., Geri, C., Laird, J., Carr, C., Yun, B.-W., Loake, G. J., Tada, Y., Sadanandom, A. & Milner, J. J. (2012). Cauliflower mosaic virus protein P6 inhibits signaling responses to salicylic acid and regulates innate immunity. PLoS ONE 7, e47535.
23. Lozano-Durán, R., Rosas-Díaz, T., Gusmaroli, G., Luna, A. P., Taconnat, L., Deng, X. W. & Bejarano, E. R. (2011). Geminiviruses subvert ubiquitination by altering CSN-mediated derubylation of SCF E3 ligase complexes and inhibit jasmonate signaling in Arabidopsis thaliana. Plant Cell 23, 1014-1032.
24. Mauck, K. E., De Moraes, C. M. & Mescher, M. C. (2010). Deceptive chemical signals induced by a plant virus attract insect vectors to inferior hosts. Proc Natl Acad Sci U S A 107, 3600-3605.
25. Palukaitis, P. & García-Arenal, F. (2003). Cucumoviruses. Adv Virus Res 62, 241-323.
26. Rohwer, C. L. & Erwin, J. E. (2008). Horticultural applications of jasmonates: a review. J Hortic Sci Biotechnol 83, 283-304.
27. Siddiqui, S. A., Sarmiento, C., Truve, E., Lehto, H. & 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.
28. Vogler, H., Akbergenov, R., Shivaprasad, P. V., Dang, V., Fasler, M., Kwon, M. O., Zhanybekova, S., Hohn, T. & Heinlein, M. (2007). Modification of small RNAs associated with suppression of RNA silencing by tobamovirus replicase protein. J Virol 81, 10379-10388.
29. Voinnet, O., Pinto, Y. M. & Baulcombe, D. C. (1999). Suppression of gene silencing: a general strategy used by diverse DNA and RNA viruses of plants. Proc Natl Acad Sci U S A 96, 14147-14152.
30. Wasternack, C. (2007). Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot (Lond) 100, 681-697.
31. Westwood, J. H. & Stevens, M. (2010). Resistance to aphid vectors of virus disease. Adv Virus Res 76, 179-210.
32. Westwood, J. H., McCann, L., Naish, M., Dixon, H., Murphy, A. M., Stancombe, M. A., Bennett, M. H., Powell, G., Webb, A. A. R. & Carr, J. P. (2013a). A viral RNA silencing suppressor interferes with abscisic acid-mediated signalling and induces drought tolerance in Arabidopsis thaliana. Mol Plant Pathol 14, 158-170.
33. Westwood, J. H., Groen, S. C., Du, Z., Murphy, A. M., Anggoro, D. T., Tungadi, T., Luang-In, V., Lewsey, M. G., Rossiter, J. T. & other authors (2013b). A trio of viral proteins tunes aphid-plant interactions in Arabidopsis thaliana. PLoS ONE 8, e83066.
34. Zhang, X., Yuan, Y. R., Pei, Y., Lin, S. S., Tuschl, T., Patel, D. J. & Chua, N. H. (2006). Cucumber mosaic virus-encoded 2b suppressor inhibits Arabidopsis Argonaute1 cleavage activity to counter plant defense. Genes Dev 20, 3255-3268.
35. Zhang, T., Luan, J. B., Qi, J. F., Huang, C. J., Li, M., Zhou, X. P. & Liu, S. S. (2012). Begomovirus-whitefly mutualism is achieved through repression of plant defences by a virus pathogenicity factor. Mol Ecol 21, 1294-1304.
36. Ziebell, H., Murphy, A. M., Groen, S. C., Tungadi, T., Westwood, J. H., Lewsey, M. G., Moulin, M., Kleczkowski, A., Smith, A. G. & other authors (2011). Cucumber mosaic virus and its 2b RNA silencing suppressor modify plant-aphid interactions in tobacco. Sci Rep 1, 187.