A viral RNA silencing suppressor interferes with abscisic acid-mediated signalling and induces drought tolerance in Arabidopsis thaliana

Molecular Plant Pathology

Volumn 14, Issue 2, 2013, Pages 158-170

  Westwood, Jack H ^a   Mccann, Lucy ^a,c   Naish, Matthew ^a   Dixon, Heather ^a,d   Murphy, Alex M ^a   Stancombe, Matthew A ^a   Bennett, Mark H ^b   Powell, Glen ^b   Webb, Alex A R ^a   Carr, John P ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^d UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

2B PROTEIN, CUCUMBER MOSAIC VIRUS; ABSCISIC ACID; AGO1 PROTEIN, ARABIDOPSIS; ARABIDOPSIS PROTEIN; ARGONAUTE PROTEIN; VIRUS PROTEIN; WATER;

ARABIDOPSIS; ARTICLE; DROUGHT; GENE EXPRESSION REGULATION; GENETICS; GERMINATION; METABOLISM; MOSAIC VIRUS; PHYSIOLOGY; PLANT STOMA; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SUPPRESSOR GENE; TRANSGENIC PLANT; VIROLOGY;

ABSCISIC ACID; ARABIDOPSIS; ARABIDOPSIS PROTEINS; ARGONAUTE PROTEINS; CUCUMOVIRUS; DROUGHTS; GENE EXPRESSION REGULATION, PLANT; GENES, SUPPRESSOR; GERMINATION; PLANT STOMATA; PLANTS, GENETICALLY MODIFIED; RNA INTERFERENCE; SIGNAL TRANSDUCTION; VIRAL PROTEINS; WATER;

ARABIDOPSIS; ARABIDOPSIS THALIANA; CUCUMBER MOSAIC VIRUS; CYTOMEGALOVIRUS;

EID: 84871723168     PISSN: 14646722     EISSN: 13643703     Source Type: Journal    
DOI: 10.1111/j.1364-3703.2012.00840.x     Document Type: Article

References (73)

1. Alexander, M. (1981) Why microbial predators and parasites do not eliminate their prey and hosts. Annu. Rev. Microbiol. 35, 113-133.
2. Anderson, R.M. and May, R.M. (1985) Coevolution of hosts and parasites. Parasitology, 85, 411-426.
3. Baumberger, N. and Baulcombe, D.C. (2005) Arabidopsis ARGONAUTE1 is an RNA Slicer that selectively recruits microRNAs and short interfering RNAs. Proc. Natl. Acad. Sci. USA, 102, 11928-11933.
4. Blevins, T., Rajeswaran, R., Shivaprasad, P.V., Beknazariants, D., Si-Ammour, A., Park, H.S., Vazquez, F., Robertson, D., Meins, F., Hohn, T. and Pooggin, M.M. (2006) Four plant dicers mediate viral small RNA biogenesis and DNA virus induced silencing. Nucleic Acids Res. 34, 6233-6246.
5. Boyes, D.C., Zayed, A.M., Ascenzi, R., McCaskill, A.J., Hoffman, N.E., Davis, K.R. and Gorlach, J. (2001) Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. Plant Cell, 13, 1499-1510.
6. 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 J. 17, 6739-6746.
7. Casimiro, I., Beeckman, T., Graham, N., Bhalerao, R., Zhang, H., Casero, P., Sandberg, G. and Bennett, M.J. (2003) Dissecting Arabidopsis lateral root development. Trends Plant Sci. 8, 165-171.
8. Csorba, T., Pantaleo, V. and Burgyán, J. (2009) RNA silencing: an antiviral mechanism. Adv. Virus Res. 75, 35-71.
9. Cutler, S.R., Rodriguez, P.L., Finkelstein, R.R. and Abrams, S.R. (2010) Abscisic acid: emergence of a core signaling network. Annu. Rev. Plant Biol. 61, 651-679.
10. De Torres Zabala, M., Bennet, M.H., Truman, W.H. and Grant, M.R. (2009) Antagonism between salicylic and abscisic acid reflects early host-pathogen conflict and moulds plant defence responses. Plant J. 59, 375-386.
11. Deleris, A., Gallego-Bartolome, J., Bao, J.S., 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.
12. Díaz-Pendón, J.A. and Ding, S.-W. (2008) Direct and indirect roles of viral suppressors of RNA silencing in pathogenesis. Annu. Rev. Phytopathol. 46, 303-326.
13. Duan, C.-G., Fang, Y.-Y., Zhou, B.-J., Zhao, J.-H., Hou, W.-N., Zhu, H., Ding, S.-W. and Guo, H.-S. (2012) Suppression of Arabidopsis ARGONAUTE1-mediated slicing, transgene-induced RNA silencing, and DNA methylation by distinct domains of the Cucumber mosaic virus 2b protein. Plant Cell, 24, 259-274.
14. Earley, K., Smith, M., Weber, R., Gregory, B. and Poethig, R. (2010) An endogenous F-box protein regulates ARGONAUTE1 in Arabidopsis thaliana. Silence, 1, 15.
15. Eckardt, N.A. (2005) MicroRNAs regulate auxin homeostasis and plant development. Plant Cell, 17, 1335-1338.
16. Forcat, S., Bennett, M., Mansfield, J. and Grant, M. (2008) A rapid and robust method for simultaneously measuring changes in the phytohormones ABA, JA and SA in plants following biotic and abiotic stress. Plant Methods, 4, 16.
17. Fraile, A. and García-Arenal, F. (2010) The coevolution of plants and viruses: resistance and pathogenicity. Adv. Virus Res. 76, 1-32.
18. González, I., Martínez, L., Rakitina, D.V., Lewsey, M.G., Atencio, F.A., Llave, C., Kalinina, N.O., Carr, J.P., Palukaitis, P. and 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.
19. González, I., Rakitina, D., Semashko, M., Taliansky, M., Praveen, S., Palukaitis, P., Carr, J.P., Kalinina, N. and 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.
20. Goto, K., Kobori, T., Kosaka, Y., Natsuaki, T. and 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.
21. Guo, H.S., Xie, Q., Fei, J.F. and Chua, N.H. (2005) MicroRNA directs mRNA cleavage of the transcription factor NAC1 to downregulate auxin signals for Arabidopsis lateral root development. Plant Cell, 17, 1376-1386.
22. 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.
23. Handford, M.G. and Carr, J.P. (2006) Plant metabolism associated with resistance and susceptibility. In: Natural Resistance Mechanisms of Plants to Viruses (Loebenstein, G. and Carr, J.P., eds), pp. 315-340. Dordrecht: Springer.
24. Harvey, J.J.W., Lewsey, M.G., Patel, K., Westwood, J., Heimstädt, S., Carr, J.P. and Baulcombe, D.C. (2011) An antiviral defense role of AGO2 in plants. Plos ONE, 6, e14639.
25. Hull, R. (2002) Matthews' Plant Virology, 4th edn. London: Academic Press.
26. Inaba, J., Kim, B.M., Shimura, H. and Masuta, C. (2011) Virus-induced necrosis is a consequence of direct protein-protein interaction between a viral RNA-silencing suppressor and a host catalase. Plant Physiol. 156, 2026-2036.
27. Jacobsen, S.E., Running, M.P. and Meyerowitz, E.M. (1999) Disruption of an RNA helicase/RNAse III gene in Arabidopsis causes unregulated cell division in floral meristems. Development, 126, 5231-5243.
28. Ji, L.H. and 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.
29. Khraiwesh, B., Zhu, J.-K. and Zhu, J. (2012) Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochim. Biophys. Acta, 1819, 137-148.
30. Lewsey, M.G. (2006) Effects of the Cucumber mosaic virus 2b gene and other viral sequences in transgenic plants. PhD Thesis, University of Cambridge.
31. Lewsey, M.G. and Carr, J.P. (2009) Effects of DICER-like proteins 2, 3 and 4 on cucumber mosaic virus and tobacco mosaic virus infections in salicylic acid-treated plants. J. Gen. Virol. 90, 3010-3014.
32. Lewsey, M.G., 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.
33. Lewsey, M.G., Surette, M., Robertson, F.C., Ziebell, H., Choi, S.H., Ryu, K.H., Canto, T., Palukaitis, P., Payne, T., Walsh, J.A. and Carr, J.P. (2009) The role of the Cucumber mosaic virus 2b protein in viral movement and symptom induction. Mol. Plant-Microbe Interact. 22, 642-654.
34. Lewsey, M.G., Murphy, A.M., MacLean, D., Dalchau, N., Westwood, J.H., Macaulay, K., Bennett, M.H., Moulin, M., Hanke, D.E., Powell, G., Smith, A.G. and Carr, J.P. (2010) Disruption of two defensive signaling pathways by a viral RNA silencing suppressor. Mol. Plant-Microbe Interact. 23, 835-845.
35. Li, W., Cui, X., Meng, Z., Huang, X., Xie, Q., Wu, H., Jin, H., Zhang, D. and Liang, W. (2012) Transcriptional regulation of Arabidopsis MIR168a and ARGONAUTE1 homeostasis in abscisic acid and abiotic stress responses. Plant Physiol. 158, 1279-1292.
36. Li, W.-X., Oono, Y., Zhu, J., He, X.-J., Wu, J.-M., Iida, K., Lu, X.-Y., Cui, X., Jin, H. and Zhu, J.-K. (2008) The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. Plant Cell, 20, 2238-2251.
37. Lozano-Duran, R., Rosas-Diaz, T., Gusmaroli, G., Luna, A.P., Taconnat, L., Deng, X.W. and 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.
38. Malamy, J.E. and Ryan, K.S. (2001) Environmental regulation of lateral root initiation in Arabidopsis. Plant Physiol. 127, 899-909.
39. Mallory, A.C. and Vaucheret, H. (2009) ARGONAUTE 1 homeostasis invokes the coordinate action of the microRNA and siRNA pathways. EMBO Rep. 10, 521-526.
40. Mallory, A.C., Bartel, D.P. and Bartel, B. (2005) MicroRNA-directed regulation of Arabidopsis AUXIN RESPONSE FACTOR17 is essential for proper development and modulates expression of early auxin response genes. Plant Cell, 17, 1360-1375.
41. Marin, E., Jouannet, V., Herz, A., Lokerse, A.S., Weijers, D., Vaucheret, H., Nussaume, L., Crespi, M.D. and Maizel, A. (2010) miR390, Arabidopsis TAS3 tasiRNAs, and their AUXIN RESPONSE FACTOR targets define an autoregulatory network quantitatively regulating lateral root growth. Plant Cell, 22, 1104-1117.
42. Marquez, L.M., Redman, R.S., Rodriguez, R.J. and Roossinck, M.J. (2007) A virus in a fungus in a plant: three-way symbiosis required for thermal tolerance. Science, 315, 513-515.
43. Martínez de Alba, A.E., Jauvion, V., Mallory, A.C., Bouteiller, N. and Vaucheret, H. (2011) The miRNA pathway limits AGO1 availability during siRNA-mediated PTGS defense against exogenous RNA. Nucleic Acids Res. 39, 9339-9344.
44. Mochizuki, T. and Ohki, S.T. (2012) Cucumber mosaic virus: viral genes as virulence determinants. Mol. Plant Pathol. 13, 217-225.
45. Morel, J.B., Godon, C., Mourrain, P., Beclin, C., Boutet, S., Feuerbach, F., Proux, F. and Vaucheret, H. (2002) Fertile hypomorphic ARGONAUTE (ago1) mutants impaired in post-transcriptional gene silencing and virus resistance. Plant Cell, 14, 629-639.
46. Nakahara, K.S., Masuta, C., Yamada, S., Shimura, H., Kashihara, Y., Wada, T.S., Meguro, A., Goto, K., Tadamura, K., Sueda, K., Sekiguchi, T., Shao, J., Itchoda, N., Matsumura, T., Igarashi, M., Ito, K., Carthew, R.W. and Uyeda, I. (2012) Tobacco calmodulin-like protein provides secondary defense by binding to and directing degradation of virus RNA silencing suppressors. Proc. Natl. Acad. Sci. USA, 109, 10113-10118.
47. Ng, J. and Perry, K.L. (1999) Stability of the aphid transmission phenotype in cucumber mosaic virus. Plant Pathol. 48, 388-394.
48. Nibau, C., Gibbs, D.J. and Coates, J.C. (2008) Branching out in new directions: the control of root architecture by lateral root formation. New Phytol. 179, 595-614.
49. Pagán, I., Fraile, A., Fernandez-Fueyo, E., Montes, N., Alonso-Blanco, C. and García-Arenal, F. (2010) Arabidopsis thaliana as a model for the study of plant-virus co-evolution. Philos. Trans. R. Soc. London, B: Biol. Sci. 365, 1983-1995.
50. R Development Core Team (2011) R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing.
51. Raghavendra, A.S., Gonugunta, V.K., Christmann, A. and Grill, E. (2010) ABA perception and signalling. Trends Plant Sci. 15, 395-401.
52. Ramakers, C., Ruijter, J.M., Deprez, R.H.L. and Moorman, A.F.M. (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci. Lett. 339, 62-66.
53. Reyes, J.L. and Chua, N.-H. (2007) ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seed germination. Plant J. 49, 592-606.
54. Robertson, F.C., Skeffington, A.W., Gardner, M.J. and Webb, A.A.R. (2009) Interactions between circadian and hormonal signalling in plants. Plant Mol. Biol. 69, 419-427.
55. Rodrigo, G., Carrera, J., Ruiz-Ferrer, V., del Toro, F.J., Llave, C., Voinnet, O. and Elena, S.F. (2012) A meta-analysis reveals the commonalities and differences in Arabidopsis thaliana response to different viral pathogens. Plos ONE, 7, e40526.
56. Roossinck, M.J. (2011) The good viruses: viral mutualistic symbioses. Nat. Rev. Microbiol. 9, 99-108.
57. Roossinck, M.J. and 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.
58. Ruijter, J.M., Ramakers, C., Hoogaars, W.M.H., Karlen, Y., Bakker, O., van den Hoff, M.J.B. and Moorman, A.F.M. (2009) Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res. 37, e45.
59. Ryabov, E.V., Fraser, G., Mayo, M.A., Barker, H. 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.
60. Ryabov, E.V., Keane, G., Naish, N., Evered, C. and Winstanley, D. (2009) Densovirus induces winged morphs in asexual clones of the rosy apple aphid, Dysaphis plantaginea. Proc. Natl. Acad. Sci. USA, 106, 8465-8470.
61. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. New York: Cold Spring Harbor Laboratory Press.
62. Schauer, S.E., Jacobsen, S.E., Meinke, D.W. and Ray, A. (2002) DICER-LIKE1: blind men and elephants in Arabidopsis development. Trends Plant Sci. 7, 487-491.
63. Schommer, C., Palatnik, J.F., Aggarwal, P., Chetelat, A., Cubas, P., Farmer, E.E., Nath, U. and Weigel, D. (2008) Control of jasmonate biosynthesis and senescence by miR319 targets. Plos Biol. 6, e230.
64. Sirichandra, C., Wasilewska, A., Vlad, F., Valon, C. and Leung, J. (2009) The guard cell as a single-cell model towards understanding drought tolerance and abscisic acid action. J. Exp. Bot. 60, 1439-1463.
65. Sunkar, R., Chinnusamy, V., Zhu, J. and Zhu, J.-K. (2007) Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends Plant Sci. 12, 301-309.
66. Whitham, S.A., Quan, S., Chang, H.S., Cooper, B., Estes, B., Zhu, T., Wang, X. and Hou, Y.M. (2003) Diverse RNA viruses elicit the expression of common sets of genes in susceptible Arabidopsis thaliana plants. Plant J. 33, 271-283.
67. Xiong, L. and Zhu, J.-K. (2003) Regulation of abscisic acid biosynthesis. Plant Physiol. 133, 29-36.
68. Xu, P., Chen, F., Mannas, J.P., Feldman, T., Sumner, L.W. and Roossinck, M.J. (2008) Virus infection improves drought tolerance. New Phytol. 180, 911-921.
69. Yuan, J.S., Wang, D. and Stewart, C.N. Jr (2008) Statistical methods for efficiency adjusted real-time PCR quantification. Biotechnol. J. 3, 112-123.
70. Zhang, J.-F., Yuan, L.-J., Shao, Y.I., Du, W.E.I., Yan, D.-W. and Lu, Y.-T. (2008) The disturbance of small RNA pathways enhanced abscisic acid response and multiple stress responses in Arabidopsis. Plant Cell Environ. 31, 562-574.
71. Zhang, X.R., 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.
72. Ziebell, H. and Carr, J.P. (2009) Effects of dicer-like endoribonucleases 2 and 4 on infection of Arabidopsis thaliana by cucumber mosaic virus and a mutant virus lacking the 2b counter-defence protein gene. J. Gen. Virol. 90, 2288-2292.
73. Ziebell, H., Murphy, A.M., Groen, S.C., Tungadi, T., Westwood, J.H., Lewsey, M.G., Moulin, M., Kleczkowski, A., Smith, A.G., Stevens, M., Powell, G. and Carr, J.P. (2011) Cucumber mosaic virus and its 2b RNA silencing suppressor modify plant-aphid interactions in tobacco. Sci. Rep. 1, 187. DOI:110.1038/srep00187.