Polycistronic artificial miRNA-mediated resistance to Wheat dwarf virus in barley is highly efficient at low temperature

Molecular Plant Pathology

Volumn 17, Issue 3, 2016, Pages 427-437

  Kis, András ^a   Tholt, Gergely ^b,c   Ivanics, Milán ^a   Várallyay, Éva ^a   Jenes, Barnabás ^a   Havelda, Zoltán ^a  

^a SZENT ISTVÁN UNIVERSITY   (Hungary)

^b INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^c EÖTVÖS LORÁND UNIVERSITY   (Hungary)

Author keywords

Artificial microRNA; Hordeum vulgare; Leafhopper; Low temperature; Resistance; Wheat dwarf virus

Indexed keywords

MICRORNA;

CHEMISTRY; COLD; CONFORMATION; DISEASE RESISTANCE; GENETICS; HORDEUM; METABOLISM; NUCLEOTIDE SEQUENCE; PHENOTYPE; PLANT DISEASE; TOBACCO; TRANSGENIC PLANT; VIROLOGY; WHEAT;

BASE SEQUENCE; COLD TEMPERATURE; DISEASE RESISTANCE; HORDEUM; MICRORNAS; NUCLEIC ACID CONFORMATION; PHENOTYPE; PLANT DISEASES; PLANTS, GENETICALLY MODIFIED; TOBACCO; TRITICUM;

EID: 84961242252     PISSN: 14646722     EISSN: 13643703     Source Type: Journal    
DOI: 10.1111/mpp.12291     Document Type: Article

References (50)

1. Ai, T., Zhang, L., Gao, Z., Zhu, C.X. and Guo, X. (2011) Highly efficient virus resistance mediated by artificial microRNAs that target the suppressor of PVX and PVY in plants. Plant Biol. 13, 304-316.
2. Bartlett, J.G., Alves, S.C., Smedley, M., Snape, J.W. and Harwood, W.A. (2008) High-throughput Agrobacterium-mediated barley transformation. Plant Methods, 4, 22.
3. Benkovics, A.H., Vida, G., Nelson, D., Veisz, O., Bedford, I., Silhavy, D., Boulton, M.I. (2010) Partial resistance to Wheat dwarf virus in winter wheat cultivars. Plant Pathol. 59, 1144-1151.
4. Bologna, N.G. and Voinnet, O. (2014) The diversity, biogenesis, and activities of endogenous silencing small RNAs in Arabidopsis. Annu. Rev. Plant Biol. 65, 473-503.
5. Boulton, M.I. (2002) Functions and interactions of mastrevirus gene products. Physiol. Mol. Plant Pathol. 60, 243-255.
6. Canto, T., Aranda, M.A. and Fereres, A. (2009) Climate change effects on physiology and population processes of hosts and vectors that influence the spread of hemipteran-borne plant viruses. Glob. Change Biol. 15, 1884-1894.
7. Chakraborty, S., Tiedemann, A.V. and Teng, P.S. (2000) Climate change: potential impact on plant diseases. Environ. Pollut. 108, 317-326.
8. Chen, X. (2012) Small RNAs in development-insights from plants. Curr. Opin. Genet. Dev. 22, 361-367.
9. Chen, X.M. (2009) Small RNAs and their roles in plant development. Annu. Rev. Cell Dev. Biol. 25, 21-44.
10. Christensen, A.H. and Quail, P.H. (1996) Ubiquitin promoter-based vectors for high-level expression of selectable and/or screenable marker genes in monocotyledonous plants. Transgenic Res. 5, 213-218.
11. Cillo, F. and Palukaitis, P. (2014) Transgenic resistance. Adv. Virus Res. 90, 35-146.
12. Deveson, I., Li, J. and Millar, A.A. (2013) MicroRNAs with analogous target complementarities perform with highly variable efficacies in Arabidopsis. FEBS Lett. 587, 3703-3708.
13. Di Nicola, E., Tavazza, M., Lucioli, A., Salandri, L. and Ilardi, V. (2014) Robust RNA silencing-mediated resistance to Plum pox virus under variable abiotic and biotic conditions. Mol. Plant Pathol. 15, 841-847.
14. Duan, C.G., Wang, C.H., Fang, R.X. and Guo, H.S. (2008) Artificial microRNAs highly accessible to targets confer efficient virus resistance in plants. J. Virol. 82, 11084-11095.
15. Fahim, M., Millar, A.A., Wood, C.C. and Larkin, P.J. (2012) Resistance to Wheat streak mosaic virus generated by expression of an artificial polycistronic microRNA in wheat. Plant Biotechnol. J. 10, 150-163.
16. Griesbach, R.J., Beek, R.M., Hammond, J. and Stommel, J.R. (2007) Gene expression in the star mutation of Petunia×hybrida Vilm. J. Am. Soc. Hortic. Sci. 132, 680-690.
17. Gu, W., Wang, X., Zhai, C., Xie, X. and Zhou, T. (2012) Selection on synonymous sites for increased accessibility around miRNA binding sites in plants. Mol. Biol. Evol. 29, 3037-3044.
18. Hu, Q., Niu, Y., Zhang, K., Liu, Y. and Zhou, X. (2011) Virus-derived transgenes expressing hairpin RNA give immunity to Tobacco mosaic virus and Cucumber mosaic virus. Virol. J. 8, 41.
19. Kasai, A., Ohnishi, S., Yamazaki, H., Funatsuki, H., Kurauchi, T., Matsumoto, T., Yumoto, S. and Senda, M. (2009) Molecular mechanism of seed coat discoloration induced by low temperature in yellow soybean. Plant Cell Physiol. 50, 1090-1098.
20. Koklu, G., Ramsell, J.N.E. and Kvarnheden, A. (2007) The complete genome sequence for a Turkish isolate of Wheat dwarf virus (WDV) from barley confirms the presence of two distinct WDV strains. Virus Genes, 34, 359-366.
21. Kung, Y.J., Lin, S.S., Huang, Y.L., Chen, T.C., Harish, S.S., Chua, N.H. and Yeh, S.D. (2012) Multiple artificial microRNAs targeting conserved motifs of the replicase gene confer robust transgenic resistance to negative-sense single-stranded RNA plant virus. Mol. Plant Pathol. 13, 303-317.
22. Li, J.F., Chung, H.S., Niu, Y., Bush, J., McCormack, M. and Sheen, J. (2013) Comprehensive protein-based artificial microRNA screens for effective gene silencing in plants. Plant Cell, 25, 1507-1522.
23. Li, J.F., Zhang, D. and Sheen, J. (2014) Epitope-tagged protein-based artificial miRNA screens for optimized gene silencing in plants. Nat. Protoc. 9, 939-949.
24. Lin, S.S., Wu, H.W., Elena, S.F., Chen, K.C., Niu, Q.W., Yeh, S.D. Chen, C.C. and Chua, N.H. (2009) Molecular evolution of a viral non-coding sequence under the selective pressure of amiRNA-mediated silencing. PLoS Pathog. 5, e1000312.
25. Lindblad, M. and Sigvald, R. (2004) Temporal spread of wheat dwarf virus and mature plant resistance in winter wheat. Crop Prot. 23, 229-234.
26. Lindsten, K. and Vacke, J. (1991) A possible barley adapted strain of Wheat Dwarf Virus (Wdv). Acta Phytopathol. Hun. 26, 175-180.
27. Manurung, B., Witsack, W., Mehner, S., Gruntzig, M. and Fuchs, E. (2005) Studies on biology and population dynamics of the leafhopper Psammotettix alienus Dahlb. (Homoptera: Auchenorrhyncha) as vector of Wheat dwarf virus (WDV) in Saxony-Anhalt, Germany. Z. Pflanzenk. Pflanzen. 112, 497-507.
28. Niu, Q.W., Lin, S.S., Reyes, J.L., Chen, K.C., Wu, H.W., Yeh, S.D. and Chua, N.H. (2006) Expression of artificial microRNAs in transgenic Arabidopsis thaliana confers virus resistance. Nat. Biotechnol. 24, 1420-1428.
29. Pall, G.S., Codony-Servat, C., Byrne, J., Ritchie, L. and Hamilton, A. (2007) Carbodiimide-mediated cross-linking of RNA to nylon membranes improves the detection of siRNA, miRNA and piRNA by northern blot. Nucleic Acids Res. 35, e60.
30. Pantaleo, V., Szittya, G. and Burgyan, J. (2007) Molecular bases of viral RNA targeting by viral small interfering RNA-programmed RISC. J. Virol. 81, 3797-3806.
31. Parizotto, E.A., Dunoyer, P., Rahm, N., Himber, C. and Voinnet, O. (2004) Invivo investigation of the transcription, processing, endonucleolytic activity, and functional relevance of the spatial distribution of a plant miRNA. Genes Dev. 18, 2237-2242.
32. Praslicka, J. (1997) Influence of occurrence of Psammotettix alienus on the degree of attack of winter wheat with wheat dwarf virus (WDV). Rost. Vyroba, 43, 81-85.
33. Qu, F., Ye, X.H., Hou, G.C., Sato, S., Clemente, T.E. and Morris, T.J. (2005) RDR6 has a broad-spectrum but temperature-dependent antiviral defense role in Nicotiana benthamiana. J. Virol. 79, 15209-15217.
34. Qu, J., Ye, J. and Fang, R. (2007) Artificial microRNA-mediated virus resistance in plants. J. Virol. 81, 6690-6699.
35. Ramsell, J.N.E., Boulton, M.I., Martin, D.P., Valkonen, J.P.T. and Kvarnheden, A. (2009) Studies on the host range of the barley strain of Wheat dwarf virus using an agroinfectious viral clone. Plant Pathol. 58, 1161-1169.
36. Schwab, R., Ossowski, S., Riester, M., Warthmann, N. and Weigel, D. (2006) Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell, 18, 1121-1133.
37. Seo, J.K., Wu, J.G., Lii, Y.F., Li, Y. and Jin, H.L. (2013) Contribution of small RNA pathway components in plant immunity. Mol. Plant-Microbe Interact. 26, 617-625.
38. Silhavy, D., Molnar, A., Lucioli, A., Szittya, G., Hornyik, C., Tavazza, M. and Burgyan, J. (2002) A viral protein suppresses RNA silencing and binds silencing-generated, 21- to 25-nucleotide double-stranded RNAs. EMBO J. 21, 3070-3080.
39. Simon-Mateo, C. and Garcia, J.A. (2006) MicroRNA-guided processing impairs Plum pox virus replication, but the virus readily evolves to escape this silencing mechanism. J. Virol. 80, 2429-2436.
40. Simon-Mateo, C. and Garcia, J.A. (2011) Antiviral strategies in plants based on RNA silencing. Biochim. Biophys. Acta, 1809, 722-731.
41. Szittya, G., Silhavy, D., Molnar, A., Havelda, Z., Lovas, A., Lakatos, L. Banfalvi, Z. and Burgyan, J. (2003) Low temperature inhibits RNA silencing-mediated defence by the control of siRNA generation. EMBO J. 22, 633-640.
42. Tiwari, M., Sharma, D. and Trivedi, P.K. (2014) Artificial microRNA mediated gene silencing in plants: progress and perspectives. Plant Mol. Biol. 86, 1-18.
43. Trebicki, P., Nancarrow, N., Cole, E., Bosque-Perez, N.A., Constable, F.E., Freeman, A.J., Rodoni, B., Yen, A.L., Luck, J.E. and Fitzgerald, G.J. (2015) Virus disease in wheat predicted to increase with a changing climate. Global Change Biol. doi:10.1111/gcb.12941.
44. Varallyay, E., Valoczi, A., Agyi, A., Burgyan, J. and Havelda, Z. (2010) Plant virus-mediated induction of miR168 is associated with repression of ARGONAUTE1 accumulation. EMBO J. 29, 3507-3519.
45. Varallyay, E., Olah, E. and Havelda, Z. (2014) Independent parallel functions of p19 plant viral suppressor of RNA silencing required for effective suppressor activity. Nucleic Acids Res. 42, 599-608.
46. Vu, T.V., Choudhury, N.R. and Mukherjee, S.K. (2013) Transgenic tomato plants expressing artificial microRNAs for silencing the pre-coat and coat proteins of a begomovirus, Tomato leaf curl New Delhi virus, show tolerance to virus infection. Virus Res. 172, 35-45.
47. Wang, M.B., Masuta, C., Smith, N.A. and Shimura, H. (2012) RNA silencing and plant viral diseases. Mol. Plant-Microbe Interact. 25, 1275-1285.
48. Wang, Y., Dang, M., Hou, H., Mei, Y., Qian, Y. and Zhou, X. (2014) Identification of an RNA silencing suppressor encoded by a mastrevirus. J. Gen. Virol. 95, 2082-2088.
49. Xu, P., Zhang, Y., Kang, L., Roossinck, M.J. and Mysore, K.S. (2006) Computational estimation and experimental verification of off-target silencing during posttranscriptional gene silencing in plants. Plant Physiol. 142, 429-440.
50. Zhang, X., Li, H., Zhang, J., Zhang, C., Gong, P., Ziaf, K. Xiao, F. and Ye, Z. (2011) Expression of artificial microRNAs in tomato confers efficient and stable virus resistance in a cell-autonomous manner. Transgenic Res. 20, 569-581.