Cytorhabdovirus phosphoprotein shows RNA silencing suppressor activity in plants, but not in insect cells

Virology

Volumn 476, Issue , 2015, Pages 413-418

  Mann, Krin S ^a   Johnson, Karyn N ^a   Dietzgen, Ralf G ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Agroinfiltration; Drosophila S2 cells; Flock House virus; Green fluorescent protein; Lettuce necrotic yellows virus; RNA silencing suppression; Viral protein expression

Indexed keywords

GREEN FLUORESCENT PROTEIN; RNA; RNA SILENCING SUPPRESSOR PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VIRUS PHOSPHOPROTEIN; VIRUS PROTEIN; PHOSPHOPROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DROSOPHILA; FLOCK HOUSE VIRUS; GENE SILENCING; INSECT CELL; LETTUCE NECROTIC YELLOW VIRUS; NICOTIANA BENTHAMIANA; NONHUMAN; PLANT CELL; REPLICON; REPORTER GENE; RHABDOVIRIDAE; ANIMAL; COMPARATIVE STUDY; GENETICS; METABOLISM; RNA INTERFERENCE; TOBACCO; VIROLOGY;

CYTORHABDOVIRUS; FLOCK HOUSE VIRUS; HEXAPODA; LETTUCE NECROTIC YELLOWS VIRUS; NICOTIANA BENTHAMIANA; RHABDOVIRIDAE;

ANIMALS; DROSOPHILA; PHOSPHOPROTEINS; RHABDOVIRIDAE; RNA INTERFERENCE; TOBACCO; VIRAL PROTEINS;

EID: 84921059221     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2014.12.023     Document Type: Article

References (43)

1. Aliyari R., Wu Q., Li H.W., Wang X.H., Li F., Green L.D., Han C.S., Li W.X., Ding S.W. Mechanism of induction and suppression of antiviral immunity directed by virus-derived small RNAs in Drosophila. Cell Host Microbe 2008, 4:387-397.
2. Ammar E.D., Tsai C.W., Whitfield A.E., Redinbaugh M.G., Hogenhout S.A. Cellular and molecular aspects of rhabdovirus interactions with insect and plant hosts. Annu. Rev. Entomol. 2009, 54:447-468.
3. Anandalakshmi R., Pruss G.J., Ge X., Marathe R., Mallory A.C., Smith T.H., Vance V.B. A viral suppressor of gene silencing in plants. Proc. Natl. Acad. Sci. USA 1998, 95:13079-13084.
4. Azevedo J., Garcia D., Pontier D., Ohnesorge S., Yu A., Garcia S., Braun L., Bergdoll M., Hakimi M.A., Lagrange T., Voinnet O. Argonaute quenching and global changes in Dicer homeostasis caused by a pathogen-encoded GW repeat protein. Genes Dev. 2010, 24:904-915.
5. Berry B., Deddouche S., Kirschner D., Imler J.L., Antoniewski C. Viral suppressors of RNA silencing hinder exogenous and endogenous small RNA pathways in Drosophila. PLoS One 2009, 4:e5866.
6. Brigneti G., Voinnet O., Li W.X., Ji L.H., Ding S.W., Baulcombe D.C. Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana. EMBO J. 1998, 17:6739-6746.
7. Burgyan J., Havelda Z. Viral suppressors of RNA silencing. Trends Plant Sci. 2011, 16:265-272.
8. Chen H.Y., Yang J., Lin C., Yuan Y.A. Structural basis for RNA-silencing suppression by Tomato aspermy virus protein 2b. EMBO Rep. 2008, 9:754-760.
9. Chiu M.H., Chen I.H., Baulcombe D.C., Tsai C.H. The silencing suppressor P25 of Potato virus X interacts with Argonaute1 and mediates its degradation through the proteasome pathway. Mol. Plant Pathol. 2010, 11:641-649.
10. Csorba T., Lozsa R., Hutvagner G., Burgyan J. Polerovirus protein P0 prevents the assembly of small RNA-containing RISC complexes and leads to degradation of ARGONAUTE1. Plant J. 2010, 62:463-472.
11. Dietzgen R.G., Callaghan B., Wetzel T., Dale J.L. Completion of the genome sequence of Lettuce necrotic yellows virus, type species of the genus Cytorhabdovirus. Virus Res. 2006, 118:16-22.
12. Dietzgen R.G., Francki R.I. Analysis of lettuce necrotic yellows virus structural proteins with monoclonal antibodies and concanavalin A. Virology 1988, 166:486-494.
13. Dietzgen R.G., Kuzmin I.V. Taxonomy of Rhabdoviruses. Rhabdoviruses: Molecular taxonomy, Evolution, Genomics, Ecology, Host-Vector Interactions, Cytopathology and Control 2012, 13-22. Caister Academic Press, Norfolk, UK. R.G. Dietzgen, I.V. Kuzmin (Eds.).
14. Ding S.W., Voinnet O. Antiviral immunity directed by small RNAs. Cell 2007, 130:413-426.
15. Fusaro A.F., Correa R.L., Nakasugi K., Jackson C., Kawchuk L., Vaslin M.F., Waterhouse P.M. The Enamovirus P0 protein is a silencing suppressor which inhibits local and systemic RNA silencing through AGO1 degradation. Virology 2012, 426:178-187.
16. Gleave A.P. A versatile binary vector system with a T-DNA organisational structure conducive to efficient integration of cloned DNA into the plant genome. Plant Mol. Biol. 1992, 20:1203-1207.
17. Guo H., Song X., Xie C., Huo Y., Zhang F., Chen X.Y., Geng Y., Fang R. Rice yellow stunt rhabdovirus protein 6 suppresses systemic RNA silencing by blocking RDR6-mediated secondary siRNA synthesis. Mol. Plant. Microbe Interact. 2013, 26:927-936.
18. Hamilton A., Voinnet O., Chappell L., Baulcombe D. Two classes of short interfering RNA in RNA silencing. EMBO J. 2002, 21:4671-4679.
19. Incarbone M., Dunoyer P. RNA silencing and its suppression: novel insights from in planta analyses. Trends Plant Sci. 2013, 18:382-392.
20. Jackson A.O., Dietzgen R.G., Goodin M.M., Bragg J.N., Deng M. Biology of plant rhabdoviruses. Annu. Rev. Phytopathol. 2005, 43:623-660.
21. Johansen L.K., Carrington J.C. Silencing on the spot. Induction and suppression of RNA silencing in the Agrobacterium-mediated transient expression system. Plant Physiol. 2001, 126:930-938.
22. Kong L., Wang Y., Yang X., Sunter G., Zhou X. Broad bean wilt virus 2 encoded VP53, VP37 and large capsid protein orchestrate suppression of RNA silencing in plant. Virus Res. 2014, 192:62-73.
23. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
24. Li H., Li W.X., Ding S.W. Induction and suppression of RNA silencing by an animal virus. Science 2002, 296:1319-1321.
25. Li W.X., Li H., Lu R., Li F., Dus M., Atkinson P., Brydon E.W., Johnson K.L., Garcia-Sastre A., Ball L.A., Palese P., Ding S.W. Interferon antagonist proteins of influenza and vaccinia viruses are suppressors of RNA silencing. Proc. Natl. Acad. Sci. USA 2004, 101:1350-1355.
26. Lindbo J.A. TRBO: a high-efficiency tobacco mosaic virus RNA-based overexpression vector. Plant Physiol. 2007, 145:1232-1240.
27. Lu R., Folimonov A., Shintaku M., Li W.X., Falk B.W., Dawson W.O., Ding S.W. Three distinct suppressors of RNA silencing encoded by a 20-kb viral RNA genome. Proc. Natl. Acad. Sci. USA 2004, 101:15742-15747.
28. Mann K.S., Dietzgen R.G. Plant rhabdoviruses: new insights and research needs in the interplay of negative-strand RNA viruses with plant and insect hosts. Arch. Virol. 2014, 159:1889-1900.
29. Martin K.M., Dietzgen R.G., Wang R., Goodin M.M. Lettuce necrotic yellows cytorhabdovirus protein localization and interaction map, and comparison with nucleorhabdoviruses. J. Gen. Virol. 2012, 93:906-914.
30. Martinez-Priego L., Donaire L., Barajas D., Llave C. Silencing suppressor activity of the Tobacco rattle virus-encoded 16-kDa protein and interference with endogenous small RNA-guided regulatory pathways. Virology 2008, 376:346-356.
31. Mitter N., Dietzgen R.G. Use of hairpin RNA constructs for engineering plant virus resistance. Methods Mol. Biol. 2012, 894:191-208.
32. Reavy B., Dawson S., Canto T., MacFarlane S.A. Heterologous expression of plant virus genes that suppress post-transcriptional gene silencing results in suppression of RNA interference in Drosophila cells. BMC Biotechnol. 2004, 4:18.
33. Schneider I. Cell lines derived from late embryonic stages of Drosophila melanogaster. J. Embryol. Exp. Morphol. 1972, 27:353-365.
34. Schnettler E., Hemmes H., Huismann R., Goldbach R., Prins M., Kormelink R. Diverging affinity of tospovirus RNA silencing suppressor proteins, NSs, for various RNA duplex molecules. J. Virol. 2010, 84:11542-11554.
35. Silhavy D., Molnar A., Lucioli A., Szittya G., Hornyik C., Tavazza M., Burgyan J. A viral protein suppresses RNA silencing and binds silencing-generated, 21- to 25-nucleotide double-stranded RNAs. EMBO J. 2002, 21:3070-3080.
36. Stubbs L.L., Grogan R.G. Necrotic yellows: a newly recognized virus disease of lettuce. Aust. J. Agric. Res. 1963, 14:439-459.
37. Sulistyowati E., Mitter N., Bastiaan-Net S., Roossinck M., Dietzgen R. Host range, symptom expression and RNA 3 sequence analyses of six Australian strains of Cucumber mosaic virus. Australas. Plant Pathol. 2004, 33:505-512.
38. Valli A., López-Moya J.J., García J.A. Encyclopedia of Life Sciences 2009, John Wiley & Sons Ltd., Chichester.
39. Varallyay E., Valoczi A., Agyi A., Burgyan J., Havelda Z. Plant virus-mediated induction of miR168 is associated with repression of ARGONAUTE1 accumulation. EMBO J. 2010, 29:3507-3519.
40. Walker P.J., Dietzgen R.G., Joubert D.A., Blasdell K.R. Rhabdovirus accessory genes. Virus Res. 2011, 162:110-125.
41. Wetzel T., Dietzgen R.G., Geering A.D., Dale J.L. Analysis of the nucleocapsid gene of lettuce necrotic yellows rhabdovirus. Virology 1994, 202:1054-1057.
42. Ye K., Malinina L., Patel D.J. Recognition of small interfering RNA by a viral suppressor of RNA silencing. Nature 2003, 426:874-878.
43. Zhang X., Yuan Y.R., Pei Y., Lin S.S., Tuschl T., Patel D.J., Chua N.H. Cucumber mosaic virus-encoded 2b suppressor inhibits Arabidopsis Argonaute1 cleavage activity to counter plant defense. Genes Dev. 2006, 20:3255-3268.