A mycoreovirus suppresses RNA silencing in the white root rot fungus, Rosellinia necatrix

Virology

Volumn 444, Issue 1-2, 2013, Pages 409-416

  Yaegashi, Hajime ^a   Yoshikawa, Nobuyuki ^b   Ito, Tsutae ^a   Kanematsu, Satoko ^a  

^a NATIONAL INSTITUTE OF FRUIT TREE SCIENCE   (Japan)

^b IWATE UNIVERSITY   (Japan)

Author keywords

DsRNA virus; Mycovirus; Reovirus; RNA silencing; Rosellinia necatrix; Viral suppressor

Indexed keywords

DOUBLE STRANDED RNA; GREEN FLUORESCENT PROTEIN; SMALL INTERFERING RNA;

AGROINFILTRATION ASSAY; ARTICLE; BIOASSAY; CONTROLLED STUDY; GENE EXPRESSION; GENE IDENTIFICATION; GENE REPRESSION; GENE SILENCING; GREEN FLUORESCENT PROTEIN GENE; MICROBIAL ACTIVITY; MYCOREOVIRUS; NICOTIANA BENTHAMIANA; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RNA ANALYSIS; RNA SEQUENCE; RNA VIRUS; RNA VIRUS INFECTION; ROSELLINIA NECATRIX; S10 GENE; VIRUS CELL INTERACTION; VIRUS GENE; WHITE ROT FUNGUS;

DSRNA VIRUS; MYCOVIRUS; REOVIRUS; RNA SILENCING; ROSELLINIA NECATRIX; VIRAL SUPPRESSOR;

GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; GENE EXPRESSION REGULATION, VIRAL; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; REOVIRIDAE; RNA INTERFERENCE; XYLARIALES;

DSRNA VIRUSES; EUKARYOTA; FUNGI; MYCOREOVIRUS; MYCOREOVIRUS 3; MYCOVIRUS; ORTHOREOVIRUS; PARTITIVIRUS; ROSELLINIA NECATRIX;

EID: 84882904658     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2013.07.010     Document Type: Article

References (50)

1. Arakawa M., Nakamura H., Uetake Y., Matsumoto N. Presence and distribution of double-stranded RNA elements in the white root rot fungus Rosellinia necatrix. Mycoscience 2002, 43:21-26.
2. Baulcombe D.C. RNA silencing in plants. Nature 2004, 431:356-363.
3. Baulcombe D.C. Molecular biology. Amplified silencing. Science 2007, 315:199-200.
4. Bivalkar-Mehla S., Vakharia J., Mehla R., Abreha M., Kanwar J.R., Tikoo A., Chauhan A. Viral RNA silencing suppressors (RSS): novel strategy of viruses to ablate the host RNA interference (RNAi) defense system. Virus Res. 2011, 155:1-9.
5. 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.
6. Busch L.K., Rodríguez-Grille J., Casal J.I., Martínez-Costas J., Benavente J. Avian and mammalian reoviruses use different molecular mechanisms to synthesize their {micro}NS isoforms. J. Gen. Virol. 2011, 92:2566-2574.
7. Cao X., Zhou P., Zhang X., Zhu S., Zhong X., Xiao Q., Ding B., Li Y. Identification of an RNA silencing suppressor from a plant double-stranded RNA virus. J. Virol. 2005, 79:13018-13027.
8. Chiba S., Salaipeth L., Lin Y.H., Sasaki A., Kanematsu S., Suzuki N. A novel bipartite double-stranded RNA mycovirus from the white root rot fungus Rosellinia necatrix: molecular and biological characterization, taxonomic considerations, and potential for biological control. J. Virol. 2009, 83:12801-12812.
9. Chiba S., Kondo H., Tani A., Saisho D., Sakamoto W., Kanematsu S., Suzuki N. Widespread endogenization of genome sequences of non-retroviral RNA viruses into plant genomes. PLoS Pathog. 2011, 7:e1002146.
10. Chiba S., Lin Y.H., Kondo H., Kanematsu S., Suzuki N. Effects of defective-interfering RNA on symptom induction by, and replication of, a novel partitivirus from a phytopathogenic fungus Rosellinia necatrix. J. Virol. 2013, 87:2330-2341.
11. Chiba S., Lin Y.H., Kondo H., Kanematsu S., Suzuki N. A novel victorivirus from a phytopathogenic fungus, Rosellinia necatrix is infectious as particles and targeted by RNA silencing. J. Virol 2013, 87, 6727-6738.
12. Choi G.H., Pawlyk D.M., Nuss D.L. The autocatalytic protease p29 encoded by a hypovirulence-associated virus of the chestnut blight fungus resembles the potyvirus-encoded protease HC-Pro. Virology 1991, 183:747-752.
13. Cogoni C. Homology-dependent gene silencing mechanisms in fungi. Annu. Rev. Microbiol. 2001, 55:381-406.
14. Dang Y., Yang Q., Xue Z., Liu Y. RNA interference in fungi: pathways, functions, and applications. Eukaryot. Cell 2011, 10:1148-1155.
15. Ding S.W., Voinnet O. Antiviral immunity directed by small RNAs. Cell 2007, 130:413-426.
16. Ghabrial S.A., Suzuki N. Viruses of plant pathogenic fungi. Annu. Rev. Phytopathol. 2009, 47:353-384.
17. Hammond T.M., Andrewski M.D., Roossinck M.J., Keller N.P. Aspergillus mycoviruses are targets and suppressors 1 of RNA silencing. Eukaryot. Cell 2008, 7:350-357.
18. Hannon G.J. RNA interference. Nature 2002, 418:244-251.
19. Himeno M., Maejima K., Komatsu K., Ozeki J., Hashimoto M., Kagiwada S., Yamaji Y., Namba S. Significantly low level of small RNA accumulation derived from an encapsidated mycovirus with dsRNA genome. Virology 2010, 396:69-75.
20. Ikeda K., Nakamura H., Matsumoto N. Comparison between Rosellinia necatrix isolates from soil and diseased roots in terms of hypovirulence. FEMS Microbiol. Ecol. 2005, 54:307-315.
21. Jacobs B.L., Langland J.O. When two strands are better than one: the mediators and modulators of the cellular responses to double-stranded RNA. Virology 1996, 219:339-349.
22. Ji W.T., Lin F.L., Wang Y.C., Shih W.L., Lee L.H., Liu H.J. Intracellular cleavage of σA protein of avian reovirus. Virus Res. 2010, 149:71-77.
23. Kanematsu S., Arakawa M., Oikawa Y., Onoue M., Osaki H., Nakamura H., Ikeda K., Kuga-Uetake Y., Nitta H., Sasaki A., Suzaki K., Yoshida K., Matsumoto N. A reovirus causes hypovirulence of Rosellinia necatrix. Phytopathology 2004, 94:561-568.
24. Kanematsu S., Sasaki A., Onoue M., Oikawa Y., Ito T. Extending the fungal host range of a partitivirus and a mycoreovirus from Rosellinia necatrix by Inoculation of protoplasts with virus particles. Phytopathology 2010, 100:922-930.
25. Lin Y.H., Chiba S., Tani A., Kondo H., Sasaki A., Kanematsu S., Suzuki N. A novel quadripartite dsRNA virus isolated from a phytopathogenic filamentous fungus, Rosellinia necatrix. Virology 2012, 426:42-50.
26. Meister G., Tuschl T. Mechanisms of gene silencing by double-stranded RNA. Nature 2004, 431:343-349.
27. Mertens P. The dsRNA viruses. Virus Res. 2004, 101:3-13.
28. Mitsuhara I, Ugaki M., Hirochika H., Ohshima M., Murakami T., Gotoh Y., Katayose Y., Nakamura S., Honkura R., Nishimiya S., Ueno K., Mochizuki A., Tanimoto H., Tsugawa H., Otsuki Y., Ohashi Y. Efficient promoter cassettes for enhanced expression of foreign genes in dicotyledonous and monocotyledonous plants. Plant Cell Physiol. 1996, 37:49-59.
29. Namiki F., Matsunaga M., Okuda M., Inoue I., Nishi K., Fujita Y., Tsuge T. Mutation of an arginine biosynthesis gene causes reduced pathogenicity in Fusarium oxysporum f. sp. melonis. Mol. Plant-Microbe Interact. 2001, 14:580-584.
30. Pearson M.N., Beever R.E., Boine B., Arthur K. Mycoviruses of filamentous fungi and their relevance to plant pathology. Mol. Plant Pathol. 2009, 10:115-128.
31. Pliego C., Kanematsu S., Ruano-Rosa D., de Vicente A., López-Herrera C., Cazorla F.M., Ramos C. GFP sheds light on the infection process of avocado roots by Rosellinia necatrix. Fungal Genet. Biol. 2009, 46:137-145.
32. Qi N., Zhang L, Qiu Y, Wang Z., Si J., Liu Y, Xiang X., Xie J., Qin C.F., Zhou X., Hu Y. Targeting of dicer-2 and RNA by a viral RNA silencing suppressor in Drosophila cells. J. Virol. 2012, 86:5763-5773.
33. Ren B., Guo Y., Gao F., Zhou P., Wu F., Meng Z., Wei C., Li Y. Multiple functions of Rice dwarf phytoreovirus Pns10 in suppressing systemic RNA silencing. J. Virol. 2010, 84:12914-12923.
34. Roth BM, Pruss G.J., Vance V.B. Plant viral suppressors of RNA silencing. Virus Res. 2004, 102:97-108.
35. Sasaki A., Miyanishi M., Ozaki K., Onoue M., Yoshida K. Molecular characterization of a partitivirus from the plant pathogenic ascomycete Rosellinia necatrix. Arch. Virol. 2005, 150:1069-1083.
36. Sasaki A., Kanematsu S., Onoue M., Oyama Y., Yoshida K. Infection of Rosellinia necatrix with purified viral particles of a member of Partitiviridae (RnPV1-W8). Arch. Virol. 2006, 151:697-707.
37. Sasaki A., Kanematsu S., Onoue M., Oikawa Y., Nakamura H., Yoshida K. Artificial infection of Rosellinia necatrix with purified viral particles of a member of the genus mycoreovirus reveals its uneven distribution in single colonies. Phytopathology 2007, 97:278-286.
38. Segers G.C., van Wezel R., Zhang X., Hong Y., Nuss D.L. Hypovirus papain-like protease p29 suppresses RNA silencing in the natural fungal host and in a heterologous plant system. Eukaryot. Cell 2006, 5:896-904.
39. Segers G.C., Zhang X., Deng F., Sun Q., Nuss D.L. Evidence that RNA silencing functions as an antiviral defense mechanism in fungi. Proc. Nat. Acad. Sci. U.S.A. 2007, 104:12902-12906.
40. Shimizu T., Ito T., Kanematsu S. Transient and multivariate system for transformation of a fungal plant pathogen, Rosellinia necatrix, using autonomously replicating vectors. Curr. Genet. 2012, 58:129-138.
41. Sun Q., Choi G.H., Nuss D.L. A single Argonaute gene is required for induction of RNA silencing antiviral defense and promotes viral RNA recombination. Proc. Nat. Acad. Sci. U.S.A. 2009, 106:17927-17932.
42. Suzuki N., Supyani S., Maruyama K., Hillman B.I. Complete genome sequence of Mycoreovirus 1/Cp9B21, a member of a new genus within the family Reoviridae, from the chestnut blight fungus Cryphonectria parasitica. J. Gen. Virol. 2004, 85:3437-3448.
43. Voinnet O. Induction and suppression of RNA silencing: insights from viral infections. Nat. Rev. Genet. 2005, 6:206-220.
44. Wang M.B., Metzlaff M. RNA silencing and antiviral defense in plants. Curr. Opin. Plant Biol. 2005, 8:216-222.
45. Wang M.B., Masuta C., Smith N.A., Shimura H. RNA silencing and plant viral diseases. Mol. Plant-Microbe Interact. 2012, 25:1275-1285.
46. Wei C.Z., Osaki H., Iwanami T., Matsumoto N., Ohtsu Y. Complete nucleotide sequences of genome segments 1 and 3 of Rosellinia anti-rot virus in the family Reoviridae. Arch. Virol. 2004, 149:773-777.
47. Yaegashi H., Takahashi T., Isogai M., Kobori T., Ohki S., Yoshikawa N. Apple chlorotic leaf spot virus 50kDa movement protein acts as a suppressor of systemic silencing without interfering with local silencing in Nicotiana benthamiana. J. Gen. Virol. 2007, 88:316-324.
48. Yaegashi H., Sawahata T., Ito T., Kanematsu S. A novel colony-print immunoassay reveals differential patterns of distribution and horizontal transmission of four unrelated mycoviruses in Rosellinia necatrix. Virology 2011, 409:280-289.
49. Zamore P.D. Ancient pathways programmed by small RNAs. Science 2002, 296:1265-1269.
50. Zhang X., Segers G.C., Sun Q., Deng F, Nuss D.L. Characterization of hypovirus-derived small RNAs generated in the chestnut blight fungus by an inducible DCL-2-dependent pathway. J. Virol. 2008, 82:2613-2619.