Beet soil-borne mosaic virus RNA-4 encodes a 32kDa protein involved in symptom expression and in virus transmission through Polymyxa betae

Virology

Volumn 423, Issue 2, 2012, Pages 187-194

  D'Alonzo, Massimiliano ^a,b   Delbianco, Alice ^a,b   Lanzoni, Chiara ^a   Autonell, Concepcion Rubies ^a   Gilmer, David ^b   Ratti, Claudio ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

Benyvirus; Polymyxa betae; Replicon; Trans replication; Transmission

Indexed keywords

VIRUS PROTEIN; VIRUS RNA;

ARTICLE; BEET; BEET SOIL BORNE MOSAIC VIRUS; CHENOPODIUM QUINOA; GENE AMPLIFICATION; MOSAIC VIRUS; NEW SPECIES; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PARASITE VECTOR; PATHOGENESIS; PLANT DISEASE; PLANT ROOT; POLYMYXA; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPLICON; SUGAR BEET; VIRUS REPLICATION; VIRUS TRANSMISSION;

BETA VULGARIS; MOSAIC VIRUSES; PLANT DISEASES; PLASMODIOPHORIDA; RNA VIRUSES; SOIL MICROBIOLOGY; VIRAL PROTEINS;

BEET NECROTIC YELLOW VEIN VIRUS; BEET SOIL-BORNE MOSAIC VIRUS; BENYVIRUS; BETA VULGARIS; BETA VULGARIS SUBSP. VULGARIS; CHENOPODIUM QUINOA; POLYMYXA BETAE;

EID: 84855781375     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2011.12.007     Document Type: Article

References (38)

1. Bleykasten-Grosshans C., Guilley H., Bouzoubaa S., Richards K.E., Jonard G. Independent expression of the first two triple gene block proteins of beet necrotic yellow vein virus complements virus defective in the corresponding gene but expression of the third protein inhibits viral cell-to-cell movement. Mol. Plant Microbe Interact. 1997, 10:240-246.
2. Bouzoubaa S., Niesbach-Klosgen U., Jupin I., Guilley H., Richards K.E., Jonard G. Shortened forms of beet necrotic yellow vein virus RNA-3 and -4: internal deletions and a subgenomic RNA. J. Gen. Virol. 1991, 72:259-266.
3. 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.
4. Bujarski J.J., Kaesberg P. Genetic recombination between RNA components of a multipartite plant virus. Nature (London) 1986, 321:528-531.
5. Cheng C., Serviene E., Nagy P. Suppression of viral RNA recombination by a host exoribonuclease. J. Virol. 2006, 80:2631-2640.
6. Dunoyer P., Pfeffer S., Fritsch C., Hemmer O., Voinnet O., Richards K.E. Identification, subcellular localization and some properties of a cysteine-rich suppressor of gene silencing encoded by peanut clump virus. Plant J. 2002, 29:555-567.
7. Gilmer D., Ratti C. Benyvirus. Virus taxonomy: classification and nomenclature of viruses: Ninth Report of the International Committee on Taxonomy of Viruses 2012, 1133-1138. A.M.Q. King, M.J. Adams, E.B. Carstens, E.J. Lefkowitz (Eds.).
8. Guilley H., Bortolamiol D., Jonard G., Bouzoubaa S., Ziegler-Graff V. Rapid screening of RNA silencing suppressors by using a recombinant virus derived from beet necrotic yellow vein virus. J. Gen. Virol. 2009, 90:2536-2541.
9. Hehn A., Bouzoubaa S., Jonard G., Guilley H., Richards K.E. Artificial defective interfering RNAs derived from RNA 2 of beet necrotic yellow vein virus. Arch. Virol. 1994, 135:143-151.
10. Heidel G., Rush C.M., Kendall T., Lommel S., French R. Characteristics of beet soilborne mosaic virus, a furo-like virus infecting sugar beet. Plant Dis. 1997, 81:1070-1076.
11. Heijbroek W., Musters-van Oorschot P., Schoone A. Variation in pathogenicity and multiplication of beet necrotic yellow vein virus (BNYVV) in relation to the resistance of sugar-beet cultivars. Eur. J. Plant Pathol. 1999, 105:397-405.
12. Hirst G.K. Genetic recombination with Newcastle disease virus, polioviruses and influenza virus. Cold Spring Harb. Symp. Quant. Biol. 1962, 27:303-309.
13. Jianping C., MacFarlane S., Wilson T. Effect of cultivation temperature on the spontaneous development of deletions in soilborne wheat mosaic furovirus RNA 2. Phytopathology 1995, 85:299-306.
14. Jupin I., Richards K.E., Jonard G., Guilley H., Pleij C. Mapping sequences required for productive replication of beet necrotic yellow vein virus RNA 3. Virology 1990, 178:273-280.
15. Klein E., Link D., Schirmer A., Erhardt M., Gilmer D. Sequence variation within Beet necrotic yellow vein virus p25 protein influences its oligomerization and isolate pathogenicity on Tetragonia expansa. Virus Res. 2007, 126:53-61.
16. Koenig R., Stein B. Distribution of beet necrotic yellow vein virus in mechanically inoculated sugarbeet plantlets of cultivars with different degrees of rizomania resistance. Proceedings of the First Symposium of the International Working Group on Plant Viruses with Fungal Vectors, Braunschweig, Germany, August 21-2 1990, 87-90.
17. Lai M.M.C. RNA recombination in animal and plant viruses. Microbiol. Rev. 1992, 56:61-79.
18. Lauber E., Guilley H., Tamada T., Richards K.E., Jonard G. Vascular movement of beet necrotic yellow vein virus in Beta macrocarpa is probably dependent on an RNA 3 sequence domain rather than a gene product. J. Gen. Virol. 1998, 79(Pt 2):385-393.
19. Lauber E., Jonard G., Guilley H., Gilmer D. Effects of structural modifications upon the accumulation in planta of replicons derived from beet necrotic yellow vein virus RNA 3. Arch. Virol. 1999, 144:1201-1208.
20. Ledinko N. Genetic recombination with poliovirus type 1: studies of crosses between a normal horse serum-resistant mutant and several guanidine-resistant mutants of the same strain. Virology 1963, 20:107-119.
21. Lee L., Telford E.B., Batten J.S., Scholthof H.B., Rush C.M. Complete nucleotide sequence and genome organization of Beet soilborne mosaic virus, a proposed member of the genus Benyvirus. Arch. Virol. 2001, 146:2443-2453.
22. Li F., Ding S.-W. Virus counterdefense: diverse strategies for evading the RNA-silencing immunity. Annu. Rev. Microbiol. 2006, 60:503-531.
23. Link D., Schmidlin L., Schirmer A., Klein E., Erhardt M., Geldreich A., Lemaire O., Gilmer D. Functional characterization of the Beet necrotic yellow vein virus RNA-5-encoded p26 protein: evidence for structural pathogenicity determinants. J. Gen. Virol. 2005, 86:2115-2125.
24. Mahmood T., Rush C.M. Evidence of cross-protection between beet soilborne mosaic virus and beet necrotic yellow vein virus in sugar beet. Plant Dis. 1999, 83:521-526.
25. Meunier A., Schmit J.-F., Stas A., Kutluk N., Bragard C. Multiplex reverse transcription-PCR for simultaneous detection of Beet necrotic yellow vein virus, Beet soilborne virus, and Beet virus Q and their vector Polymyxa betae KESKIN on sugar beet. Appl. Environ. Microbiol. 2003, 69:2356-2360.
26. Miller W.A., White K.A. Long-distance RNA-RNA interactions in plant virus gene expression and replication. Annu. Rev. Phytopathol. 2006, 44:447-467.
27. Nagy P., Pogany J. Partial purification and characterization of cucumber necrosis virus and tomato bushy stunt virus RNA-dependent RNA polymerases: similarities and differences in template usage between tombusvirus and carmovirus RNA-dependent RNA polymerases. Virology 2000, 276:279-288.
28. Peltier C., Hleibieh K., Thiel H., Klein E., Bragard C., Gilmer D. Molecular biology of the beet necrotic yellow vein virus. Plant Viruses 2008, 2:14-24.
29. Quillet L., Guilley H., Jonard G., Richards K.E. In vitro synthesis of biologically active beet necrotic yellow vein virus RNA. Virology 1989, 172:293-301.
30. Rahim M.D., Andika I.B., Han C., Kondo H., Tamada T. RNA4-encoded p31 of beet necrotic yellow vein virus is involved in efficient vector transmission, symptom severity and silencing suppression in roots. J. Gen. Virol. 2007, 88:1611-1619.
31. Ratti C., Clover G.R.G., Rubies Autonell C., Harju V.A., Henry C.M. A multiplex RT-PCR assay capable of distinguishing beet necrotic yellow vein virus types A and B. J. Virol. Methods 2005, 124:41-47.
32. Ratti C., Hleibieh K., Bianchi L., Schirmer A., Rubies Autonell C., Gilmer D. Beet soil-borne mosaic virus RNA-3 is replicated and encapsidated in the presence of BNYVV RNA-1 and -2 and allows long distance movement in Beta macrocarpa. Virology 2009, 385:392-399.
33. Rush C.M. Ecology and epidemiology of benyviruses and plasmodiophorid vectors. Annu. Rev. Phytopathol. 2003, 41:567-592.
34. Schmidlin L., Link D., Mutterer J., Guilley H., Gilmer D. Use of a Beet necrotic yellow vein virus RNA-5-derived replicon as a new tool for gene expression. J. Gen. Virol. 2005, 86:463-467.
35. Tamada T., Abe H. Evidence that beet necrotic yellow vein virus RNA-4 is essential for efficient transmission by the fungus Polymyxa betae. J. Gen. Virol. 1989, 70:3391-3398.
36. Tamada T., Kusume T. Evidence that the 75K readthrough protein of beet necrotic yellow vein virus RNA-2 is essential for transmission by the fungus Polymyxa betae. J. Gen. Virol. 1991, 72(Pt 7):1497-1504.
37. Verchot-Lubicz J., Torrance L., Solovyev A.G., Morozov S.Y., Jackson A.O., Gilmer D. Varied movement strategies employed by triple gene block-encoding viruses. Mol. Plant Microbe Interact. 2010, 23:1231-1247.
38. Wisler G.C., Lewellen R., Sears J., Wasson J., Liu H.Y., Wintermantel W. Interactions between Beet necrotic yellow vein virus and Beet soilborne mosaic virus in sugar beet. Plant Dis. 2003, 87:1170-1175.