Complementation between Two Tospoviruses Facilitates the Systemic Movement of a Plant Virus Silencing Suppressor in an Otherwise Restrictive Host

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Bag, Sudeep ^a   Mitter, Neena ^b   Eid, Sahar ^a   Pappu, Hanu R ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

SMALL INTERFERING RNA; VIRUS RNA;

ARTICLE; CONTROLLED STUDY; DATURA STRAMONIUM; GENE EXPRESSION; GENE FUNCTION; GENE MUTATION; GENE REPRESSION; GENE SILENCING; GENETIC COMPLEMENTATION; GENETIC REASSORTMENT; GENETIC RECOMBINATION; GENETIC VARIABILITY; HOST RESISTANCE; INOCULATION; IRIS YELLOW SPOT VIRUS; NONHUMAN; PLANT LEAF; RNA INTERFERENCE; SUPPRESSOR GENE; TOSPOVIRUS; VIRAL GENE SILENCING SUPPRESSOR GENE; VIRUS CELL INTERACTION; VIRUS GENE; VIRUS GENOME; VIRUS PATHOGENESIS; VIRUS VIRULENCE;

BASE SEQUENCE; DATURA; DNA PRIMERS; GENE SILENCING; GENES, VIRAL; GENETIC COMPLEMENTATION TEST; PLANT VIRUSES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TOSPOVIRUS;

EID: 84867593207     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0044803     Document Type: Article

References (50)

1. Elliott RM, (1997) Emerging Viruses: The Bunyaviridae. Molecular Medicine 3: 572-577.
2. Pappu HR, Jones RAC, Jain RK, (2009) Global status of tospovirus epidemics in diverse cropping systems: Successes gained and challenges ahead. Virus Research 141: 219-236.
3. Tsompana M, Moyer JW (2008) Tospoviruses. In: Mahy BWJ, Van Regenmortel, MHV editors. Encyclopedia of Virology. 3rd Edn. Vol 5. Elsevier Ltd, Oxford, UK. pp 157-162.
4. Pappu HR (2008) Tomato spotted wilt virus (Bunyaviridae). In: Mahy BWJ, Van Regenmortel, MHV editors. Encyclopedia of Virology. 3rd Edn., Vol 5. Elsevier Ltd, Oxford, UK. pp 133-138.
5. Adkins S, (2000) Tomato spotted wilt virus-positive steps towards negative success. Molecular Plant Pathology 1: 151-157.
6. Ullman DE, Meideros R, Campbell LR, Whitfield AE, Sherwood JL, et al. (2002) Thrips as vectors of tospoviruses. Advances in Botanical Research 36: 113-140.
7. Whitfield AE, Ullman DE, German TL, (2005) Tospovirus-thrips interactions. Annual Review Phytopathology 43: 459-489.
8. Mound LA (2001) So many thrips-so few tospovirus. In: Marullo R, Mound LA, editors. Thrips and Tospoviruses: Proceedings of the 7th International Symposium on Thysanoptera. pp 17-18.
9. Law MD, Moyer JW, (1990) A tomato spotted wilt-like virus with a serologically distinct N protein. Journal of General Virology 71: 933-938.
10. Mandal B, Jain RK, Krishnareddy M, Krishna Kumar NK, Ravi KS, et al. (2012) Emerging problems of Tospoviruses (Bunyaviridae) and their management in the Indian subcontinent. Plant Disease 96: 468-479.
11. Hall JM, Mohan K, Knott EA, Moyer JW, (1993) Tospoviruses associated with scape blight of onion (Allium cepa) seed crops in Idaho. Plant Disease 77: 952.
12. Webster CG, Perry KL, Lu X, Horsman L, Frantz G, et al. (2010) First report of Groundnut ringspot virus infecting tomato in south Florida. Plant Health Progress doi:10.1094/PHP-2010-0707-01-BR.
13. Zhou J, Kantartzi SK, Wen RH, Newman M, Hajimorad MR, et al. (2011) Molecular characterization of a new tospovirus infecting soybean. Virus Genes 43: 289-295.
14. Moya A, Elena SF, Bracho A, Miralles R, Barrio E, (2000) The evolution of RNA viruses: A population genetics view. Proc Natl Acad Sci USA 97: 6967-6973.
15. Webster CG, Stuart RR, Perry KL, Scott A, (2011) A natural M RNA reassortant arising from two species of plant- and insect-infecting bunyaviruses and comparison of its sequence and biological properties to parental species. Virology 413: 216-225.
16. Roossinck MJ, (1997) Mechanisms of plant virus evolution. Annual Review of Phytopathology 35: 191-209.
17. Moyer JW (2000) Tospoviruses. In: Hull R, editor. Encyclopedia of Microbiology. Vol. 4. Academic Press. pp. 592-597.
18. Kormelink R, Storms M, van Lent J, Peters D, Goldbach R, (1994) Expression and subcellular location of the NSm protein of Tomato spotted wilt virus (TSWV), a putative viral movement protein. Virology 200: 56-65.
19. Sin SH, McNulty BC, Kennedy GG, Moyer JW, (2005) Viral genetic determinants for thrips transmission of Tomato spotted wilt virus. Proc Natl Acad Sci USA 102: 5168-5173.
20. Takeda A, Sugiyamaa K, Naganob H, Moric M, Kaidoa M, et al. (2002) Identification of a novel RNA silencing suppressor, NSs protein of Tomato spotted wilt virus. FEBS Letters 532: 75-79.
21. Qiu WP, Geske SM, Hickey CM, Moyer JW, (1998) Tomato spotted wilt Tospovirus genome reassortment and genome segment-specific adaptation. Virology 244: 186-194.
22. Hoffmann K, Qiu WP, Moyer JW, (2001) Overcoming host and pathogen mediated resistance in tomato and tobacco maps to the M RNA of Tomato spotted wilt virus. Molecular Plant Microbe Interaction 14: 242-249.
23. Kunkalikar SR, Poojari S, Arun BM, Rajagopalan PA, Chen TC, et al. (2011) Importance and genetic diversity of vegetable-infecting tospoviruses in India. Phytopathology 101: 367-376.
24. Mullis SW, Langston DB Jr, Gitaitis RD, Sherwood JL, Csinos AC, (2004) First report of Vidalia onion (Allium cepa) naturally infected with Tomato spotted wilt virus and Iris yellow spot virus (family Bunyaviridae, genus Tospovirus) in Georgia. Plant Disease 88: 1285.
25. Bag S, Pappu HR, (2009) Symptomatology of Iris yellow spot virus in selected indicator hosts. Plant Health Progress doi:10.1094/PHP-2009-0824-01-BR.
26. Palukaitis P, Garci{dotless}a-Arenal F, (2003) Cucumoviruses. Advances in Virus Research 62: 241-323.
27. Wege C, Siegmund D, (2007) Synergism of a DNA and a RNA virus: enhanced tissue infiltration of the begomovirus Abutilon mosaic virus (AbMV) mediated by Cucumber mosaic virus (CMV). Virology 357: 10-28.
28. Webster CG, Turechek WW, Mellinger HC, Frantz G, Roe N, et al. (2011) Expansion of Groundnut ringspot virus host and geographic ranges in solanaceous vegetables in Peninsular Florida. Plant Health Progress doi:10.1094/PHP-2011-0725-01-BR.
29. Latham JR, Wilson AK, (2008) Transcomplementation and synergism in plants: implications for viral transgenes? Molecular Plant Pathology 9: 85-103.
30. Calvert LA, Ghabrial S, (1983) Enhancement by Soybean mosaic virus of Bean pod mottle virus titer in doubly infected soybean. Phytopathology 73: 992-997.
31. Choi SK, Yoon JY, Ryu KH, Choi JK, Palukaitis P, et al. (2002) Systemic movement of a movement-deficient strain of Cucumber mosaic virus in zucchini squash is facilitated by a cucurbit infecting potyvirus. Journal of General Virolology 83: 3173-3178.
32. Goldberg KB, Brakke MK, (1987) Concentration of Maize chlorotic mottle virus increased in mixed infections with Maize dwarf mosaic virus, strain B. Phytopathology 77: 162-167.
33. Ilenia RC, Beatriz XC, Roberto RM, Rafael FRB, (2011) Geminivirus mixed infection on pepper plants: Synergistic interaction between PHYVV and PepGMV. Virology Journal 8: 104.
34. Malyshenko SI, Kondakova OA, Taliansky M, Atabekov JG, (1989) Plant virus transport function: complementation by helper viruses is non-specific. Journal of General Virology 70: 2751-2757.
35. Mascia T, Fabrizio C, Fanelli V, Sialer MMF, De Stradis A, et al. (2010) Characterization of the interactions between Cucumber mosaic virus and Potato virus Y in mixed infections in tomato. Molecular Plant Microbe Interaction 23: 1514-1524.
36. Palukaitis P, Kaplan IB (1997) Synergy of virus accumulation and pathology in transgenic plants expressing viral sequences. In: Tepfer M, Balázs E. editors. Virus-Resistant Transgenic Plants: Potential Ecological Impact. Springer-Verlag, Berlin. pp 77-84.
37. Pruss G, Ge X, Shi XM, Carrington JC, Vance BV, (1997) Plant viral synergism: The potyviral genome encodes a broad range pathogenicity enhancer that trans-activates replication of heterologous viruses. Plant Cell 9: 859-868.
38. Vance VB, (1991) Replication of Potato virus X RNA is altered in coinfections with Potato virus Y. Virology 182: 486-494.
39. Wang Y, Gaba V, Yang J, Palukaitis P, Gal-on A, (2002) Characterization of synergy between Cucumber mosaic virus and potyviruses in cucurbit hosts. Phytopathology 92: 51-58.
40. Hassani-Mehraban A, Brenkman AB, van den Broek NJF, Goldbach R, Kormelink R, (2009) RNAi-mediated transgenic tospovirus resistance broken by intraspecies silencing suppressor protein complementation. Molecular Plant Microbe Interaction 22: 1250-1257.
41. Garcia S, Billecocq A, Crance JM, Prins M, Garin D, et al. (2006) Viral suppressors of RNA interference impair RNA silencing induced by a Semliki Forest virus replicon in tick cells. Journal of General Virology 87: 1985-1989.
42. Oliveira VC, Bartassona L, de Castrob MEB, Corrêaa JR, Ribeiroa BM, et al. (2011) A silencing suppressor protein (NSs) of a tospovirus enhances baculovirus replication in permissive and semipermissive insect cell lines. Virus Research 155: 259-267.
43. Lokesh B, Rashmi PR, Amruta BS, Srisathiyanarayanan D, Murthy MRN, et al. (2010) NSs encoded by Groundnut bud necrosis virus is a bifunctional enzyme. PLoS ONE 5: e9757.
44. Schnettler E, Hemmes H, Huismann R, Goldbach R, Prins M, et al. (2010) Diverging Affinity of Tospovirus RNA silencing suppressor proteins, NSs, for various RNA duplex molecules. Journal of Virology 84: 11542-11554.
45. Geerts-Dimitriadou C, Lu YY, Geertsema C, Goldbach R, Kormelink R, (2012) Analysis of the Tomato spotted wilt virus ambisense S RNA-encoded hairpin structure in translation. PLoS ONE 7: e31013.
46. Siddiqui SA, Valkonen JPT, Rajamäki ML, Lehto K, (2011) The 2b silencing suppressor of a mild strain of Cucumber mosaic virus alone is sufficient for synergistic interaction with Tobacco mosaic virus and induction of severe leaf malformation in 2b-Transgenic Tobacco Plants. Molecular Plant Microbe Interaction 24: 685-693.
47. Bag S, Druffel KL, Rondon S, Riley DG, Pappu HR, (2009) A serological assay for the detection of the nonstructural protein (NSs) of Iris yellow spot virus and its use in virus detection in plant and thrips vectors. Journal of Insect Science 10: 166.
48. Hamilton AJ, Voinnet O, Chappell L, Baulcombe DC, (2002) Two classes of short interfering RNA in RNA silencing. EMBO 21: 4671-4679.
49. Sambrook J, Fritsch EF, Maniatis T (2001) Molecular Cloning: A Laboratory Manual. 3rd (Ed). Cold Spring Harbor Laboratory Press, New York.
50. Mitter N, Sulistyowati E, Dietzgen RG, (2003) Cucumber mosaic virus infection transiently breaks dsRNA-induced transgenic immunity to Potato virus Y in tobacco. Molecular Plant Microbe Interactions 16: 936-944.