Analysis of tospovirus nss proteins in suppression of systemic silencing

PLoS ONE

Volumn 10, Issue 8, 2015, Pages

  Hedil, Marcio ^a   Sterken, Mark G ^a   De Ronde, Dryas ^a   Lohuis, Dick ^a   Kormelink, Richard ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED RNA; GREEN FLUORESCENT PROTEIN; NSS PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VIRUS PROTEIN; PLANT RNA; VIRAL PROTEIN; VIRUS RNA;

ARTICLE; BINDING AFFINITY; GENE CONSTRUCT; GENE MUTATION; GENE SILENCING; GENETIC REGULATION; GROUNDNUT RINGSPOT VIRUS; NICOTIANA BENTHAMIANA; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN RNA BINDING; QUANTITATIVE ANALYSIS; RNA SILENCING SUPPRESSION; TOMATO SPOTTED WILT VIRUS; TOMATO YELLOW RING VIRUS; TOSPOVIRUS; VIRUS GENE; VIRUS ISOLATION; BINDING SITE; CHEMISTRY; COMPARATIVE STUDY; GENETICS; METABOLISM; MUTATION; RNA INTERFERENCE; TOBACCO; TRANSGENIC PLANT; VIROLOGY;

BINDING SITES; GREEN FLUORESCENT PROTEINS; MUTATION; PLANTS, GENETICALLY MODIFIED; RNA INTERFERENCE; RNA, DOUBLE-STRANDED; RNA, PLANT; RNA, VIRAL; TOBACCO; TOSPOVIRUS; VIRAL NONSTRUCTURAL PROTEINS;

EID: 84942868571     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0134517     Document Type: Article

References (41)

1. Roth BM, Pruss GJ, Vance VB. Plant viral suppressors of RNA silencing. Virus Res. 2004; 102(1):97-108. ISI:000221004900013. PMID: 15068885
2. Molnar A, Csorba T, Lakatos L, Varallyay E, Lacomme C, Burgyan J. Plant virus-derived small interfering RNAs originate predominantly from highly structured single-stranded viral RNAs. J Virol. 2005; 79 (12):7812-8. ISI:000229416100053. PMID: 15919934
3. Merai Z, Kerenyi Z, Kertesz S, Magna M, Lakatos L, Silhavy D. Double-stranded RNA binding may be a general plant RNA viral strategy to suppress RNA silencing. J Virol. 2006; 80(12):5747-56. ISI:000238103900011. PMID: 16731914
4. Lakatos L, Csorba T, Pantaleo V, Chapman EJ, Carrington JC, Liu YP, et al. Small RNA binding is a common strategy to suppress RNA silencing by several viral suppressors. Embo J. 2006; 25(12):2768-80. Epub 2006/05/26. 7601164 [pii] doi: 10.1038/sj.emboj.7601164 PMID: 16724105; PubMed Central PMCID: PMC1500863.
5. Lichner Z, Silhavy D, Burgyan J. Double-stranded RNA-binding proteins could suppress RNA interference-mediated antiviral defences. J Gen Virol. 2003; 84(Pt 4):975-80. Epub 2003/03/26. PMID: 12655099.
6. Baumberger N, Tsai CH, Lie M, Havecker E, Baulcombe DC. The Polerovirus silencing suppressor P0 targets ARGONAUTE proteins for degradation. Curr Biol. 2007; 17(18):1609-14. Epub 2007/09/18. S0960-9822(07)01856-8 [pii] PMID: 17869110.
7. Zhang XR, Yuan YR, Pei Y, Lin SS, Tuschl T, Patel DJ, et al. Cucumber mosaic virus-encoded 2b suppressor inhibits Arabidopsis Argonaute1 cleavage activity to counter plant defense. Gene Dev. 2006; 20(23):3255-68. ISI:000242527100007. PMID: 17158744
8. Voinnet O. Non-cell autonomous RNA silencing. Febs Lett. 2005; 579(26):5858-71. ISI:000233002500006. PMID: 16242131
9. Voinnet O, Baulcombe DC. Systemic signalling in gene silencing. Nature. 1997; 389(6651):553. doi: 10.1038/39215 ISI:A1997YA00800037. PMID: 9335491
10. Palauqui JC, Elmayan T, Pollien JM, Vaucheret H. Systemic acquired silencing: Transgene-specific post-transcriptional silencing is transmitted by grafting from silenced stocks to non-silenced scions. Embo J. 1997; 16(15):4738-45. ISI:A1997XR25500026. PMID: 9303318
11. Dunoyer P, Schott G, Himber C, Meyer D, Takeda A, Carrington JC, et al. Small RNA Duplexes Function as Mobile Silencing Signals Between Plant Cells. Science. 2010; 328(5980):912-6. ISI:000277618800055. doi: 10.1126/science.1185880 PMID: 20413458
12. Voinnet O, Vain P, Angell S, Baulcombe DC. Systemic spread of sequence-specific transgene RNA degradation in plants is initiated by localized introduction of ectopic promoterless DNA. Cell. 1998; 95 (2):177-87. ISI:000076538300006. PMID: 9790525
13. Baulcombe D. Viral suppression of systemic silencing. Trends Microbiol. 2002; 10(7):306-8. ISI:000176847300003. PMID: 12110203
14. Hamilton A, Voinnet O, Chappell L, Baulcombe D. Two classes of short interfering RNA in RNA silencing. Embo J. 2002; 21(17):4671-9. doi: 10.1093/Emboj/Cdf464 ISI:000177770100029. PMID: 12198169
15. Bucher E, Sijen T, de Haan P, Goldbach R, Prins M. Negative-strand tospoviruses and tenuiviruses carry a gene for a suppressor of gene silencing at analogous genomic positions. J Virol. 2003; 77 (2):1329-36. ISI:000180166600053. PMID: 12502849
16. Takeda A, Sugiyama K, Nagano H, Mori M, Kaido M, Mise K, et al. Identification of a novel RNA silencing suppressor, NSs protein of Tomato spotted wilt virus. Febs Lett. 2002; 532(1-2):75-9. Pii S0014-5793(02)03632-3. ISI:000179799200015. PMID: 12459466
17. King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ, editors. Ninth Report of the International Committee on Taxonomy of Viruses. London: Elsevier/Academic Press; 2012.
18. Pappu HR, Jones RAC, Jain RK. Global status of tospovirus epidemics in diverse cropping systems: Successes achieved and challenges ahead. Virus Res. 2009; 141(2):219-36. ISI:000265735600013. doi: 10.1016/j.virusres.2009.01.009 PMID: 19189852
19. Margaria P, Miozzi L, Rosa C, Axtell MJ, Pappu HR, Turina M. Small RNA profiles of wild-type and silencing suppressor-deficient tomato spotted wilt virus infected Nicotiana benthamiana. Virus Res. 2015; 208:30-8. Epub 2015/06/07. S0168-1702(15)00231-2 [pii] doi: 10.1016/j.virusres.2015.05.021 PMID: 26047586.
20. 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 (21):11542-54. doi: 10.1128/Jvi.00595-10 ISI:000282643400058. PMID: 20739523
21. Giner A, Lakatos L, Garcia-Chapa M, Lopez-Moya JJ, Burgyan J. Viral Protein Inhibits RISC Activity by Argonaute Binding through Conserved WG/GW Motifs. Plos Pathog. 2010; 6(7). ARTN e1000996 doi: 10.1371/journal.ppat.1000996 ISI:000280527000029.
22. de Ronde D, Pasquier A, Ying S, Butterbach P, Lohuis D, Kormelink R. Analysis of Tomato spotted wilt virus NSs protein indicates the importance of the N-terminal domain for avirulence and RNA silencing suppression. Mol Plant Pathol. 2014; 15(2):185-95. Epub 2013/10/10. doi: 10.1111/mpp.12082 PMID: 24103150.
23. Lokesh B, Rashmi PR, Amruta BS, Srisathiyanarayanan D, Murthy MR, Savithri HS. NSs encoded by groundnut bud necrosis virus is a bifunctional enzyme. Plos One. 2010; 5(3):e9757. Epub 2010/03/23. doi: 10.1371/journal.pone.0009757 PMID: 20305786; PubMed Central PMCID: PMC2841200.
24. Bhushan L, Abraham A, Choudhury NR, Rana VS, Mukherjee SK, Savithri HS. Demonstration of helicase activity in the nonstructural protein, NSs, of the negative-sense RNA virus, groundnut bud necrosis virus. Arch Virol. 2015; 160(4):959-67. Epub 2015/02/04. doi: 10.1007/s00705-014-2331-9 PMID: 25643815.
25. Ruiz MT, Voinnet O, Baulcombe DC. Initiation and maintenance of virus-induced gene silencing. Plant Cell. 1998; 10(6):937-46. ISI:000074567500007. PMID: 9634582
26. Luna AP, Morilla G, Voinnet O, Bejarano ER. Functional Analysis of Gene-Silencing Suppressors from Tomato Yellow Leaf Curl Disease Viruses. Mol Plant Microbe In. 2012; 25(10):1294-306. doi: 10.1094/Mpmi-04-12-0094-R ISI:000308781000003.
27. Valli A, Martin-Hernandez AM, Lopez-Moya JJ, Garcia JA. RNA silencing suppression by a second copy of the P1 serine protease of Cucumber vein yellowing ipomovirus, a member of the family Potyviridae that lacks the cysteine protease HCPro. J Virol. 2006; 80(20):10055-63. Epub 2006/09/29. 80/20/10055 [pii] doi: 10.1128/JVI.00985-06 PMID: 17005683; PubMed Central PMCID: PMC1617295.
28. de Ronde D, Butterbach P, Lohuis D, Hedil M, Van Lent JWM, Kormelink R. Tsw gene-based resistance is triggered by a functional RNA silencing suppressor protein of the Tomato spotted wilt virus. Mol Plant Pathol. 2013; 14(4):405-15. ISI:000317020200007. doi: 10.1111/mpp.12016 PMID: 23360130
29. Chen TC, Huang CW, Kuo YW, Liu FL, Yuan CH, Hsu HT, et al. Identification of Common Epitopes on a Conserved Region of NSs Proteins Among Tospoviruses of Watermelon silver mottle virus Serogroup. Phytopathology. 2006; 96(12):1296-304. Epub 2008/10/24. doi: 10.1094/PHYTO-96-1296 PMID: 18943661.
30. Molnar A, Melnyk C, Baulcombe DC. Silencing signals in plants: a long journey for small RNAs. Genome Biol. 2011; 12(1). ISI:000289437000003.
31. Burgyan J, Havelda Z. Viral suppressors of RNA silencing. Trends Plant Sci. 2011; 16(5):265-72. ISI:000291191000006. PMID: 21439890
32. Azevedo J, Garcia D, Pontier D, Ohnesorge S, Yu A, Garcia S, et al. Argonaute quenching and global changes in Dicer homeostasis caused by a pathogen-encodedGW repeat protein. Genes Dev. 2010; 24(9):904-15. Epub 2010/05/05. doi: 10.1101/gad.1908710 24/9/904 [pii]. PMID: 20439431; PubMed Central PMCID: PMC2861190.
33. Silhavy D, Burgyan J. Effects and side-effects of viral RNA silencing suppressors on short RNAs. Trends Plant Sci. 2004; 9(2):76-83. Epub 2004/04/23. doi: 10.1016/j.tplants.2003.12.010 S1360-1385 (03)00331-5 [pii]. PMID: 15102373.
34. Kormelink R, Kitajima EW, Dehaan P, Zuidema D, Peters D, Goldbach R. The Nonstructural Protein (Nss) Encoded by the Ambisense-S Rna Segment of Tomato Spotted Wilt Virus Is Associated with Fibrous Structures in Infected-Plant Cells. Virology. 1991; 181(2):459-68. ISI:A1991FB49600004. PMID: 1826573
35. Hassani-Mehraban A, Saaijer J, Peters D, Goldbach R, Kormelink R. A new tomato-infecting tospovirus from iran. Phytopathology. 2005; 95(8):852-8. Epub 2008/10/24. doi: 10.1094/PHYTO-95-0852 PMID: 18944405.
36. Hamilton CM, Frary A, Lewis C, Tanksley SD. Stable transfer of intact high molecular weight DNA into plant chromosomes. P Natl Acad Sci USA. 1996; 14:9975-9. doi: 10.1073/pnas.93.18.9975
37. Carbonell A, de Alba AEM, Flores R, Gago S. Double-stranded RNA interferes in a sequence-specific manner with the infection of representative members of the two viroid families. Virology. 2008; 371 (1):44-53. ISI:000252725700005. PMID: 18028975
38. Hedil M, Hassani-Mehraban A, Lohuis D, Kormelink R. Analysis of the A-U rich hairpin from the intergenic region of tospovirus S RNA as target and inducer of RNA silencing. Plos One. 2014; 9(9): e106027. Epub 2014/10/01.doi: 10.1371/journal.pone.0106027 PONE-D-14-15699 [pii]. PMID: 25268120; PubMed Central PMCID: PMC4182118.
39. Karimi M, Inze D, Depicker A. GATEWAY((TM)) vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 2002; 7(5):193-5. ISI:000175361600003. PMID: 11992820
40. de Avila AC, de Haan P, Smeets ML, Resende RD, Kormelink R, Kitajima EW, et al. Distinct Levels of Relationships between Tospovirus Isolates. Arch Virol. 1993; 128(3-4):211-27. ISI: A1993KK74000002. PMID: 8435042
41. Hassani-Mehraban A, Brenkman AB, van den Broek NJ, Goldbach R, Kormelink R. RNAi-mediated transgenic Tospovirus resistance broken by intraspecies silencing suppressor protein complementation. Mol Plant Microbe Interact. 2009; 22(10):1250-7. Epub 2009/09/10. doi: 10.1094/MPMI-22-10-1250 PMID: 19737098.