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PMID: 14512550 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Tomato mosaic virus replication protein suppresses virus-targeted posttranscriptional gene silencing.

Journal of virology ·Vol. 77 ·No. 20 ·2003-10-00 ·Pages 11016-26

Kubota K, Tsuda S, Tamai A, Meshi T

Abstract

Posttranscriptional gene silencing (PTGS), a homology-dependent RNA degradation system, has a role in defending against virus infection in plants, but plant viruses encode a suppressor to combat PTGS. Using transgenic tobacco in which the expression of green fluorescent protein (GFP) is posttranscriptionally silenced, we investigated a tomato mosaic virus (ToMV)-encoded PTGS suppressor. Infection with wild-type ToMV (L strain) interrupted GFP silencing in tobacco, coincident with visible symptoms, whereas some attenuated strains of ToMV (L(11) and L(11)A strains) failed to suppress GFP silencing. Analyses of recombinant viruses containing the L and L(11)A strains revealed that a single base change in the replicase gene, which causes an amino acid substitution, is responsible for the symptomless and suppressor-defective phenotypes of the attenuated strains. An agroinfiltration assay indicated that the 130K replication protein acts as a PTGS suppressor. Small interfering RNAs (siRNAs) of 21 to 25 nucleotides accumulated during ToMV infection, suggesting that the major target of the ToMV-encoded suppressor is downstream from the production of siRNAs in the PTGS pathway. Analysis with GFP-tagged recombinant viruses revealed that the suppressor inhibits the establishment of the ToMV-targeted PTGS system in the inoculated leaves but does not detectably suppress the activity of the preexisting, sequence-specific PTGS machinery there. Taken together, these results indicate that it is likely that the ToMV-encoded suppressor, the 130K replication protein, blocks the utilization of silencing-associated small RNAs, so that a homology-dependent RNA degradation machinery is not newly formed.

MeSH Terms
Green Fluorescent Proteins Luminescent Proteins/genetics Lycopersicon esculentum/virology RNA Interference RNA, Small Interfering/biosynthesis RNA, Viral/biosynthesis RNA-Dependent RNA Polymerase/physiology Tobamovirus/genetics,physiology Viral Proteins/physiology Virus Replication
Chemicals
Luminescent Proteins RNA, Small Interfering RNA, Viral Viral Proteins Green Fluorescent Proteins RNA-Dependent RNA Polymerase
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Kubota Kenji
Department of Botany, Graduate School of Science, Kyoto University, Kyoto 606-8502, Japan.
Tsuda Shinya
Tamai Atsushi
Meshi Tetsuo
References (40)
40 references, click to expand
  1. RNA silencing: small RNAs as ubiquitous regulators of gene expression.
    Curr Opin Plant Biol. 2002 Oct;5(5):444-51 PMID: 12183184
  2. In vitro mutagenesis of the putative replicase genes of tobacco mosaic virus.
    Nucleic Acids Res. 1986 Nov 11;14(21):8291-305 PMID: 3786131
  3. Gene silencing as an adaptive defence against viruses.
    Nature. 2001 Jun 14;411(6839):834-42 PMID: 11459066
  4. The coat protein of turnip crinkle virus suppresses posttranscriptional gene silencing at an early initiation step.
    J Virol. 2003 Jan;77(1):511-22 PMID: 12477856
  5. A counterdefensive strategy of plant viruses: suppression of posttranscriptional gene silencing.
    Cell. 1998 Nov 13;95(4):461-70 PMID: 9827799
  6. Unique nature of an attenuated strain of tobacco mosaic virus: autoregulation.
    Microbiol Immunol. 1984;28(5):589-99 PMID: 6472136
  7. On the origin of dark green tissue in tobacco leaves infected with tobacco mosaic virus.
    Virology. 1970 Feb;40(2):344-56 PMID: 5440442
  8. A similarity between viral defense and gene silencing in plants.
    Science. 1997 Jun 6;276(5318):1558-60 PMID: 18610513
  9. A viral movement protein prevents spread of the gene silencing signal in Nicotiana benthamiana.
    Cell. 2000 Sep 29;103(1):157-67 PMID: 11051555
  10. The helicase domain of the TMV replicase proteins induces the N-mediated defence response in tobacco.
    Plant J. 1999 Apr;18(1):67-75 PMID: 10341444
  11. A biochemical framework for RNA silencing in plants.
    Genes Dev. 2003 Jan 1;17(1):49-63 PMID: 12514099
  12. Low temperature inhibits RNA silencing-mediated defence by the control of siRNA generation.
    EMBO J. 2003 Feb 3;22(3):633-40 PMID: 12554663
  13. Specialized binary vector for plant transformation: expression of the Arabidopsis thaliana AHAS gene in Nicotiana tabacum.
    Nucleic Acids Res. 1988 Nov 25;16(22):10765-82 PMID: 3060849
  14. A viral suppressor of gene silencing in plants.
    Proc Natl Acad Sci U S A. 1998 Oct 27;95(22):13079-84 PMID: 9789044
  15. A viral protein suppresses RNA silencing and binds silencing-generated, 21- to 25-nucleotide double-stranded RNAs.
    EMBO J. 2002 Jun 17;21(12):3070-80 PMID: 12065420
  16. Virus-encoded suppressor of posttranscriptional gene silencing targets a maintenance step in the silencing pathway.
    Proc Natl Acad Sci U S A. 2000 Nov 21;97(24):13401-6 PMID: 11078509
  17. P1/HC-Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA unction.
    Dev Cell. 2003 Feb;4(2):205-17 PMID: 12586064
  18. Nucleotide sequence of the tobacco mosaic virus (tomato strain) genome and comparison with the common strain genome.
    J Biochem. 1984 Dec;96(6):1915-23 PMID: 6549393
  19. Post-transcriptional gene silencing in plants.
    J Cell Sci. 2001 Sep;114(Pt 17):3083-91 PMID: 11590235
  20. Tobamoviral movement protein transiently expressed in a single epidermal cell functions beyond multiple plasmodesmata and spreads multicellularly in an infection-coupled manner.
    Mol Plant Microbe Interact. 2001 Feb;14(2):126-34 PMID: 11204775
  21. RNA silencing and the mobile silencing signal.
    Plant Cell. 2002;14 Suppl:S289-301 PMID: 12045284
  22. Molecular basis of plant viral virulence; the complete nucleotide sequence of an attenuated strain of tobacco mosaic virus.
    Nucleic Acids Res. 1985 Aug 12;13(15):5585-90 PMID: 3839921
  23. Cell-to-cell movement of Potato virus X: the role of p12 and p8 encoded by the second and third open reading frames of the triple gene block.
    Mol Plant Microbe Interact. 2001 Oct;14(10):1158-67 PMID: 11605955
  24. Suppression of gene silencing: a general strategy used by diverse DNA and RNA viruses of plants.
    Proc Natl Acad Sci U S A. 1999 Nov 23;96(24):14147-52 PMID: 10570213
  25. Plant viral synergism: the potyviral genome encodes a broad-range pathogenicity enhancer that transactivates replication of heterologous viruses.
    Plant Cell. 1997 Jun;9(6):859-68 PMID: 9212462
  26. Arabidopsis SGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance.
    Cell. 2000 May 26;101(5):533-42 PMID: 10850495
  27. RNA silencing as a plant immune system against viruses.
    Trends Genet. 2001 Aug;17(8):449-59 PMID: 11485817
  28. RNA viruses as inducers, suppressors and targets of post-transcriptional gene silencing.
    Plant Mol Biol. 2000 Jun;43(2-3):295-306 PMID: 10999412
  29. An RNA-dependent RNA polymerase gene in Arabidopsis is required for posttranscriptional gene silencing mediated by a transgene but not by a virus.
    Cell. 2000 May 26;101(5):543-53 PMID: 10850496
  30. HC-Pro suppression of transgene silencing eliminates the small RNAs but not transgene methylation or the mobile signal.
    Plant Cell. 2001 Mar;13(3):571-83 PMID: 11251097
  31. In vitro transcription of infectious RNAs from full-length cDNAs of tobacco mosaic virus.
    Proc Natl Acad Sci U S A. 1986 Jul;83(14):5043-7 PMID: 16593727
  32. Two classes of short interfering RNA in RNA silencing.
    EMBO J. 2002 Sep 2;21(17):4671-9 PMID: 12198169
  33. A species of small antisense RNA in posttranscriptional gene silencing in plants.
    Science. 1999 Oct 29;286(5441):950-2 PMID: 10542148
  34. A viral protein inhibits the long range signaling activity of the gene silencing signal.
    EMBO J. 2002 Feb 1;21(3):398-407 PMID: 11823432
  35. Jellyfish green fluorescent protein as a reporter for virus infections.
    Plant J. 1995 Jun;7(6):1045-53 PMID: 7599646
  36. Ancient pathways programmed by small RNAs.
    Science. 2002 May 17;296(5571):1265-9 PMID: 12016303
  37. Subcellular localization of host and viral proteins associated with tobamovirus RNA replication.
    EMBO J. 2003 Jan 15;22(2):344-53 PMID: 12514140
  38. RNA silencing: the genome's immune system.
    Science. 2002 May 17;296(5571):1263-5 PMID: 12016302
  39. Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana.
    EMBO J. 1998 Nov 16;17(22):6739-46 PMID: 9822616
  40. Gene silencing without DNA. rna-mediated cross-protection between viruses
    Plant Cell. 1999 Jul;11(7):1207-16 PMID: 10402423
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
DOI
10.1128/jvi.77.20.11016-11026.2003
Published
2003-10-00
Pages
11016-26
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC224966
Subset
IM
External Links
PubMed source DOI: 10.1128/jvi.77.20.11016-11026.2003 PMC Full Text View journal details
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