1887

Abstract

(TYLCV) is a DNA virus belonging to the genus . TYLCV replicates using double-stranded DNA intermediates that can become the target of plant transcriptional gene silencing (TGS). Here, we show that the V2 protein of TYLCV can suppress TGS of a transcriptionally silenced green fluorescent protein (GFP) transgene in line 16-TGS. Through bisulfite sequencing and chop-PCR, we demonstrated that the TYLCV V2 can reverse GFP transgene silencing by reducing the methylation levels in the 35S promoter sequence. Both and loci in were previously reported to be strongly methylated, and we show that the methylation status of both loci was significantly reduced in TYLCV V2 transgenic plants. We conclude that TYLCV can efficiently suppress TGS when it infects plants, and its V2 protein is responsible for the TGS suppression activity.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.055798-0
2014-01-01
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/jgv/95/1/225.html?itemId=/content/journal/jgv/10.1099/vir.0.055798-0&mimeType=html&fmt=ahah

References

  1. Amin I., Patil B. L., Briddon R. W., Mansoor S., Fauquet C. M. 2011; Comparison of phenotypes produced in response to transient expression of genes encoded by four distinct begomoviruses in Nicotiana benthamiana and their correlation with the levels of developmental miRNAs. Virol J 8:238 [View Article][PubMed]
    [Google Scholar]
  2. Bird A. 2002; DNA methylation patterns and epigenetic memory. Genes Dev 16:6–21 [View Article][PubMed]
    [Google Scholar]
  3. Bisaro D. M. 2006; Silencing suppression by geminivirus proteins. Virology 344:158–168 [View Article][PubMed]
    [Google Scholar]
  4. Buchmann R. C., Asad S., Wolf J. N., Mohannath G., Bisaro D. M. 2009; Geminivirus AL2 and L2 proteins suppress transcriptional gene silencing and cause genome-wide reductions in cytosine methylation. J Virol 83:5005–5013 [View Article][PubMed]
    [Google Scholar]
  5. Cao X., Jacobsen S. E. 2002a; Locus-specific control of asymmetric and CpNpG methylation by the DRM and CMT3 methyltransferase genes. Proc Natl Acad Sci U S A 99:Suppl 416491–16498 [View Article][PubMed]
    [Google Scholar]
  6. Cao X., Jacobsen S. E. 2002b; Role of the arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing. Curr Biol 12:1138–1144 [View Article][PubMed]
    [Google Scholar]
  7. Clough S. J., Bent A. F. 1998; Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. . Plant J 16:735–743 [View Article][PubMed]
    [Google Scholar]
  8. Cruz S. S., Roberts A. G., Prior D. A. M., Chapman S., Oparka K. J. 1998; Cell-to-cell and phloem-mediated transport of potato virus X. The role of virions. Plant Cell 10:495–510[PubMed] [CrossRef]
    [Google Scholar]
  9. Cui X., Li G., Wang D., Hu D., Zhou X. 2005; A Begomovirus DNAbeta-encoded protein binds DNA, functions as a suppressor of RNA silencing, and targets the cell nucleus. J Virol 79:10764–10775 [View Article][PubMed]
    [Google Scholar]
  10. Dry I. B., Rigden J. E., Krake L. R., Mullineaux P. M., Rezaian M. A. 1993; Nucleotide sequence and genome organization of tomato leaf curl geminivirus. J Gen Virol 74:147–151 [View Article][PubMed]
    [Google Scholar]
  11. Fauquet C. M., Briddon R. W., Brown J. K., Moriones E., Stanley J., Zerbini M., Zhou X. 2008; Geminivirus strain demarcation and nomenclature. Arch Virol 153:783–821 [View Article][PubMed]
    [Google Scholar]
  12. Glick E., Zrachya A., Levy Y., Mett A., Gidoni D., Belausov E., Citovsky V., Gafni Y. 2008; Interaction with host SGS3 is required for suppression of RNA silencing by tomato yellow leaf curl virus V2 protein. Proc Natl Acad Sci U S A 105:157–161 [View Article][PubMed]
    [Google Scholar]
  13. Goll M. G., Bestor T. H. 2005; Eukaryotic cytosine methyltransferases. Annu Rev Biochem 74:481–514 [View Article][PubMed]
    [Google Scholar]
  14. Hanley-Bowdoin L., Settlage S. B., Robertson D. 2004; Reprogramming plant gene expression: a prerequisite to geminivirus DNA replication. Mol Plant Pathol 5:149–156 [View Article][PubMed]
    [Google Scholar]
  15. Johnson L. M., Law J. A., Khattar A., Henderson I. R., Jacobsen S. E. 2008; SRA-domain proteins required for DRM2-mediated de novo DNA methylation. PLoS Genet 4:e1000280 [View Article][PubMed]
    [Google Scholar]
  16. Koornneef M., Alonso-Blanco C., Peeters A. J. M., Soppe W. 1998; Genetic control of flowering time in Arabidopsis. Annu Rev Plant Physiol Plant Mol Biol 49:345–370 [View Article][PubMed]
    [Google Scholar]
  17. Lu R., Malcuit I., Moffett P., Ruiz M. T., Peart J., Wu A.-J., Rathjen J. P., Bendahmane A., Day L., Baulcombe D. C. 2003; High throughput virus-induced gene silencing implicates heat shock protein 90 in plant disease resistance. EMBO J 22:5690–5699 [View Article][PubMed]
    [Google Scholar]
  18. Mishiba K., Nishihara M., Nakatsuka T., Abe Y., Hirano H., Yokoi T., Kikuchi A., Yamamura S. 2005; Consistent transcriptional silencing of 35S-driven transgenes in gentian. Plant J 44:541–556 [View Article][PubMed]
    [Google Scholar]
  19. Navot N., Pichersky E., Zeidan M., Zamir D., Czosnek H. 1991; Tomato yellow leaf curl virus: a whitefly-transmitted geminivirus with a single genomic component. Virology 185:151–161 [View Article][PubMed]
    [Google Scholar]
  20. Padidam M., Beachy R. N., Fauquet C. M. 1996; The role of AV2 (“precoat”) and coat protein in viral replication and movement in tomato leaf curl geminivirus. Virology 224:390–404 [View Article][PubMed]
    [Google Scholar]
  21. Pilartz M., Jeske H. 1992; Abutilon mosaic geminivirus double-stranded DNA is packed into minichromosomes. Virology 189:800–802 [View Article][PubMed]
    [Google Scholar]
  22. Pilartz M., Jeske H. 2003; Mapping of abutilon mosaic geminivirus minichromosomes. J Virol 77:10808–10818 [View Article][PubMed]
    [Google Scholar]
  23. Qian W., Miki D., Zhang H., Liu Y., Zhang X., Tang K., Kan Y., La H., Li X. other authors 2012; A histone acetyltransferase regulates active DNA demethylation in Arabidopsis. . Science 336:1445–1448 [View Article][PubMed]
    [Google Scholar]
  24. Raja P., Sanville B. C., Buchmann R. C., Bisaro D. M. 2008; Viral genome methylation as an epigenetic defense against geminiviruses. J Virol 82:8997–9007 [View Article][PubMed]
    [Google Scholar]
  25. Raja P., Wolf J. N., Bisaro D. M. 2010; RNA silencing directed against geminiviruses: post-transcriptional and epigenetic components. Biochim Biophys Acta 1799:337–351 [View Article][PubMed]
    [Google Scholar]
  26. Roberts A. G., Cruz S. S., Roberts I. M., Prior D. A. M., Turgeon R., Oparka K. J. 1997; Phloem unloading in sink leaves of Nicotiana benthamíana: comparison of a fluorescent solute with a fluorescent virus. Plant Cell 9:1381–1396[PubMed] [CrossRef]
    [Google Scholar]
  27. Rodríguez-Negrete E. A., Carrillo-Tripp J., Rivera-Bustamante R. F. 2009; RNA silencing against geminivirus: complementary action of posttranscriptional gene silencing and transcriptional gene silencing in host recovery. J Virol 83:1332–1340 [View Article][PubMed]
    [Google Scholar]
  28. Rodríguez-Negrete E. A., Lozano-Durán R., Piedra-Aguilera A., Cruzado L., Bejarano E. R., Castillo A. G. 2013; Geminivirus Rep protein interferes with the plant DNA methylation machinery and suppresses transcriptional gene silencing. New Phytol 199:464–475 [View Article][PubMed]
    [Google Scholar]
  29. Rojas M. R., Hagen C., Lucas W. J., Gilbertson R. L. 2005; Exploiting chinks in the plant’s armor: evolution and emergence of geminiviruses. Annu Rev Phytopathol 43:361–394 [View Article][PubMed]
    [Google Scholar]
  30. Yang X., Xie Y., Raja P., Li S., Wolf J. N., Shen Q., Bisaro D. M., Zhou X. 2011; Suppression of methylation-mediated transcriptional gene silencing by βC1-SAHH protein interaction during geminivirus-betasatellite infection. PLoS Pathog 7:e1002329 [View Article][PubMed]
    [Google Scholar]
  31. Zhang X., Garreton V., Chua N. H. 2005; The AIP2 E3 ligase acts as a novel negative regulator of ABA signaling by promoting ABI3 degradation. Genes Dev 19:1532–1543 [View Article][PubMed]
    [Google Scholar]
  32. Zhang X., Yazaki J., Sundaresan A., Cokus S., Chan S. W.-L., Chen H., Henderson I. R., Shinn P., Pellegrini M. other authors 2006; Genome-wide high-resolution mapping and functional analysis of DNA methylation in arabidopsis. Cell 126:1189–1201 [View Article][PubMed]
    [Google Scholar]
  33. Zhang H., Gong H., Zhou X. 2009; Molecular characterization and pathogenicity of tomato yellow leaf curl virus in China. Virus Genes 39:249–255 [View Article][PubMed]
    [Google Scholar]
  34. Zhang Z., Chen H., Huang X., Xia R., Zhao Q., Lai J., Teng K., Li Y., Liang L. other authors 2011; BSCTV C2 attenuates the degradation of SAMDC1 to suppress DNA methylation-mediated gene silencing in Arabidopsis. Plant Cell 23:273–288 [View Article][PubMed]
    [Google Scholar]
  35. Zhang J., Dong J., Xu Y., Wu J. 2012; V2 protein encoded by Tomato yellow leaf curl China virus is an RNA silencing suppressor. Virus Res 163:51–58 [View Article][PubMed]
    [Google Scholar]
  36. Zhou X. 2013; Advances in understanding begomovirus satellites. Annu Rev Phytopathol 51:357–381 [View Article][PubMed]
    [Google Scholar]
  37. Zrachya A., Glick E., Levy Y., Arazi T., Citovsky V., Gafni Y. 2007; Suppressor of RNA silencing encoded by Tomato yellow leaf curl virus-Israel. Virology 358:159–165 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.055798-0
Loading
/content/journal/jgv/10.1099/vir.0.055798-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error