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Suppressor of RNA silencing encoded by the monopartite tomato leaf curl Java begomovirus

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We previously isolated the monopartite begomovirus tomato leaf curl Java virus (ToLCJAV) and satellite DNAβ02 from the same naturally infected tomato source in Indonesia. ToLCJAV induced mild leaf curl symptoms in Nicotiana benthamiana plants; DNAβ02 encoded the βC1 gene and produced severe leaf curl symptoms when co-inoculated with ToLCJAV in N. benthamiana. However, DNAβ02mβC1, which contains a frame shift mutation, did not induce severe symptoms in N. benthamiana when co-inoculated with ToLCJAV. Expression of the βC1 gene in N. benthamiana using a potato virus X (PVX) vector induced virus-like symptoms in the absence of ToLCJAV infection. When βC1 and green fluorescent protein (GFP) genes were co-expressed in the GFP-expressing N. benthamiana line 16c from a PVX vector, βC1 was able to suppress posttranscriptional gene silencing (PTGS) induced by GFP and eliminated the short interfering RNA (siRNA) associated with GFP expression, with a correlated increase in GFP mRNA accumulation. When C2 or C4 genes of ToLCJAV and the GFP gene were co-expressed in the GFP-expressing N. benthamiana line 16c, C2 showed a weak suppressor activity and C4 was unable to suppress PTGS induced by GFP, and siRNA associated with GFP was detected. The results of the sub-cellular localization of ToLCJAV-βC1 in the epidermal cells of N. benthamiana and onion tissues showed that this protein is accumulated towards the periphery of the cell.

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References

  • DC Baulcombe SN Chapman S Santa Cruz (1995) ArticleTitleJellyfish green fluorescent protein as a reporter for virus infections Plant J 7 1045–1053 Occurrence Handle7599646 Occurrence Handle10.1046/j.1365-313X.1995.07061045.x Occurrence Handle1:CAS:528:DyaK2MXnsF2ltL4%3D

    Article  PubMed  CAS  Google Scholar 

  • DM Bisaro (2006) ArticleTitleSilencing suppression by geminivirus proteins Virology 344 158–168 Occurrence Handle16364747 Occurrence Handle10.1016/j.virol.2005.09.041 Occurrence Handle1:CAS:528:DC%2BD2MXhtlCqtb3M

    Article  PubMed  CAS  Google Scholar 

  • R Briddon S Bull I Amin A Idris S Mansoor I Bedford P Dhawan N Rishi S Siwatch A Abdel-Salam J Brown Y Zafar P Markham (2003) ArticleTitleDiversity of DNAβ, a satellite molecule associated with some monopartite begomoviruses Virology 312 106–121 Occurrence Handle12890625 Occurrence Handle10.1016/S0042-6822(03)00200-9 Occurrence Handle1:CAS:528:DC%2BD3sXlvVKjt78%3D

    Article  PubMed  CAS  Google Scholar 

  • R Briddon S Mansoor ID Bedford MS Pinner K Saunders J Stanley Y Zafar KA Malik PG Markham (2001) ArticleTitleIdentification of DNA components required for induction of cotton leaf curl disease Virology 285 234–243 Occurrence Handle11437658 Occurrence Handle10.1006/viro.2001.0949 Occurrence Handle1:CAS:528:DC%2BD3MXkvVOrs7s%3D

    Article  PubMed  CAS  Google Scholar 

  • G Brigneti O Voinnet WX Li LH Ji SW Ding DC Baulcombe (1998) ArticleTitleViral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana EMBO J 17 6739–6746 Occurrence Handle9822616 Occurrence Handle10.1093/emboj/17.22.6739 Occurrence Handle1:CAS:528:DyaK1cXnvF2jtLw%3D

    Article  PubMed  CAS  Google Scholar 

  • EJ Chapman AI Prokhnevsky K Gopinath VV Dolja JC Carrington (2004) ArticleTitleViral RNA silencing suppressors inhibit the microRNA pathway at an intermediate step Genes Dev 18 1179–1186 Occurrence Handle15131083 Occurrence Handle10.1101/gad.1201204 Occurrence Handle1:CAS:528:DC%2BD2cXktlCqs7o%3D

    Article  PubMed  CAS  Google Scholar 

  • PP Chellappan R Vanitharani CM Fauquet (2005) ArticleTitleMicroRNA-binding viral protein interferes with Arabidopsis development Proc Natl Acad Sci USA 102 10381–10386 Occurrence Handle16006510 Occurrence Handle10.1073/pnas.0504439102 Occurrence Handle1:CAS:528:DC%2BD2MXmvVeksLg%3D

    Article  PubMed  CAS  Google Scholar 

  • H Chen RS Nelson JL Sherwood (1994) ArticleTitleEnhanced recovery of transformants of Agrobacterium tumefaciens after freeze-thaw transformation and drug selection Biotechniques 16 664–670 Occurrence Handle8024787 Occurrence Handle1:CAS:528:DyaK2cXltVSksbc%3D

    PubMed  CAS  Google Scholar 

  • J Chen WX Li D Xie JR Peng SW Ding (2004) ArticleTitleViral virulence protein suppresses RNA silencing-mediated defense but upregulates the role of microRNA in host gene expression Plant Cell 16 1302–1313 Occurrence Handle15100397 Occurrence Handle10.1105/tpc.018986 Occurrence Handle1:CAS:528:DC%2BD2cXktlOqtr4%3D

    Article  PubMed  CAS  Google Scholar 

  • CW Collmer SH Howell (1992) ArticleTitleRole of satellite RNA in expression of symptoms caused by plant viruses Annu Rev Phytopathol 30 419–442 Occurrence Handle10.1146/annurev.py.30.090192.002223 Occurrence Handle1:CAS:528:DyaK3sXhvFWnsw%3D%3D

    Article  CAS  Google Scholar 

  • X Cui G Li D Wang D Hu X Zhou (2005) ArticleTitleA begomovirus DNAβ-encoded protein binds DNA, functions as a suppressor of RNA silencing, and targets the cell nucleus J Virol 79 10764–10775 Occurrence Handle16051868 Occurrence Handle10.1128/JVI.79.16.10764-10775.2005 Occurrence Handle1:CAS:528:DC%2BD2MXntFCqsLs%3D

    Article  PubMed  CAS  Google Scholar 

  • X Cui X Tao Y Xie CM Fauquet X Zhou (2004) ArticleTitleA DNAβ associated with Tomato yellow leaf curl China virus is required for symptom induction J Virol 78 13966–13974 Occurrence Handle15564504 Occurrence Handle10.1128/JVI.78.24.13966-13974.2004 Occurrence Handle1:CAS:528:DC%2BD2cXhtFSisL3N

    Article  PubMed  CAS  Google Scholar 

  • X Dong R van Wezel J Stanley Y Hong (2003) ArticleTitleFunctional characterization of the nuclear localization signal for a suppressor of posttranscriptional gene silencing J Virol 77 7026–7033 Occurrence Handle12768021 Occurrence Handle10.1128/JVI.77.12.7026-7033.2003 Occurrence Handle1:CAS:528:DC%2BD3sXksFGhs7Y%3D

    Article  PubMed  CAS  Google Scholar 

  • P Dunoyer C-H Lecellier EA Parizotto C Himber O Voinnet (2004) ArticleTitleProbing the microRNA and small Interfering RNA pathways with virus-encoded suppressors of RNA silencing Plant Cell 16 1235–1250 Occurrence Handle15084715 Occurrence Handle10.1105/tpc.020719 Occurrence Handle1:CAS:528:DC%2BD2cXktlOqsbs%3D

    Article  PubMed  CAS  Google Scholar 

  • P Gopal PP Kumar B Sinilal J Jose A Yadunandam R Usha (2007) ArticleTitleDifferential roles of C4 and βC1 in mediating suppression of post-transcriptional gene silencing: Evidence for transactivation by the C2 of Bhendi yellow vein mosaic virus, a monopartite begomovirus Virus Res 123 9–18 Occurrence Handle16949698 Occurrence Handle10.1016/j.virusres.2006.07.014 Occurrence Handle1:CAS:528:DC%2BD28Xht1eku7bN

    Article  PubMed  CAS  Google Scholar 

  • K Goto A Kanazawa M Kusaba C Masuta (2003) ArticleTitleA simple and rapid method to detect plant siRNA using nonradioactive probes Plant Mol Biol Rep 21 51–58 Occurrence Handle1:CAS:528:DC%2BD3sXlt1Khurk%3D

    CAS  Google Scholar 

  • A Hamilton DC Baulcombe (1999) ArticleTitleA species of small antisense RNA in posttranscriptional gene silencing in plants Science 286 950–952 Occurrence Handle10542148 Occurrence Handle10.1126/science.286.5441.950 Occurrence Handle1:CAS:528:DyaK1MXntFaktbY%3D

    Article  PubMed  CAS  Google Scholar 

  • S Hammond E Bernstein D Beach G Hannon (2000) ArticleTitleAn RNA-directed nuclease mediates PTGS in Drosophila cells Nature 404 293–296 Occurrence Handle10749213 Occurrence Handle10.1038/35005107 Occurrence Handle1:CAS:528:DC%2BD3cXit1agtrw%3D

    Article  PubMed  CAS  Google Scholar 

  • J Jose R Usha (2003) ArticleTitleBhendi yellow vein mosaic disease in India is caused by association of a DNAβ satellite with a begomovirus Virology 305 310–315 Occurrence Handle12573576 Occurrence Handle10.1006/viro.2002.1768 Occurrence Handle1:CAS:528:DC%2BD3sXptlOrsQ%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • KD Kasschau JC Carrington (1998) ArticleTitleA counterdefensive strategy of plant viruses: suppression of posttranscriptional gene silencing Cell 95 461–470 Occurrence Handle9827799 Occurrence Handle10.1016/S0092-8674(00)81614-1 Occurrence Handle1:CAS:528:DyaK1cXns1ektro%3D

    Article  PubMed  CAS  Google Scholar 

  • T Kon LM Dolores NB Bajet S Hase H Takahashi M Ikegami (2003) ArticleTitleMolecular characterization of a strain of Squash leaf curl China virus from the Phillippines J Phytopathol 151 535–539 Occurrence Handle10.1046/j.1439-0434.2003.00764.x Occurrence Handle1:CAS:528:DC%2BD3sXhtVSltrjO

    Article  CAS  Google Scholar 

  • T Kon LM Dolores A Murayama NB Bajet S Hase H Takahashi M Ikegami (2002) ArticleTitleGenome organization of an infectious clone of Tomato leaf curl virus (Philippines), a new monopartite Begomovirus J Phytopathol 150 587–591 Occurrence Handle10.1046/j.1439-0434.2002.00817.x Occurrence Handle1:CAS:528:DC%2BD3sXovVShug%3D%3D

    Article  CAS  Google Scholar 

  • T Kon SH Hidayat S Hase H Takahashi M Ikegami (2006) ArticleTitleThe natural occurrence of two distinct begomoviruses associated with DNAβ and a recombinant DNA in a tomato plant from Indonesia Phytopathology 96 517–525 Occurrence Handle10.1094/PHYTO-96-0517 Occurrence Handle1:CAS:528:DC%2BD28Xksl2msLc%3D

    Article  CAS  Google Scholar 

  • Kon T, Kuwabara K, Hidayat SH, Ikegami M (2007) A begomovirus associated with yellow vein disease in Indonasia: evidence for natural recombination between tomato leaf curl Java virus and Ageratum yellow vein virus-[Java]. Arch Virol (DOI: 10.1007/s00705-006-0928-3)

  • P Kumar R Usha A Zrachya Y Levy H Spanov Y Gafni (2006) ArticleTitleProtein–protien interactions and nuclear trafficking of coat protein and βC1 associated with Bhendi yellow vein mosaic disease Virus Res 122 127–136 Occurrence Handle10.1016/j.virusres.2006.07.007 Occurrence Handle1:CAS:528:DC%2BD28XhtFeqtL%2FP

    Article  CAS  Google Scholar 

  • AP Lucy HS Guo WX Li SW Ding (2000) ArticleTitleSuppression of post-transcriptional gene silencing by a plant viral protein localized in the nucleus EMBO J 19 1672–1680 Occurrence Handle10747034 Occurrence Handle10.1093/emboj/19.7.1672 Occurrence Handle1:CAS:528:DC%2BD3cXislymtL0%3D

    Article  PubMed  CAS  Google Scholar 

  • G Moissiard O Voinnet (2004) ArticleTitleViral suppression of RNA silencing in plants Mol Plant Pathol 5 71–82 Occurrence Handle10.1111/j.1364-3703.2004.00207.x Occurrence Handle1:CAS:528:DC%2BD2cXitVKgsb4%3D

    Article  CAS  Google Scholar 

  • Y Niwa T Hirano K Yoshimoto M Shimizu H Kobayashi (1999) ArticleTitleNon-invasive quantitative detection and applications of nontoxic-, S65T-type green fluorescent protein in living plants Plant J 18 455–463 Occurrence Handle10406127 Occurrence Handle10.1046/j.1365-313X.1999.00464.x Occurrence Handle1:CAS:528:DyaK1MXktlKgtL8%3D

    Article  PubMed  CAS  Google Scholar 

  • BM Roth GJ Pruss VB Vance (2004) ArticleTitlePlant viral suppressors of RNA silencing Virus Res 102 97–108 Occurrence Handle15068885 Occurrence Handle10.1016/j.virusres.2004.01.020 Occurrence Handle1:CAS:528:DC%2BD2cXivVKmtLw%3D

    Article  PubMed  CAS  Google Scholar 

  • K Saunders ID Bedford RW Briddon PG Markham SM Wong J Stanley (2000) ArticleTitleA novel virus complex causes Ageratum yellow vein disease Proc Natl Acad Sci USA 97 6890–6895 Occurrence Handle10841581 Occurrence Handle10.1073/pnas.97.12.6890 Occurrence Handle1:CAS:528:DC%2BD3cXktFahtrw%3D

    Article  PubMed  CAS  Google Scholar 

  • K Saunders ID Bedford T Yahara J Stanley (2003) ArticleTitleThe earliest recoded plant virus disease Nature 422 831 Occurrence Handle12712190 Occurrence Handle10.1038/422831a Occurrence Handle1:CAS:528:DC%2BD3sXjtFCit70%3D

    Article  PubMed  CAS  Google Scholar 

  • K Saunders A Norman S Gucciardo J Stanley (2004) ArticleTitleThe DNAβ satellite component associated with ageratum yellow vein disease encodes an essential pathogenicity protein (βC1) Virology 324 37–47 Occurrence Handle15183051 Occurrence Handle10.1016/j.virol.2004.03.018 Occurrence Handle1:CAS:528:DC%2BD2cXks1ersLs%3D

    Article  PubMed  CAS  Google Scholar 

  • LA Selth JW Randles MA Rezaian (2004) ArticleTitleHost responses to transient expression of individual genes encoded by Tomato leaf curl virus Mol Plant Microbe Interact 17 27–33 Occurrence Handle14714865 Occurrence Handle10.1094/MPMI.2004.17.1.27 Occurrence Handle1:CAS:528:DC%2BD2cXivVSltr8%3D

    Article  PubMed  CAS  Google Scholar 

  • Stanley J, Briddon RW, Brown JK, Fauquet CM, Harrison BD, Rybicki, Stinger DC (2005) Geminiviridae. In: Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA (eds) Virus taxonomy. VIIIth Report of the International Committee on Taxonomy of Viruses. Elsevier/Academic Press, London, 301–326

  • D Trinks R Rajeswaran PV Shivaprasad R Akbergenov EJ Oakeley K Veluthambi T Hohn MM Pooggin (2005) ArticleTitleSuppression of RNA silencing by a geminivirus nuclear protein, AC2, correlates with transactivation of host genes J Virol 79 2517–2527 Occurrence Handle15681452 Occurrence Handle10.1128/JVI.79.4.2517-2527.2005 Occurrence Handle1:CAS:528:DC%2BD2MXitleisr4%3D

    Article  PubMed  CAS  Google Scholar 

  • R van Wezel X Dong H Liu P Tien J Stanley Y Hong (2002) ArticleTitleMutation of three cysteine residues in Tomato yellow leaf curl virus-China C2 protein causes dysfunction in pathogenesis and posttranscriptional gene-silencing suppression Mol Plant Microbe Interact 15 203–208 Occurrence Handle11952122 Occurrence Handle10.1094/MPMI.2002.15.3.203 Occurrence Handle1:CAS:528:DC%2BD38XitF2gtLY%3D

    Article  PubMed  CAS  Google Scholar 

  • R van Wezel H Liu P Tien J Stanley Y Hong (2001) ArticleTitleGene C2 of the monopartite geminivirus tomato yellow leaf curl virus-China encodes a pathogenicity determinant that is localized in the nucleus Mol Plant Microbe Interact 14 1125–1128 Occurrence Handle11551077 Occurrence Handle10.1094/MPMI.2001.14.9.1125 Occurrence Handle1:CAS:528:DC%2BD3MXmvFGhs7o%3D

    Article  PubMed  CAS  Google Scholar 

  • R van Wezel H Liu Z Wu J Stanley Y Hong (2003) ArticleTitleContribution of the zinc finger to zinc and DNA binding by a suppressor of posttranscriptional gene silencing J Virol 77 696–700 Occurrence Handle12477872 Occurrence Handle10.1128/JVI.77.1.696-700.2003 Occurrence Handle1:CAS:528:DC%2BD3sXkt1Km

    Article  PubMed  CAS  Google Scholar 

  • R Vanitharani P Chellappan JS Pita CM Faququet (2004) ArticleTitleDifferential roles of AC2 and AC4 of cassava geminiviruses in mediating synergism and suppression of posttranscriptional gene silencing J Virol 78 9487–9498 Occurrence Handle15308741 Occurrence Handle10.1128/JVI.78.17.9487-9498.2004 Occurrence Handle1:CAS:528:DC%2BD2cXntVKhsLY%3D

    Article  PubMed  CAS  Google Scholar 

  • O Voinnet (2001) ArticleTitleRNA silencing as a plant immune system against viruses Trends Genet 17 449–459 Occurrence Handle11485817 Occurrence Handle10.1016/S0168-9525(01)02367-8 Occurrence Handle1:CAS:528:DC%2BD3MXlsFylu70%3D

    Article  PubMed  CAS  Google Scholar 

  • O Voinnet YM Pinto DC Baulcombe (1999) ArticleTitleSuppression of gene silencing: a general strategy used by diverse DNA and RNA viruses of plants Proc Natl Acad Sci USA 96 14147–14152 Occurrence Handle10570213 Occurrence Handle10.1073/pnas.96.24.14147 Occurrence Handle1:CAS:528:DyaK1MXns1yjs7o%3D

    Article  PubMed  CAS  Google Scholar 

  • H Wang KJ Buckley X Yang RC Buchmann DM Bisaro (2005) ArticleTitleAdenosine kinase inhibition and suppression of RNA silencing by geminivirus AL2 and L2 proteins J Virol 79 7410–7418 Occurrence Handle15919897 Occurrence Handle10.1128/JVI.79.12.7410-7418.2005 Occurrence Handle1:CAS:528:DC%2BD2MXkvFCnu7k%3D

    Article  PubMed  CAS  Google Scholar 

  • PM Waterhouse MB Wang T Lough (2001) ArticleTitleGene silencing as an adaptive defense against viruses Nature 411 834–842 Occurrence Handle11459066 Occurrence Handle10.1038/35081168 Occurrence Handle1:CAS:528:DC%2BD3MXksF2gu7Y%3D

    Article  PubMed  CAS  Google Scholar 

  • Z Xie LK Johansen AM Gustafson KD Kasschau AD Lellis D Zilberman SE Jacobsen JC Carrington (2004) ArticleTitleGenetic and functional diversification of small RNA pathways in plants PLoS Biol 2 E104 Occurrence Handle15024409 Occurrence Handle10.1371/journal.pbio.0020104

    Article  PubMed  Google Scholar 

  • PD Zamore T Tuschl PA Sharp DP Bartel (2000) ArticleTitleRNAi: dsRNA directs the ATP-dependent cleavage of mRNA at 21–23 nt intervals Cell 101 25–33 Occurrence Handle10778853 Occurrence Handle10.1016/S0092-8674(00)80620-0 Occurrence Handle1:CAS:528:DC%2BD3cXisVaitbo%3D

    Article  PubMed  CAS  Google Scholar 

  • X Zhou Y Xie X Tao Z Zhang Z Li CM Fauquet (2003) ArticleTitleCharacterization of DNAβ associated with begomoviruses in China and evidence for co-evolution with their cognate viral DNA-A J Gen Virol 84 237–247 Occurrence Handle12533720 Occurrence Handle10.1099/vir.0.18608-0 Occurrence Handle1:CAS:528:DC%2BD3sXksl2huw%3D%3D

    Article  PubMed  CAS  Google Scholar 

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Kon, T., Sharma, P. & Ikegami, M. Suppressor of RNA silencing encoded by the monopartite tomato leaf curl Java begomovirus. Arch Virol 152, 1273–1282 (2007). https://doi.org/10.1007/s00705-007-0957-6

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