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Post-transcriptional gene silencing in controlling viruses of the Tomato yellow leaf curl virus complex

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Summary.

Tomato yellow leaf curl disease (TYLCD) is caused by a group of geminiviruses that belong to the Tomato yellow leaf curl virus (TYLCV) complex and are transmitted by the whitefly (Bemisia tabaci Genn.). The disease causes great yield losses in many countries throughout the Mediterranean region and the Middle East. In this study, the efficacy of post-transcriptional gene silencing (PTGS) to control the disease caused by TYLCV complex was investigated. Non-coding conserved regions from the genome of TYLCV, Tomato yellow leaf curl virus – mild, tomato yellow leaf curl Sardinia virus, tomato yellow leaf curl Malaga virus, and tomato yellow leaf curl Sardinia virus – Spain [2] were selected and used to design a construct that can trigger broad resistance against different viruses that cause tomato yellow leaf curl disease. The silencing construct was cloned into an Agrobacterium-binary vector in sense and antisense orientation and used in transient assay to infiltrate tomato and Nicotiana benthamiana plants. A high level of resistance was obtained when plants were agro-infiltrated with an infectious clone of the Egyptian isolate of TYLCV (TYLCV-[EG]) or challenge inoculated with TYLCV, TYLCV-Mld, and TYLCSV-ES[2] using whitefly-mediated transmission 16–20 days post infiltration with the silencing construct. Results of the polymerase chain reaction showed that the resistance was effective against all three viruses. Furthermore, dot blot hybridization and PCR failed to detect viral DNA in symptomless, silenced plants. A positive correlation between resistance and the accumulation of TYLCV-specific siRNAs was observed in silenced plants. Together, these data provide compelling evidence that PTGS can be used to engineer geminivirus-resistant plants.

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References

  • GP Accotto J Navas-Castillo E Noris E Moriones D Louro (2000) ArticleTitleTyping of tomato yellow leaf curl viruses in Europe Eur J Plant Pathol 106 179–186 Occurrence Handle10.1023/A:1008736023293

    Article  Google Scholar 

  • GH Anfoka M Abhary MK Nakhla (2005) ArticleTitleMolecular identification of species of the Tomato yellow leaf curl virus complex in Jordan J Plant Pathol 87 61–66

    Google Scholar 

  • EY Antignus S Cohen (1994) ArticleTitleComplete nucleotide sequence of an infectious clone of a mild isolate of tomato yellow leaf curl virus (TYLCV) Phytopathology 84 707–712 Occurrence Handle1:CAS:528:DyaK2MXmt1Oisg%3D%3D

    CAS  Google Scholar 

  • S Asad WA Haris A Bashir Y Zafar KA Malik NN Malik CP Lichtenstein (2003) ArticleTitleTransgenic tobacco expressing geminiviral RNAs are resistant to the serious viral pathogen causing cotton leaf curl disease Arch Virol 148 2341–2352 Occurrence Handle14648290 Occurrence Handle1:CAS:528:DC%2BD3sXptleks7w%3D Occurrence Handle10.1007/s00705-003-0179-5

    Article  PubMed  CAS  Google Scholar 

  • DC Baulcombe (1996) ArticleTitleMechanisms of pathogen-derived resistance to viruses in transgenic plants Plant Cell 8 1833–1844 Occurrence Handle12239365 Occurrence Handle1:CAS:528:DyaK28Xmsl2muro%3D Occurrence Handle10.1105/tpc.8.10.1833

    Article  PubMed  CAS  Google Scholar 

  • DC Baulcombe (1999) ArticleTitleFast forward genetics based on virus-induced gene silencing Curr Opin Plant Biol 2 109–113 Occurrence Handle10322199 Occurrence Handle1:CAS:528:DyaK1MXivVGlsL8%3D Occurrence Handle10.1016/S1369-5266(99)80022-3

    Article  PubMed  CAS  Google Scholar 

  • M Bendahmane B Gronenborn (1997) ArticleTitleEngineering resistance against tomato yellow leaf curl virus (TYLCV) using antisense RNA Plant Mol Biol 33 351–357 Occurrence Handle9037152 Occurrence Handle1:CAS:528:DyaK2sXhsFaktLs%3D Occurrence Handle10.1023/A:1005715805000

    Article  PubMed  CAS  Google Scholar 

  • Briddon RW, Markham PG (1995) Family Geminiviridae. In: Murphy FA, Fauquet CM, Bishop DHL, Ghabrial SA, Jarvis AW, Martelli GP, Mayo MA, Summers MD (eds) Virus Taxonomy: Classification and Nomenclature of Viruses. Sixth Report of the International Committee on Taxonomy of Viruses. Springer, Wien, New York, pp 158–165

  • A Brunetti R Tavazza E Noris A Lucioli GP Accotto M Tavazza (2001) ArticleTitleTransgenically expressed T-Rep of tomato yellow leaf curl Sardinia virus acts as a trans-dominant-negative mutant, inhibiting viral transcription and replication J Virol 75 10573–10581 Occurrence Handle11602699 Occurrence Handle1:CAS:528:DC%2BD3MXnvVelsLw%3D Occurrence Handle10.1128/JVI.75.22.10573-10581.2001

    Article  PubMed  CAS  Google Scholar 

  • R Campos-Olivas JM Louis D Clerot B Gronenborn AM Gronenborn (2002) ArticleTitleThe structure of a replication initiator unites diverse aspects of nucleic acid metabolism PNAS 99 10310–10315 Occurrence Handle12130667 Occurrence Handle1:CAS:528:DC%2BD38Xmt1Citbk%3D Occurrence Handle10.1073/pnas.152342699

    Article  PubMed  CAS  Google Scholar 

  • P Chellappan R Vanitharani CM Fauquet (2004) ArticleTitlesiRNA accumulation correlates with host recovery in DNA virus infected hosts and gene silencing targets specific viral sequences J Virol 78 7465–7477 Occurrence Handle15220420 Occurrence Handle1:CAS:528:DC%2BD2cXlvFShtbY%3D Occurrence Handle10.1128/JVI.78.14.7465-7477.2004

    Article  PubMed  CAS  Google Scholar 

  • A Chicas G Macino (2001) ArticleTitleCharacteristics of post-transcriptional gene silencing EMBO Rep 2 992–996 Occurrence Handle11713190 Occurrence Handle1:CAS:528:DC%2BD3MXovFOnsLo%3D Occurrence Handle10.1093/embo-reports/kve231

    Article  PubMed  CAS  Google Scholar 

  • S Cohen Y Antignus (1994) ArticleTitleTomato yellow leaf curl virus, a whitefly-borne geminivirus of tomatoes Adv Dis Vector Res 10 259–288

    Google Scholar 

  • C Cogoni G Macino (1999) ArticleTitleGene silencing in Neurospora crassa requires a protein homologous to RNA-dependent RNA polymerase Nature 399 166–169 Occurrence Handle10335848 Occurrence Handle1:CAS:528:DyaK1MXjsVOhtb8%3D Occurrence Handle10.1038/20215

    Article  PubMed  CAS  Google Scholar 

  • H Czosnek H Laterrot (1997) ArticleTitleA worldwide survey of tomato yellow leaf curl viruses Arch Virol 142 1391–1406 Occurrence Handle9267451 Occurrence Handle1:CAS:528:DyaK2sXls1ymtrs%3D Occurrence Handle10.1007/s007050050168

    Article  PubMed  CAS  Google Scholar 

  • SM Elbashir W Lendeckel T Tuschl (2001) ArticleTitleRNA interference is mediated by 21- and 22-nucleotide RNAs Genes Dev 15 188–200 Occurrence Handle11157775 Occurrence Handle1:CAS:528:DC%2BD3MXhvVOjtbg%3D Occurrence Handle10.1101/gad.862301

    Article  PubMed  CAS  Google Scholar 

  • CM Fauquet DM Bisaro RW Briddon JK Brown BD Harrison EP Rybicki DC Stenger J Stanley (2003) ArticleTitleRevision of taxonomic criteria for species demarcation in the family Geminiviridae, and an updated list of begomovirus species Arch Virol 148 405–421 Occurrence Handle12557003 Occurrence Handle1:CAS:528:DC%2BD3sXntV2nsw%3D%3D Occurrence Handle10.1007/s00705-002-0957-5

    Article  PubMed  CAS  Google Scholar 

  • A Fire S Xu MK Montgomery SA Kostas SE Driver CC Mello (1998) ArticleTitlePotent and specific genetic interference by double stranded RNA in Caenorhabditis elegans Nature 391 806–811 Occurrence Handle9486653 Occurrence Handle1:CAS:528:DyaK1cXhtlCju74%3D Occurrence Handle10.1038/35888

    Article  PubMed  CAS  Google Scholar 

  • M Friedmann M Lapidot S Cohen M Pilowsky (1998) ArticleTitleA novel source of resistance to tomato yellow leaf curl virus exhibiting a symptomless reaction to viral infection J Am Soc Hortic Sci 123 1004–1007

    Google Scholar 

  • ER Gauthier SD Madison RN Michel (1997) ArticleTitleRapid RNA isolation without the use of commercial kits: application to small tissue samples Pflugers Arch – Eur J Physiol 433 644–668

    Google Scholar 

  • L Hanley-Bowdoin SB Settlage BM Orozco S Nagar D Robertson (1999) ArticleTitleGeminiviruses: models for plant DNA replication, transcription, and cell cycle regulation Crit Rev Plant Sci 18 71–106 Occurrence Handle1:CAS:528:DyaK1MXht12qtL8%3D Occurrence Handle10.1016/S0735-2689(99)00383-4

    Article  CAS  Google Scholar 

  • LK Johansen JC Carrington (2001) ArticleTitleSilencing on the spot. Induction and suppression of RNA silencing in the Agrobacterium-mediated transient expression system Plant Physiology 126 930–938 Occurrence Handle11457942 Occurrence Handle1:CAS:528:DC%2BD3MXlsVartLk%3D Occurrence Handle10.1104/pp.126.3.930

    Article  PubMed  CAS  Google Scholar 

  • A Kheyr-Pour M Bendahmane V Matzeit GP Accotto S Crespi B Gronenborn (1991) ArticleTitleTomato yellow leaf curl virus from Sardinia is a whitefly-transmitted monopartite geminivirus Nucleic Acids Res 19 6763–6769 Occurrence Handle1840676 Occurrence Handle1:CAS:528:DyaK3sXpsFensw%3D%3D

    PubMed  CAS  Google Scholar 

  • J Laufs W Traut F Heyraud V Matzeit SG Rogers J Schell B Gronenborn (1995) ArticleTitleIn vitro cleavage and joining at the viral origin of replication by the replication initiator protein of tomato yellow leaf curl virus Proc Natl Acad Sci USA 92 3879–3883 Occurrence Handle7732000 Occurrence Handle1:CAS:528:DyaK2MXlsVSksr0%3D Occurrence Handle10.1073/pnas.92.9.3879

    Article  PubMed  CAS  Google Scholar 

  • A Lucioli E Noris A Brunetti R Tavazza V Ruzza AG Castillo ER Bejarano GP Accotto M Tavazza (2003) ArticleTitleTomato yellow leaf curl Sardinia virus rep-derived resistance to homologous and heterologous geminiviruses occurs by different mechanisms and is overcome if virus-mediated transgene silencing is activated J Virol 77 6785–6798 Occurrence Handle12767999 Occurrence Handle1:CAS:528:DC%2BD3sXksFGhsrk%3D Occurrence Handle10.1128/JVI.77.12.6785-6798.2003

    Article  PubMed  CAS  Google Scholar 

  • A Luke J Randles M Rezaian (2004) ArticleTitleHost responses to transient expression of individual genes encoded by tomato leaf curl virus MPMI 17 IssueID1 27–33

    Google Scholar 

  • KM Makkouk (1978) ArticleTitleA study on tomato viruses in the Jordan Valley with special emphasis on tomato yellow leaf curl Plant Dis Rep 62 259–262

    Google Scholar 

  • MA Matzke AJM Matzke G Pruss VB Vance (2001) ArticleTitleRNA-based silencing strategies in plants Curr Opin Gene Devel 11 221–227 Occurrence Handle1:CAS:528:DC%2BD3MXis1aku7s%3D Occurrence Handle10.1016/S0959-437X(00)00183-0

    Article  CAS  Google Scholar 

  • F Meins SuffixJr (2000) ArticleTitleRNA degradation and models for post-transcriptional gene silencing Plant Mol Biol 43 261–273 Occurrence Handle10999409 Occurrence Handle1:CAS:528:DC%2BD3cXmsFyqu7o%3D Occurrence Handle10.1023/A:1006443731515

    Article  PubMed  CAS  Google Scholar 

  • F Monci S Sanchez-Campos J Navas-Castillo E Moriones (2002) ArticleTitleA natural recombination between the geminiviruses Tomato yellow leaf curl Sardinia virus and Tomato yellow leaf curl virus exhibits a novel pathogenic phenotype and is becoming prevalent in Spanish populations Virology 303 317–326 Occurrence Handle12490393 Occurrence Handle1:CAS:528:DC%2BD38XpsFyhurw%3D Occurrence Handle10.1006/viro.2002.1633

    Article  PubMed  CAS  Google Scholar 

  • E Moriones J Navas-Castillo (2000) ArticleTitleTomato yellow leaf curl virus, an emerging virus complex causing epidemics worldwide Virus Res 71 123–134 Occurrence Handle11137167 Occurrence Handle1:CAS:528:DC%2BD3MXptVSnuw%3D%3D Occurrence Handle10.1016/S0168-1702(00)00193-3

    Article  PubMed  CAS  Google Scholar 

  • C Napoli C Lemieux R Jorgensen (1990) ArticleTitleIntroduction of a chimeric chalcone synthase gene into petunia results in reversible co-suppression of homologous genes in trans Plant Cell 2 279–289 Occurrence Handle12354959 Occurrence Handle1:CAS:528:DyaK3cXkvFalu7c%3D Occurrence Handle10.1105/tpc.2.4.279

    Article  PubMed  CAS  Google Scholar 

  • J Navas-Castillo S Sanchez-Campos E Noris D Louro GP Accotto E Moriones (2000) ArticleTitleNatural recombination between Tomato yellow leaf curl virus-Is and Tomato leaf curl virus J Gen Virol 81 2797–2801 Occurrence Handle11038394 Occurrence Handle1:CAS:528:DC%2BD3cXnvFWnsr4%3D

    PubMed  CAS  Google Scholar 

  • E Noris E Hidalgo GP Accotto E Moriones (1994) ArticleTitleHigh similarity among the tomato yellow leaf curl virus from the west Mediterranean basin: The nucleotide sequence of an infectious clone from Spain Arch Virol 135 165–170 Occurrence Handle8198442 Occurrence Handle1:CAS:528:DyaK2MXnvFWl Occurrence Handle10.1007/BF01309774

    Article  PubMed  CAS  Google Scholar 

  • E Noris GP Accotto R Tavazza A Brunetti S Crespi M Tavazza (1996) ArticleTitleResistance to tomato yellow leaf curl geminivirus in Nicotiana benthamiana plants transformed with a truncated viral C1 gene Virology 224 130–138 Occurrence Handle8862407 Occurrence Handle1:CAS:528:DyaK28XmsVSkur8%3D Occurrence Handle10.1006/viro.1996.0514

    Article  PubMed  CAS  Google Scholar 

  • E Noris A Lucioli R Tavazza P Caciagli GP Accotto M Tavazza (2004) ArticleTitleTomato yellow leaf curl Sardinia virus can overcome transgene-mediated RNA silencing of two essential viral genes J Gen Virol 85 1745–1749 Occurrence Handle15166460 Occurrence Handle1:CAS:528:DC%2BD2cXltlGhtLg%3D Occurrence Handle10.1099/vir.0.79944-0

    Article  PubMed  CAS  Google Scholar 

  • JC Palauqui Elmayan JM Pollien H Vaucheret (1997) ArticleTitleSystemic acquired silencing: transgene-specific post-transcriptional silencing is transmitted by grafting from silenced stocks to non-silenced scions EMBO J 16 4738–4745 Occurrence Handle9303318 Occurrence Handle1:CAS:528:DyaK2sXlsVClsbk%3D Occurrence Handle10.1093/emboj/16.15.4738

    Article  PubMed  CAS  Google Scholar 

  • JL Potter MK Nakhla L Mejía DP Maxwell (2003) ArticleTitlePCR and DNA hybridization methods for specific detection of bean-infecting begomoviruses in the Americas and Caribbean Plant Dis 87 1205–1212 Occurrence Handle1:CAS:528:DC%2BD3sXotFCku7g%3D

    CAS  Google Scholar 

  • M Prins R Goldbach (1996) ArticleTitleRNA-mediated virus resistance in transgenic plants Arch Virol 141 2259–2276 Occurrence Handle9526535 Occurrence Handle1:CAS:528:DyaK2sXpt1KhtA%3D%3D Occurrence Handle10.1007/BF01718629

    Article  PubMed  CAS  Google Scholar 

  • MR Rojas RL Gilbertson DR Russell DP Maxwell (1993) ArticleTitleUse of degenerate primers in the polymerase chain reaction to detect whitefly-transmitted geminiviruses Plant Dis 77 340–347 Occurrence Handle1:CAS:528:DyaK3sXltV2qt74%3D Occurrence Handle10.1094/PD-77-0340

    Article  CAS  Google Scholar 

  • S Sánchez-Campos JA Díaz F Monci ER Bejarano J Reina J Navas-Castillo MA Aranda E Moriones (2002) ArticleTitleHigh genetic stability of the begomovirus Tomato yellow leaf curl Sardinia virus in southern Spain over an 8-year period Phytopathology 92 842–849 Occurrence Handle18942962

    PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • SV Wesley CA Helliwell NA Smith M Wang DT Rouse Q Liu PS Gooding SP Singh D Abbott PA Stoutjesdijk SP Robinson AP Gleave AG Green PM Waterhouse (2001) ArticleTitleConstruct design for efficient, effect and high throughput gene silencing in plants Plant J 27 581–590 Occurrence Handle11576441 Occurrence Handle1:CAS:528:DC%2BD3MXos12ktLo%3D Occurrence Handle10.1046/j.1365-313X.2001.01105.x

    Article  PubMed  CAS  Google Scholar 

  • Y Yang TA Sherwood CP Patte E Hiebert JE Polston (2004) ArticleTitleUse of Tomato yellow leaf curl virus (TYLCV) Rep gene sequences to engineer TYLCV resistance in tomato Phytopathology 94 490–496 Occurrence Handle1:CAS:528:DC%2BD2cXkt1Sitrs%3D Occurrence Handle18943768

    CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Biotechnology, Faculty of Agricultural Technology, Al-Balqa’ Applied University, Al-Salt, Jordan

    M. K. Abhary & G. H. Anfoka

  2. Department of Plant Pathology, University of Wisconsin-Madison, Madison, WI, U.S.A.

    M. K. Nakhla & D. P. Maxwell

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  1. M. K. Abhary
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  2. G. H. Anfoka
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  3. M. K. Nakhla
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  4. D. P. Maxwell
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Abhary, M., Anfoka, G., Nakhla, M. et al. Post-transcriptional gene silencing in controlling viruses of the Tomato yellow leaf curl virus complex. Arch Virol 151, 2349–2363 (2006). https://doi.org/10.1007/s00705-006-0819-7

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