Skip to main content

Advertisement

SpringerLink
Log in

Making a friend from a foe: expressing a GroEL gene from the whitefly Bemisia tabaci in the phloem of tomato plants confers resistance to tomato yellow leaf curl virus

  • Published:
Archives of Virology Aims and scope Submit manuscript

Summary

Some (perhaps all) plant viruses transmitted in a circulative manner by their insect vectors avoid destruction in the haemolymph by interacting with GroEL homologues, ensuring transmission. We have previously shown that the phloem-limited begomovirus tomato yellow leaf curl virus (TYLCV) interacts in vivo and in vitro with GroEL produced by the whitefly vector Bemisia tabaci. In this study, we have exploited this phenomenon to generate transgenic tomato plants expressing the whitefly GroEL in their phloem. We postulated that following inoculation, TYLCV particles will be trapped by GroEL in the plant phloem, thereby inhibiting virus replication and movement, thereby rendering the plants resistant. A whitefly GroEL gene was cloned in an Agrobacterium vector under the control of an Arabidopsis phloem-specific promoter, which was used to transform two tomato genotypes. During three consecutive generations, plants expressing GroEL exhibited mild or no disease symptoms upon whitefly-mediated inoculation of TYLCV. In vitro assays indicated that the sap of resistant plants contained GroEL-TYLCV complexes. Infected resistant plants served as virus source for whitefly-mediated transmission as effectively as infected non-transgenic tomato. Non-transgenic susceptible tomato plants grafted on resistant GroEL-transgenic scions remained susceptible, although GroEL translocated into the grafted plant and GroEL-TYLCV complexes were detected in the grafted tissues.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • MK Abhary GH Anfoka MK Nakhla DP Maxwell (2006) ArticleTitlePost-transcriptional gene silencing in controlling viruses of the Tomato yellow leaf curl virus complex Arch Virol 148 405–421

    Google Scholar 

  • F Akad N Dotan H Czosnek (2004) ArticleTitleTrapping of Tomato yellow leaf curl virus (TYLCV) and other plant viruses with a GroEL homologue from the whitefly Bemisia tabaci Arch Virol 149 1481–1497 Occurrence Handle15290375 Occurrence Handle10.1007/s00705-004-0317-8 Occurrence Handle1:CAS:528:DC%2BD2cXmtVWkurg%3D

    Article  PubMed  CAS  Google Scholar 

  • Y Antignus R Vunsh O Lachman M Pearsman L Maslenin U Hananya A Rosner (2004) ArticleTitleTruncated Rep gene originated from Tomato yellow leaf curl virus-Israel [Mild] confers strain-specific resistance in transgenic tomato Ann Appl Biol 144 39–44 Occurrence Handle10.1111/j.1744-7348.2004.tb00314.x

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • R Barg M Pilowsky S Shabtai N Carmi AD Szechtman B Dedicova Y Salts (1997) ArticleTitleThe TYLCV-tolerant tomato line MP-1 is characterized by superior transformation competence J Exp Botany 48 1919–1923 Occurrence Handle1:CAS:528:DyaK2sXotVCrsr0%3D

    CAS  Google Scholar 

  • R Bernatzky SD Tanksley (1986) ArticleTitleMajority of random cDNA clones correspond to single loci in the tomato genome Mol Gen Gene 203 8–14 Occurrence Handle10.1007/BF00330377 Occurrence Handle1:CAS:528:DyaL28XktF2ktro%3D

    Article  CAS  Google Scholar 

  • JK Brown H Czosnek (2002) Whitefly transmission of plant viruses RT Plumb (Eds) Advances in botanical research SeriesTitlePlant virus vector interactions NumberInSeries36 Academic Press New York 65–100

    Google Scholar 

  • A Brunetti M Tavazza E Noris R Tavazza P Caciagli G Ancora S Crespi GP Accotto (1997) ArticleTitleHigh expression of truncated viral rep protein confers resistance to tomato yellow leaf curl virus in transgenic tomato plants Mol Plant-Microbe Interact 10 571–579 Occurrence Handle10.1094/MPMI.1997.10.5.571 Occurrence Handle1:CAS:528:DyaK2sXjvFOktrk%3D

    Article  CAS  Google Scholar 

  • Brunt AA, Crabtree K, Dallwitz MJ, Gibbs AJ, Watson L, Zurcher EJ (eds) (1996) Plant viruses online: descriptions and lists from the VIDE database. Version: 20th August 1996. URL http://image.fs.uidaho.edu/vide/refs.htm

  • S Cohen (1993) ArticleTitleSweet potato whitefly biotypes and their connection with squash silver leaf Phytoparasitica 21 174

    Google Scholar 

  • Y Gafni B Epel (2002) ArticleTitleThe role of host and viral proteins in intra- and inter-cellular trafficking of geminiviruses Physiol Mol Plant Pathol 60 231–241 Occurrence Handle10.1006/pmpp.2002.0402 Occurrence Handle1:CAS:528:DC%2BD38Xltlamu7Y%3D

    Article  CAS  Google Scholar 

  • M Gibbs (1999) ArticleTitleChaperonin camouflage Nature 399 415 Occurrence Handle10.1038/20813 Occurrence Handle1:CAS:528:DyaK1MXjvVyrurY%3D

    Article  CAS  Google Scholar 

  • L Hanley-Bowdoin SB Settlage D Robertson (2004) ArticleTitleReprogramming plant gene expression – a prerequisite to geminivirus DNA replication Mol Plant Pathol 5 149–156 Occurrence Handle10.1111/j.1364-3703.2004.00214.x Occurrence Handle1:CAS:528:DC%2BD2cXjt1GqurY%3D

    Article  CAS  Google Scholar 

  • S Hehnle C Wege H Jeske (2004) ArticleTitleInteraction of DNA with the movement proteins of geminiviruses revisited J Virol 78 7698–7706 Occurrence Handle15220444 Occurrence Handle10.1128/JVI.78.14.7698-7706.2004 Occurrence Handle1:CAS:528:DC%2BD2cXlvFSgsrw%3D

    Article  PubMed  CAS  Google Scholar 

  • T Kunik R Salomon N Navot M Zeidan I Michelson D Zamir Y Gafni H Czosnek (1994) ArticleTitleTransgenic tomato plants expressing the tomato yellow leaf curl virus capsid protein are resistant to the virus BioTechnology 12 500–504 Occurrence Handle7764709 Occurrence Handle10.1038/nbt0594-500 Occurrence Handle1:CAS:528:DyaK2cXltVChurk%3D

    Article  PubMed  CAS  Google Scholar 

  • UK Laemmli (1970) ArticleTitleCleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227 680–685 Occurrence Handle5432063 Occurrence Handle10.1038/227680a0 Occurrence Handle1:CAS:528:DC%2BD3MXlsFags7s%3D

    Article  PubMed  CAS  Google Scholar 

  • M Lapidot M Friedmann (2002) ArticleTitleBreeding for resistance to whitefly-transmitted geminiviruses Ann Appl Biol 140 109–127 Occurrence Handle10.1111/j.1744-7348.2002.tb00163.x

    Article  Google Scholar 

  • M Lapidot M Friedmann M Pilowsky R Ben-Joseph S Cohen (2001) ArticleTitleEffect of host plant resistance to Tomato yellow leaf curl virus (TYLCV) on virus acquisition and transmission by its whitefly vector Phytopathology 91 209–1213 Occurrence Handle10.1094/PHYTO.2001.91.12.1209

    Article  Google Scholar 

  • MP Mayer (2005) ArticleTitleRecruitment of Hsp70 chaperones: a crucial part of viral survival strategies Rev Physiol Biochem Pharmacol 153 1–46 Occurrence Handle15243813 Occurrence Handle10.1007/s10254-004-0025-5 Occurrence Handle1:CAS:528:DC%2BD2MXktlOjsbo%3D

    Article  PubMed  CAS  Google Scholar 

  • N Mitter E Sulistyowati MW Graham RG Dietzgen (2001) ArticleTitleSuppression of gene silencing, a threat to virus-resistant transgenic plants Trends Plant Sci 6 246–247 Occurrence Handle11378464 Occurrence Handle10.1016/S1360-1385(01)01947-1 Occurrence Handle1:CAS:528:DC%2BD3MXlsFyhsbc%3D

    Article  PubMed  CAS  Google Scholar 

  • S Morin M Ghanim M Zeidan H Czosnek M Verbeek JFJM van den Heuvel (1999) ArticleTitleA GroEL homologue from endosymbiotic bacteria of the whitefly Bemisia tabaci is implicated in the circulative transmission of Tomato yellow leaf curl virus Virology 256 75–84 Occurrence Handle10087228 Occurrence Handle10.1006/viro.1999.9631 Occurrence Handle1:CAS:528:DyaK1MXhvFWiu7o%3D

    Article  PubMed  CAS  Google Scholar 

  • S Morin M Ghanim I Sobol H Czosnek (2000) ArticleTitleThe GroEL protein of the whitefly Bemisia tabaci interacts with the coat protein of transmissible and non-transmissible begomoviruses in the yeast two-hybrid system Virology 276 404–416 Occurrence Handle11040131 Occurrence Handle10.1006/viro.2000.0549 Occurrence Handle1:CAS:528:DC%2BD3cXntl2ntbg%3D

    Article  PubMed  CAS  Google Scholar 

  • T Murashige F Skoog (1962) ArticleTitleA revised medium for rapid growth and bioassays with tobacco tissue culture Physiologia Plantarum 15 473–479 Occurrence Handle10.1111/j.1399-3054.1962.tb08052.x Occurrence Handle1:CAS:528:DyaF3sXksFKm

    Article  CAS  Google Scholar 

  • N Navot E Pichersky M Zeidan D Zamir H Czosnek (1991) ArticleTitle Tomato yellow leaf curl virus, a whitefly-transmitted geminivirus with a single genomic component Virology 185 151–161 Occurrence Handle1926771 Occurrence Handle10.1016/0042-6822(91)90763-2 Occurrence Handle1:CAS:528:DyaK38Xmt1Ohu7g%3D

    Article  PubMed  CAS  Google Scholar 

  • JP Nitsch C Nitsch (1969) ArticleTitleHaploid plants from pollen grains Science 163 85–87 Occurrence Handle10.1126/science.163.3862.85 Occurrence Handle17780179

    Article  PubMed  Google Scholar 

  • M Prins (2003) ArticleTitleBroad virus resistance in transgenic plants Trends Biotech 21 373–375 Occurrence Handle10.1016/S0167-7799(03)00183-5 Occurrence Handle1:CAS:528:DC%2BD3sXms1yht74%3D

    Article  CAS  Google Scholar 

  • PD Reid E del Campillo LN Lewis (1990) ArticleTitleAnatomical changes and immunolocalization of cellulase during abscission as observed on nitrocellulose tissue prints Plant Physiol 93 160–165 Occurrence Handle16667429 Occurrence Handle1:CAS:528:DyaK3cXktlOrs7o%3D Occurrence Handle10.1104/pp.93.1.160

    Article  PubMed  CAS  Google Scholar 

  • C Rudolph PH Schreier JF Uhrig (2003) ArticleTitlePeptide-mediated broad-spectrum plant resistance to tospoviruses Proc Natl Acad Sci USA 100 4429–4434 Occurrence Handle12682295 Occurrence Handle10.1073/pnas.0730832100 Occurrence Handle1:CAS:528:DC%2BD3sXjt12gtb8%3D

    Article  PubMed  CAS  Google Scholar 

  • JC Sanford SA Johnston (1985) ArticleTitleThe concept of parasite-derived resistance – deriving resistance genes from the parasite’s own genome J Theor Biol 113 395–405 Occurrence Handle10.1016/S0022-5193(85)80234-4

    Article  Google Scholar 

  • NA Smith SP Singh MB Wang PA Stoutjesdijk AG Green PM Waterhouse (2000) ArticleTitleTotal silencing by intron-spliced hairpin RNAs Nature 407 319–320 Occurrence Handle11014180 Occurrence Handle10.1038/35036500 Occurrence Handle1:CAS:528:DC%2BD3cXnsVKls7Y%3D

    Article  PubMed  CAS  Google Scholar 

  • R Stadler KM Wright C Lauterbach G Amon M Gahrtz A Feuerstein KJ Oparka N Sauer (2005) ArticleTitleExpression of GFP-fusions in Arabidopsis companion cells reveals non-specific protein trafficking into sieve elements and identifies a novel post-phloem domain in roots Plant J 41 319–331 Occurrence Handle15634207 Occurrence Handle10.1111/j.1365-313X.2004.02298.x Occurrence Handle1:CAS:528:DC%2BD2MXhtVWit7c%3D

    Article  PubMed  CAS  Google Scholar 

  • E Truernit N Sauer (1995) ArticleTitleThe promoter of the Arabidopsis thaliana SUC2 sucrose-H+ symporter gene directs expression of β-glucuronidase to the phloem: evidence for phloem loading and unloading by SUC2 Planta 196 564–570 Occurrence Handle7647685 Occurrence Handle10.1007/BF00203657 Occurrence Handle1:CAS:528:DyaK2MXmvFWms7c%3D

    Article  PubMed  CAS  Google Scholar 

  • JFJM van den Heuvel M Verbeek F van der Wilk (1994) ArticleTitleEndosymbiotic bacteria associated with circulative transmission of Potato leafroll virus by Myzus persicae J Gen Virol 75 2559–2565 Occurrence Handle7931143 Occurrence Handle1:CAS:528:DyaK2cXmt1Krsrk%3D Occurrence Handle10.1099/0022-1317-75-10-2559

    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 

  • TMA Wilson (1993) ArticleTitleStrategies to protect crop plants against viruses: pathogen-derived resistance blossoms Proc Natl Acad Sci USA 90 3134–3141 Occurrence Handle8475051 Occurrence Handle10.1073/pnas.90.8.3134 Occurrence Handle1:STN:280:DyaK3s3jsVCmsw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • KM Wright AG Roberts HJ Martens N Sauer KJ Oparka (2003) ArticleTitleStructural and functional vein maturation in developing tobacco leaves in relation to AtSUC2 promoter activity Plant Physiol 131 1555–1565 Occurrence Handle12692315 Occurrence Handle10.1104/pp.102.016022 Occurrence Handle1:CAS:528:DC%2BD3sXjt1Sqsrk%3D

    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 Handle10.1094/PHYTO.2004.94.5.490 Occurrence Handle1:CAS:528:DC%2BD2cXkt1Sitrs%3D Occurrence Handle18943768

    Article  CAS  PubMed  Google Scholar 

  • M Zeidan H Czosnek (1991) ArticleTitleAcquisition of Tomato yellow leaf curl virus by the whitefly Bemisia tabaci J Gen Virol 72 2607–2614 Occurrence Handle1940856 Occurrence Handle1:CAS:528:DyaK38XjvFOg

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. The Otto Warburg Minerva Center for Agricultural Biotechnology & The Robert H. Smith Institute for Plant Science and Genetics in Agriculture, The Hebrew University of Jerusalem, Rehovot, Israel

    F. Akad, A. Eybishtz, D. Edelbaum, R. Gorovits & H. Czosnek

  2. UNESCO Biotechnology Center, Bethlehem University, Bethlehem, West Bank, Palestinian Authority

    O. Dar-Issa & N. Iraki

Authors
  1. F. Akad
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Eybishtz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. D. Edelbaum
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. R. Gorovits
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. O. Dar-Issa
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. N. Iraki
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. H. Czosnek
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Akad, F., Eybishtz, A., Edelbaum, D. et al. Making a friend from a foe: expressing a GroEL gene from the whitefly Bemisia tabaci in the phloem of tomato plants confers resistance to tomato yellow leaf curl virus. Arch Virol 152, 1323–1339 (2007). https://doi.org/10.1007/s00705-007-0942-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-007-0942-0

Keywords

Search

Navigation