Skip to main content

Advertisement

Log in

Potentiality of Methylation-sensitive Amplification Polymorphism (MSAP) in Identifying Genes Involved in Tomato Response to Tomato Yellow Leaf Curl Sardinia Virus

  • Published:
Plant Molecular Biology Reporter Aims and scope Submit manuscript

Abstract

Plants have developed several genetically regulated defense strategies against a wide range of biotic stresses (viruses, fungi, bacteria, nematodes). There is experimental evidence that DNA methylation and post-transcriptional gene silencing (PTGS) are strongly associated and have evolved as plant defense mechanisms against invasion by foreign nucleic acids, including viruses. Recent studies have shown that PTGS is activated in plants infected by the geminivirus Tomato yellow leaf curl Sardinia virus (TYLCSV). To compare the DNA methylation profiles in TYLCSV-infected vs mock-inoculated tomato (Solanum lycopersicum syn. Lycopersicon esculentum) plants, a methylation-sensitive amplification polymorphism (MSAP) methodology was applied. The pattern of methylation was assayed at different stages of infection (1, 7, and 14 days) after inoculation by the natural vector Bemisia tabaci. Thirty-four polymorphic fragments were identified, of which ten were sequenced. The majority (eight out of ten) of polymorphisms generated by changes in methylation after TYLCSV infection belong to expressed portions of the tomato genome, mostly involved in defense and stress responses. Although the differences in expression levels during infection (in all cases examined except one) could be detected at least at one time-point, no clear correlation could be found between overexpression or underexpression and changes in methylation profiles. Our data demonstrate that TYLCSV induces changes in the methylation status of the tomato genome and that MSAP might contribute in identifying genes involved in plant–virus interactions.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

MSAP:

methylation-sensitive amplification polymorphism

AFLP:

amplified fragment length polymorphism

RT-qPCR:

reverse transcription quantitative PCR

PTGS:

post-transcriptional gene silencing

TGS:

transcriptional gene silencing

TYLCSV:

Tomato yellow leaf curl Sardinia virus

TLCV:

Tomato leaf curl virus

TGMV:

Tomato golden mosaic virus

IAP:

inoculation access period

AGT:

actin gene tomato

BLAST:

basic local alignment search tool

CDS:

coding sequence

GSS:

Genome Survey Sequences (database)

PLACE:

plant cis-acting regulatory DNA elements (database)

References

  • Accotto GP, Navas-Castillo J, Noris E, Moriones E, Louro D. Typing tomato yellow leaf curl viruses in Europe. Eur J Plant Pathol. 2000;106:179–86.

    Article  Google Scholar 

  • Ach RA, Durfee T, Miller AB, Taranto P, Hanley-Bowdoin L, Zambriski PC, et al. RRB1 and RRB2 encode maize retinoblastoma-related proteins that interact with a plant D-type cyclin and a geminivirus replication protein. Mol Cell Biol. 1997;17:5077–86.

    PubMed  CAS  Google Scholar 

  • Agrawal N, Dasaradhi PV, Mohmmed A, Malhotra P, Bhatnagar RK, Mukherjee SK. RNA interference: biology, mechanism, and applications. Microbiol Mol Biol Rev. 2003;67 4:657–85.

    Article  PubMed  CAS  Google Scholar 

  • Arguello-Astorga G, Lopez-Ochoa L, Kong LJ, Orozco BM, Settlage SB, Hanley-Bowdoin L. A novel motif in geminivirus replication proteins interacts with the plant retinoblastoma-related protein. J Virol. 2004;78 9:4817–26.

    Article  PubMed  CAS  Google Scholar 

  • Ashikawa I. Surveying CpG methylation at 5′-CCGG in the genomes of rice cultivars. Plant Mol Biol. 2001;45 1:31–9.

    Article  PubMed  CAS  Google Scholar 

  • Avrova AO, Stewart HE, De Jong WD, Heilbronn J, Lyon GD, Birch PR. A cysteine protease gene is expressed early in resistant potato interactions with Phytophthora infestans. Mol Plant–Microbe Interact. 1999;12 12:1114–9.

    Article  PubMed  CAS  Google Scholar 

  • Bassam BJ, Caetano-Anolles G, Gresshoff PM. Fast and sensitive silver staining of DNA in polyacrylamide gels. Anal Biochem. 1991;196 1:80–3.

    Article  PubMed  CAS  Google Scholar 

  • Baurens FC, Bonnot F, Bienvenu D, Causse S, Legavre T. Using SD-AFLP and MSAP to assess CCGG methylation in the banana genome. Plant Mol Biol Report. 2003;21:339–48.

    Article  CAS  Google Scholar 

  • Bhende PM, Seaman WT, Delecluse HJ, Kenney SC. The EBV lytic switch protein, Z, preferentially binds to and activates the methylated viral genome. Nat Genet. 2004;36 10:1099–104.

    Article  PubMed  CAS  Google Scholar 

  • Brough CL, Gardiner WE, Inamdar NM, Zhang XY, Ehrlich M, Bisaro DM. DNA methylation inhibits propagation of tomato golden mosaic virus DNA in transfected protoplasts. Plant Mol Biol. 1992;18 4:703–12.

    Article  PubMed  CAS  Google Scholar 

  • Cassens S, Ulrich U, Beimling P, Simon D. Inhibition of human T cell leukaemia virus type I long terminal repeat expression by DNA methylation: implications for latency. J Gen Virol 1994;75 11:3255–9.

    Article  PubMed  CAS  Google Scholar 

  • Collin S, Fernandez-Lobato M, Gooding PS, Mullineaux PM, Fenoll C. The two nonstructural proteins from wheat dwarf virus involved in viral gene expression and replication are retinoblastoma-binding proteins. Virology 1996;219 1:324–9.

    Article  PubMed  CAS  Google Scholar 

  • Dixon MS, Hatzixanthis K, Jones DA, Harrison K, Jones JDG. The tomato Cf-5 disease resistance gene and six homologs show pronounced allelic variation in leucine-rich repeat copy number. Plant Cell 1998;10:1915–1925.

    Article  PubMed  CAS  Google Scholar 

  • Doyle JJ, Doyle JL. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 1987;19:11–5.

    Google Scholar 

  • Drake R, John I, Farrell A, Cooper W, Schuch W, Grierson D. Isolation and analysis of cDNAs encoding tomato cysteine proteases expressed during leaf senescence. Plant Mol Biol. 1996;30 4:755–67.

    Article  PubMed  CAS  Google Scholar 

  • Edamoto Y, Hara A, Biernat W, Terracciano L, Cathomas G, Riehle HM, et al. Alterations of RB1, p53 and Wnt pathways in hepatocellular carcinomas associated with hepatitis C, hepatitis B and alcoholic liver cirrhosis. Int J Cancer. 2003;106 3:334–41.

    Article  PubMed  CAS  Google Scholar 

  • Ernberg I, Falk K, Minarovits J, Busson P, Tursz T, Masucci MG, et al. The role of methylation in the phenotype-dependent modulation of Epstein–Barr nuclear antigen 2 and latent membrane protein genes in cells latently infected with Epstein–Barr virus. J Gen Virol. 1989;70:2989–3002.

    Article  PubMed  CAS  Google Scholar 

  • Fang JY, Mikovits JA, Bagni R, Petrow-Sadowski CL, Ruscetti FW. Infection of lymphoid cells by integration-defective human immunodeficiency virus type 1 increases de novo methylation. J Virol. 2001;75 20:9753–61.

    Article  PubMed  CAS  Google Scholar 

  • Gutterson N, Reuber TL. Regulation of disease resistance pathways by AP2/ERF transcription factors. Curr Opin Plant Biol. 2004;7 4:465–71.

    Article  PubMed  CAS  Google Scholar 

  • Hebsgaard SM, Korning PG, Tolstrup N, Engelbrecht J, Rouze P, Brunak S. Splice site prediction in Arabidopsis thaliana DNA by combining local and global sequence information. Nucleic Acids Res. 1996;24 17:3439–52.

    Article  PubMed  CAS  Google Scholar 

  • Higo K, Ugawa Y, Iwamoto M, Korenaga T. Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res. 1999;27 1:297–300.

    Article  PubMed  CAS  Google Scholar 

  • Jones L, Hamilton AJ, Voinnet O, Thomas CL, Maule AJ, Baulcombe DC. RNA-DNA interactions and DNA methylation in post-transcriptional gene silencing. Plant Cell. 1999;11 12:2291–301.

    Article  PubMed  CAS  Google Scholar 

  • Jones L, Ratcliff F, Baulcombe DC. RNA-directed transcriptional gene silencing in plants can be inherited independently of the RNA trigger and requires Met1 for maintenance. Curr Biol. 2001;11 10:747–57.

    Article  PubMed  CAS  Google Scholar 

  • Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J. Repbase Update, a database of eukaryotic repetitive elements. Cytogenet Genome Res. 2005;110:462–7.

    Article  PubMed  CAS  Google Scholar 

  • Kheyr-Pour A, Bendahmane M, Matzeit V, Accotto GP, Crespi S, Gronenborn B. Tomato yellow leaf curl virus from Sardinia is a whitefly-transmitted monopartite geminivirus. Nucleic Acids Res. 1991;19 24:6763–9.

    Article  PubMed  CAS  Google Scholar 

  • Lam E, del Pozo O. Caspase-like protease involvement in the control of plant cell death. Plant Mol Biol. 2000;44:417–28.

    Article  PubMed  CAS  Google Scholar 

  • Li HP, Leu YW, Chang YS. Epigenetic changes in virus-associated human cancers. Cell Res. 2005;15 4:262–71.

    Article  PubMed  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001;25 4:402–8.

    Article  PubMed  CAS  Google Scholar 

  • Llave C, Kasschau KD, Carrington JC. Virus encoded suppressor of post-transcriptional gene silencing targets a maintenance step in silencing pathway. Proc Natl Acad Sci USA. 2000;97:13401–6.

    Article  PubMed  CAS  Google Scholar 

  • Lucioli A, Noris E, Brunetti A, Tavazza R, Ruzza V, Castello AG, et al. Rep-protein-mediated resistance to homologous and heterologous geminiviruses occurs by two distinct mechanisms while viruses overcome these by silencing the transgene. J Virol. 2003;77 12:6785–98.

    Article  PubMed  CAS  Google Scholar 

  • Matthes M, Singh R, Cheah SC, Karp A. Variation in oil palm (Elaeis guineensis Jacq.) tissue culture-derived regenerants revealed by AFLPs with methylation-sensitive enzymes. Theor Appl Genet. 2001;102:971–9.

    Article  CAS  Google Scholar 

  • Peraza-Echeverria S, Herrera-Valencia VA, James-Kay A. Detection of DNA methylation changes in micropropagated banana plants using methylation-sensitive amplification polymorphism (MSAP). Plant Sci. 2001;161:359–67.

    Article  PubMed  CAS  Google Scholar 

  • Portis E, Acquadro A, Comino C, Lanteri S. Analysis of DNA methylation during germination of pepper (Capsicum annuum L.) seeds using methylation-sensitive amplification polymorphism (MSAP). Plant Sci. 2004;166 1:169–78.

    Article  CAS  Google Scholar 

  • Reese MG, Eeckman FH, Kulp D, Haussler D. Improved splice site detection in genie. J Comp Biol. 1997;4 3:311–23.

    Article  CAS  Google Scholar 

  • Reyna-López GE, Simpson J, Ruiz-Herrera J. Differences in DNA methylation pattern are detectable during the dimorphic transition of fungi by amplification of restriction polymorphisms. Mol Gen Genet. 1997;253:703–10.

    Article  PubMed  Google Scholar 

  • Robertson KD, Wolffe AP. DNA methylation in health and disease. Nat Rev Genet 2000;1:11–9.

    Article  PubMed  CAS  Google Scholar 

  • Rozen S, Skaletsky HJ. Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S, editors. Bioinformatics methods and protocols: methods in molecular biology. Totowa, NJ: Humana; 2000. p. 365–86.

    Google Scholar 

  • Seemanpillai M, Dry I, Randles J, Rezaian A. Transcriptional silencing of geminiviral promoter-driven transgenes following homologous virus infection. Mol Plant–Microbe Interact. 2003;16 5:429–38.

    Article  PubMed  CAS  Google Scholar 

  • Sha AH, Lin XH, Huang JB, Zhang DP. Analysis of DNA methylation related to rice adult plant resistance to bacterial blight based on methylation-sensitive AFLP (MSAP) analysis. Mol Genet Genomics. 2005;273 6:484–90.

    Article  PubMed  CAS  Google Scholar 

  • Sherman JD, Talbert LE. Vernalization-induced changes in the methylation pattern of winter wheat. Genome. 2002;45:253–60.

    Article  PubMed  CAS  Google Scholar 

  • Simon B, Cenis JL, Demichelis S, Rapisarda C, Caciagli P, Bosco D. Survey of Bemisia tabaci (Hemiptera: Aleyrodidae) biotypes in Italy with the description of a new biotype (T) from Euphorbia characias. Bull Entomol Res. 2003;93 3:259–64.

    Article  PubMed  CAS  Google Scholar 

  • Tanaka J, Ishida T, Choi BI, Yasuda J, Watanabe T, Iwakura Y. Latent HIV-1 reactivation in transgenic mice requires cell cycle -dependent demethylation of CREB/ATF sites in the LTR. AIDS. 2003;17 2:167–75.

    Article  PubMed  CAS  Google Scholar 

  • Voinnet O. Induction and suppression of RNA silencing: insights from viral infections. Nat Rev Genet 2005;6:206–20.

    Article  PubMed  CAS  Google Scholar 

  • Vos P, Hogers R, Bleeker M, Reijans M, Lee TV, Hornes M, et al. AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res. 1995;23:4407–14.

    Article  PubMed  CAS  Google Scholar 

  • Waterhouse PM, Wang MB, Lough T. Gene silencing as an adaptive defence against viruses. Nature. 2001;411:834–42.

    Article  PubMed  CAS  Google Scholar 

  • Xie Q, Suarez-Lopez P, Gutierrez C. Identification and analysis of a retinoblastoma binding motif in the replication protein of a plant DNA virus: requirement for efficient viral DNA replication. EMBO J. 1995;14 16:4073–82.

    PubMed  CAS  Google Scholar 

  • Xiong LZ, Xu CG, Maroof S, Zhang G. Patterns of cytosine methylation in an elite rice hybrid and its parental lines, detected by a methylation-sensitive amplification polymorphism technique. Mol Gen Genet. 1999;261:439–46.

    Article  PubMed  CAS  Google Scholar 

  • Xu M, Li X, Korban SS. AFLP-based detection of DNA methylation. Plant Mol Biol Report. 2000;18:361–8.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Lorenzo Barchi, Daniele Marian, and Manuela Vecchiati for the technical assistance; Piero Caciagli for the help with whitefly transmission; and Robert G. Milne for the critical reading of the manuscript. This work was supported in part by funds for scientific research of Regione Piemonte.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Gian Paolo Accotto or Ezio Portis.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mason, G., Noris, E., Lanteri, S. et al. Potentiality of Methylation-sensitive Amplification Polymorphism (MSAP) in Identifying Genes Involved in Tomato Response to Tomato Yellow Leaf Curl Sardinia Virus. Plant Mol Biol Rep 26, 156–173 (2008). https://doi.org/10.1007/s11105-008-0031-x

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11105-008-0031-x

Keywords

Navigation