Advertisement

Archives of Virology

, Volume 163, Issue 5, pp 1357–1362 | Cite as

Conferring virus resistance in tomato by independent RNA silencing of three tomato homologs of Arabidopsis TOM1

  • Md Emran Ali
  • Yuko Ishii
  • Jyun-ichi Taniguchi
  • Sumyya Waliullah
  • Kappei Kobayashi
  • Takashi Yaeno
  • Naoto Yamaoka
  • Masamichi Nishiguchi
Brief Report

Abstract

The TOM1/TOM3 genes from Arabidopsis are involved in the replication of tobamoviruses. Tomato homologs of these genes, LeTH1, LeTH2 and LeTH3, are known. In this study, we examined transgenic tomato lines where inverted repeats of either LeTH1, LeTH2 or LeTH3 were introduced by Agrobacterium. Endogenous mRNA expression for each gene was detected in non-transgenic control plants, whereas a very low level of each of the three genes was found in the corresponding line. Small interfering RNA was detected in the transgenic lines. Each silenced line showed similar levels of tobamovirus resistance, indicating that each gene is similarly involved in virus replication.

Keywords

Tomato Virus resistance RNA silencing LeTH1 LeTH2 LeTH3 TOM1 TOM3 Tomato mosaic virus 

Notes

Acknowledgements

We are grateful to M. Ishikawa for providing plasmids, and to M. Syonaka, Y. Watanabe and A. Mochizuki for Agrobacterium clones and the transgenic tomato seeds. We also thank D. Murphy and A. Stasko for checking the English in the manuscript. This work was supported by the Program for Promotion of Basic and Applied Research in Bio-oriented Industry (BRAIN), the Ministry of Education, Culture, Sports and Technology of Japan [Grant-in-Aid for Scientific Research for Scientific Research (C), No. 24580065] to MN and the Japan Science and Technology Agency for the A-step (Adaptable and Seamless Technology Transfer Program through Target-driven R & D) to MN.

Compliance with ethical standards

Conflict of interest

The authors have declared that no competing interests exist.

Ethical approval

This article does not contain any studies with animals performed by any of the authors.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Supplementary material

705_2018_3747_MOESM1_ESM.pptx (805 kb)
Supplementary material 1 (PPTX 805 kb)

References

  1. 1.
    Roossinck MJ (2011) The good viruses: viral mutualistic symbioses. Nature Rev Microbiol 9:99–108CrossRefGoogle Scholar
  2. 2.
    Ishibashi K, Ishikawa M (2016) Replication of tobamovirus RNA. Annu Rev Phytopathol 54:55–78CrossRefPubMedGoogle Scholar
  3. 3.
    Buck KW (1996) Comparison of the replication of positive-stranded RNA viruses of plants and animals. Adv Virus Res 47:159–251CrossRefPubMedGoogle Scholar
  4. 4.
    Ohno T, Aoyagi M, Yamanashi Y, Saito H, Ikawa S, Meshi T, Okada Y (1984) Nucleotide sequence of the tobacco mosaic virus (tomato strain) genome and comparison with the common strain genome. J Biochem 96:1915–1923CrossRefPubMedGoogle Scholar
  5. 5.
    Lai MMC (1998) Cellular factors in the transcription and replication of viral RNA genomes: a parallel to DNA-dependent RNA transcription. Virology 244:1–12CrossRefPubMedGoogle Scholar
  6. 6.
    Lee WM, Ishikawa M, Ahlquist P (2001) Mutation of host delta ∆9 fatty acid desaturase inhibits brome mosaic virus RNA replication between template recognition and RNA synthesis. J Virol 75(5):2097–2106CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Noueiry AO, Chen JB, Ahlquist P (2000) A mutant allele of essential, general translation initiation factor DED1 selectively inhibits translation of a viral mRNA. Proc Natl Acad Sci 97(24):12985–12990CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Ishikawa M, Obata F, Kumagai T, Ohno T (1991) Isolation of mutants of Arabidopsis thaliana in which accumulation of tobacco mosaic virus coat protein is reduced to low levels. Mol Gen Genet 230(1–2):33–38CrossRefPubMedGoogle Scholar
  9. 9.
    Yamanaka T, Imai T, Satoh R, Kawashima A, Takahashi M, Tomita K, Kubota K, Meshi T, Naito S, Ishikawa M (2002) Complete inhibition of tobamovirus multiplication by simultaneous mutations in two homologous host genes. J Virol 76:2491–2497CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Tsujimoto Y, Numaga T, Ohshima K, Yano M, Ohsawa R, Derek BG, Naito S, Ishikawa M (2003) Arabidopsis TOBAMOVIRUS MULTIPLICATION(TOM) 2 locus encodes a transmembrane protein that interacts with TOM1. EMBO 22:335–343CrossRefGoogle Scholar
  11. 11.
    Asano M, Satoh R, Mochizuki A, Tsuda S, Yamanaka T, Nishiguchi M, Hirai K, Meshi T, Naito S, Ishikawa M (2005) Tobamovirus-resistant tobacco generated by RNA interference directed against host genes. FEBS Lett 579:4479–4484CrossRefPubMedGoogle Scholar
  12. 12.
    Sunil K, Ashvini KD, Ruma K, Kukkundoor RK, Mathew KM, Harischandra SP (2012) Inhibition of TMV multiplication by siRNA constructs against TOM1 and TOM3 genes of Capsicum annuum. J Virol Meth 186(1–2):78–85Google Scholar
  13. 13.
    Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806–811CrossRefPubMedGoogle Scholar
  14. 14.
    Bernstein E, Caudy AA, Hammond SM, Hannon GJ (2001) Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409:363–366CrossRefPubMedGoogle Scholar
  15. 15.
    Hammond SM, Bernstein E, Beach D, Hannon GJ (2000) An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells. Nature 404:293–296CrossRefPubMedGoogle Scholar
  16. 16.
    Baulcombe DC (2004) RNA silencing in plants. Nature 431:356–363CrossRefPubMedGoogle Scholar
  17. 17.
    Hamilton AJ, Baulcombe DC (1999) A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286:950–952CrossRefPubMedGoogle Scholar
  18. 18.
    Voinnet O (2001) RNA silencing as a plant immune system against viruses. Trends Genet 17:449–459CrossRefPubMedGoogle Scholar
  19. 19.
    Waterhouse PM, Wang MB, Lough T (2001) Gene silencing as an adaptive defence against viruses. Nature 411:834–842CrossRefPubMedGoogle Scholar
  20. 20.
    Sun HJ, Uchii S, Watanabe S, Ezura H (2006) A highly efficient transformation protocol for micro-tom, a model cultivar for tomato functional genomics. Plant Cell Physiol 47(3):426–431CrossRefPubMedGoogle Scholar
  21. 21.
    Chetty VJ, Ceballos N, Garcia D, Narváez-Vásquez J, Lopez W, Orozco-Cárdenas ML (2013) Evaluation of four Agrobacterium tumefaciens strains for the genetic transformation of tomato (Solanum lycopersicum L.) cultivar Micro-Tom. Plant Cell Rep 32:239–247CrossRefPubMedGoogle Scholar
  22. 22.
    Ali ME, Tabei Y, Kobayashi K, Yamaoka N, Nishiguchi M (2012) Molecular analysis of transgenic melon plants showing virus resistance conferred by direct repeat of movement gene of Cucumber green mottle mosaic virus. Plant Cell Rep 31(8):1371–1377CrossRefPubMedGoogle Scholar
  23. 23.
    Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bull 19:11–15Google Scholar
  24. 24.
    Ali ME, Kobayashi K, Yamaoka N, Ishikawa M, Nishiguchi M (2013) Graft transmission of RNA silencing to non-transgenic scions for conferring virus resistance in tobacco. PLoS ONE 8(5):e63257CrossRefGoogle Scholar
  25. 25.
    Haque AKMN, Tanaka Y, Nishiguchi M (2007) Analysis of transitive RNA silencing after grafting in transgenic plants with the coat protein gene of Sweet potato feathery mottle virus. Plant Mol Biol 63:35–47CrossRefPubMedGoogle Scholar
  26. 26.
    Chen B, Jiang JH, Zhou XP (2007) A TOM1 homologue is required for multiplication of Tobacco mosaic virus in Nicotiana benthamiana. J Zhejiang Univ Science B 8:256–259CrossRefGoogle Scholar
  27. 27.
    Meyer P, Saedler H (1996) Homology dependent gene silencing in plants. Ann Rev Plant Physiol Plant Mol Biol 47:23–48CrossRefGoogle Scholar
  28. 28.
    Kenyon L, Kumar S, Tsai WS, Hughes JďA (2014) Virus diseases of peppers (Capsicum spp.) and their control. Adv Virus Res 90:297CrossRefPubMedGoogle Scholar
  29. 29.
    Cruz-Reyes R, vila-Sakar GÁ, Sánchez-Montoya G, Quesada M (2015) Experimental assessment of gene flow between transgenic squash and a wild relative in the center of origin of cucurbits. Ecosphere 6(12):248.  https://doi.org/10.1890/ES15-00304.1 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Faculty of AgricultureEhime UniversityMatsuyamaJapan

Personalised recommendations