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.
This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Tax calculation will be finalised during checkout.
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
Tax calculation will be finalised during checkout.
Roossinck MJ (2011) The good viruses: viral mutualistic symbioses. Nature Rev Microbiol 9:99–108
Ishibashi K, Ishikawa M (2016) Replication of tobamovirus RNA. Annu Rev Phytopathol 54:55–78
Buck KW (1996) Comparison of the replication of positive-stranded RNA viruses of plants and animals. Adv Virus Res 47:159–251
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 96:1915–1923
Lai MMC (1998) Cellular factors in the transcription and replication of viral RNA genomes: a parallel to DNA-dependent RNA transcription. Virology 244:1–12
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):2097–2106
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):12985–12990
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):33–38
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 76:2491–2497
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 22:335–343
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 579:4479–4484
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):78–85
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 391:806–811
Bernstein E, Caudy AA, Hammond SM, Hannon GJ (2001) Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409:363–366
Hammond SM, Bernstein E, Beach D, Hannon GJ (2000) An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells. Nature 404:293–296
Baulcombe DC (2004) RNA silencing in plants. Nature 431:356–363
Hamilton AJ, Baulcombe DC (1999) A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286:950–952
Voinnet O (2001) RNA silencing as a plant immune system against viruses. Trends Genet 17:449–459
Waterhouse PM, Wang MB, Lough T (2001) Gene silencing as an adaptive defence against viruses. Nature 411:834–842
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):426–431
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 32:239–247
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):1371–1377
Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bull 19:11–15
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):e63257
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 63:35–47
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 8:256–259
Meyer P, Saedler H (1996) Homology dependent gene silencing in plants. Ann Rev Plant Physiol Plant Mol Biol 47:23–48
Kenyon L, Kumar S, Tsai WS, Hughes JďA (2014) Virus diseases of peppers (Capsicum spp.) and their control. Adv Virus Res 90:297
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
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.
Conflict of interest
The authors have declared that no competing interests exist.
This article does not contain any studies with animals performed by any of the authors.
Informed consent was obtained from all individual participants included in the study.
Handling Editor: F. Murilo Zerbini.
Electronic supplementary material
Below is the link to the electronic supplementary material.
About this article
Cite this article
Ali, M.E., Ishii, Y., Taniguchi, Ji. et al. Conferring virus resistance in tomato by independent RNA silencing of three tomato homologs of Arabidopsis TOM1. Arch Virol 163, 1357–1362 (2018). https://doi.org/10.1007/s00705-018-3747-4
- Virus resistance
- RNA silencing
- Tomato mosaic virus