Skip to main content
SpringerLink
Log in

Molecular characterization and host reaction to tomato mottle mosaic virus isolated from sweet pepper seeds in Japan

  • Original Article
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

Many countries have identified tomato mottle mosaic virus (ToMMV) as a serious threat to tomato production. Here, we constructed and characterized infectious clones of ToMMV isolated from Japanese sweet pepper seeds. The genome of the Japanese isolate is 6399 nucleotides in length and exhibits the highest identity with previously characterized isolates. For example, it is 99.7% identical to that of the Mauritius isolate, which occurs worldwide. Phylogenetic analysis based on complete genome sequences revealed that the Japanese isolates clustered in the same clade as those from other countries. When homozygous tomato cultivars with tobamovirus resistance genes were inoculated with an infectious cDNA clone of ToMMV, the virus systemically infected tomato plants with symptoms typical of Tm-1-carrying tomato cultivars. In contrast, tomato cultivars carrying Tm-2 or Tm-22 showed symptoms only on the inoculated leaves. Furthermore, when commercial cultivars of Tm-22 heterozygous tomato were inoculated with ToMMV, systemic infections were observed in all cultivars, with infection frequencies ranging from 25 to 100%. Inoculation of heterozygous sweet pepper cultivars with tobamovirus resistance genes (L1, L3, and L4) with ToMMV resulted in an infection frequency of about 70%, but most of the infected L1, L3, and L4 cultivars were symptomless, and 10-20% showed symptoms of necrosis and yellowing. Tomato mosaic virus strain L11A, an attenuated virus, did not provide cross-protection against ToMMV and led to systemic infection with typical symptoms. These results suggest that ToMMV might cause extensive damage to existing tomato and sweet pepper cultivars commonly grown in Japan.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Li R, Gao S, Fei Z, Ling KS (2013) Complete genome sequence of a new tobamovirus naturally infecting tomatoes in Mexico. Genome Announc 1:e00794-e813

    Article  PubMed  PubMed Central  Google Scholar 

  2. Fillmer K, Adkins S, Pongam P, D’Elia T (2015) Complete genome sequence of a tomato mottle mosaic virus isolate from the United States. Genome Announc 3:e00167-e215

    PubMed  PubMed Central  Google Scholar 

  3. Padmanabhan C, Zheng Y, Martin GB, Fei Z, Ling KS (2015) Complete genome sequence of a tomato-infecting tomato mottle mosaic virus in New York. Genome Announc 3:e01523-e1615

    PubMed  PubMed Central  Google Scholar 

  4. Turina M, Geraats BPJ, Ciuffo M (2016) First report of Tomato mottle mosaic virus in tomato crops in Israel. New Dis Rep 33:1

    Article  Google Scholar 

  5. Ambros S, Martinez F, Ivars P, Hernandez C, de la Iglesia F, Elena SF (2017) Molecular and biological characterization of an isolate of Tomato mottle mosaic virus (ToMMV) infecting tomato and other experimental hosts in Eastern Spain. Eur J Plant Pathol 149:261–268

    Article  CAS  Google Scholar 

  6. Li Y, Wang Y, Hu J, Xiao L, Tan G, Lan P, Liu Y, Li F (2017) The complete genome sequence, occurrence and host range of Tomato mottle mosaic virus Chinese isolate. Virol J 14:15

    Article  PubMed  PubMed Central  Google Scholar 

  7. Sui X, Zheng Y, Li R, Padmanabhan C, Tian T, Groth-Helms D, Keinath AP, Fei Z, Wu Z, Lin KS (2017) Molecular and biological characterization of Tomato mottle mosaic virus and development of RT-PCR detection. Plant Dis 101:704–711

    Article  CAS  PubMed  Google Scholar 

  8. Lovelock DA, Kinoti WM, Bottcher C, Wildman O, Dall D, Rodoni BC, Constable FE (2020) Tomato mottle mosaic virus intercepted by Australian biosecurity in Capsicum annuum seed. Australasian Plant Dis Notes 15:8

    Article  CAS  Google Scholar 

  9. Tu L, Wu S, Gao D, Liu Y, Zhu Y, Ji Y (2021) Synthesis and characterization of a full-length infectious cDNA clone of Tomato mottle mosaic virus. Viruses 13:1050

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Fowkes AR, Botermans M, Frew L, deKoning PPM, Buxton-Kirk A, Westenberg M, Ward R, Schenk MF, Webster G, Alraiss K, Harju V, Skelton A, Conyers C, Barrett B, Adams IP, McGreig S, Fox A, Vazquez-Iglesias I (2022) First report of Tomato mottle mosaic virus in Solanum lycopersicum seeds in The Netherlands and intercepted in seed imported from Asia. New Dis Rep 45:e12067

    Article  Google Scholar 

  11. Adams MJ, Adkins S, Bragard C, Gilmer D, Li D, MacFarlane SA, Wong SM, Melcher U, Ratti C, Ryu KH, ICTV Report Consortium (2017) ICTV virus taxonomy profile: Virgaviridae. J Gen Virol 98:1999–2000

    Article  PubMed  Google Scholar 

  12. Ishibashi K, Kubota K, Kano A, Ishikawa M (2023) Tobamoviruses: old and new threats to tomato cultivation. J Gen Plant Pathol 89:305–321

    Article  Google Scholar 

  13. Hall TJ (1980) Resistance at the Tm-2 locus in the tomato to tomato mosaic virus. Euphytica 29:189–197

    Article  Google Scholar 

  14. Lanfermeijer FC, Dijkhuis J, Sturre MJ, de Haan P, Hille J (2003) Cloning and characterization of the durable tomato mosaic virus resistance gene Tm-22 from Lycopersicon esculentum. Plant Mol Biol 52:1037–1049

    Article  CAS  PubMed  Google Scholar 

  15. Ishibashi K, Masuda K, Naito S, Meshi T, Ishikawa M (2007) An inhibitor of viral RNA replication is encoded by a plant resistance gene. Proc Natl Acad Sci USA 104:13833–13838

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Kobayashi M, Yamamoto-Katou A, Katou S, Hirai K, Meshi T, Ohashi Y, Mitsuhara I (2011) Identification of an amino acid residue required for differential recognition of a viral movement protein by the Tomato mosaic virus resistance gene Tm-22. J Plant Physiol 168:1142–1145

    Article  CAS  PubMed  Google Scholar 

  17. Meshi T, Motoyoshi F, Adachi A, Watanabe Y, Takamatsu N, Okada Y (1988) Two concomitant base substitutions in the putative replicase genes of tobacco mosaic virus confer the ability to overcome the effects of a tomato resistance gene, Tm-1. EMBO J 7:1575–1581

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Meshi T, Motoyoshi F, Maeda T, Yoshiwoka S, Watanabe H, Okada Y (1989) Mutations in the tobacco mosaic virus 30-kD protein gene overcome Tm-2 resistance in tomato. Plant Cell 1:515–522

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Strasser M, Pfitzner A (2007) The double-resistance-breaking Tomato mosaic virus strain ToMV1-2 contains two independent single resistance-breaking domains. Arch Virol 152:903–914

    Article  CAS  PubMed  Google Scholar 

  20. Calder VL, Palukaitis P (1992) Nucleotide sequence analysis of the movement genes of resistance breaking strains of tomato mosaic virus. J Gen Virol 73:165–168

    Article  CAS  PubMed  Google Scholar 

  21. Webster CG, Rosskopf EN, Lucas L, Mellinger HC, Adkins S (2014) First report of Tomato mottle mosaic virus infecting tomato in the United States. Plant Health Prog 15:151–152

    Article  Google Scholar 

  22. Kuroiwa M, Handa S, Gyoutoku Y, Moriyama M, Neriya Y, Nishigawa H, Natsuaki T (2022) Characterization of a ToMV isolate overcoming Tm-22 resistance gene in tomato. Virus Genes 58:478–482

    Article  CAS  PubMed  Google Scholar 

  23. Tsuda S, Kirita M, Watanabe Y (1998) Characterization of a pepper mild mottle tobamovirus strain capable of overcoming the L3 gene-mediated resistance, distinct from the resistance-breaking Italian isolate. Mol Plant Microbe Interact 11:327–331

    Article  CAS  PubMed  Google Scholar 

  24. Genda Y, Kanda A, Hamada H, Sato K, Ohnishi J, Tsuda S (2007) Two amino acid substitutions in the coat protein of Pepper mild mottle virus are responsible for overcoming the L4 gene-mediated resistance in Capsicum spp. Phytopathology 97:787–793

    Article  CAS  PubMed  Google Scholar 

  25. Li YY, Wang CL, Xiang D, Li RH, Liu Y, Li F (2014) First report of tomato mottle mosaic virus infection of pepper in China. Plant Dis 98:1447

    Article  CAS  PubMed  Google Scholar 

  26. Levitzky N, Smith E, Lachman O, Luria N, Mizrahi Y, Bakelman H, Sela N, Laskar O, Milrot E, Dombrovsky A (2019) The bumblebee Bombus terrestris carries a primary inoculum of Tomato brown rugose fruit virus contributing to disease spread in tomatoes. PLoS ONE 14:e0210871

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Gibbs A, Armstrong J, Mackenzie A, Weiller G (1998) GPRIME, a computer program package for designing group PCR primers; its use for characterizing plant viruses. J Virol Methods 74:67–76

    Article  CAS  PubMed  Google Scholar 

  28. Gibbs A, Armstrong J, Gibbs M (2004) A type of nucleotide motif that distinguishes tobamovirus species more efficiently than nucleotide signatures. Arch Virol 149:1941–1954

    CAS  PubMed  Google Scholar 

  29. Heinze C, Lesemann DE, Ilmberger N, Willingmann P, Adam G (2006) The phylogenetic structure of the cluster of tobamovirus species serologically related to ribgrass mosaic virus (RMV) and the sequence of streptocarpus flower break virus (SFBV). Arch Virol 151:763–774

    Article  CAS  PubMed  Google Scholar 

  30. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  CAS  PubMed  Google Scholar 

  31. Tamura K, Stecher G, Kumar S (2021) MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol 38:3022–3027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Meshi T, Ishikawa M, Motoyoshi F, Samba K, Okada Y (1986) In vitro transcription of infectious RNAs from full-length cDNA of tobacco mosaic virus. Proc Natl Acad Sci USA 83:5013–5017

    Article  Google Scholar 

  33. Hajdukiewicz P, Svab Z, Maliga P (1994) The small, versatile pPZP family of Agrobacterium binary vectors for plant transformation. Plant Mol Biol 25:989–994

    Article  CAS  PubMed  Google Scholar 

  34. Yamamoto H, Abe T, Ueda K, Inoue M, Matsumot (2002) A missense mutation in Tomato mosaic virus L11A-Fukushima genome determines its symptomless systemic infection of tomato. J Gen Plant Pathol 68:385–389

    Article  CAS  Google Scholar 

  35. Pasin F, Menzel W, Daròs JA (2019) Harnessed viruses in the age of metagenomics and synthetic biology: an update on infectious clone assembly and biotechnologies of plant viruses. Plant Biotechnol J 17:1010–1026

    Article  PubMed  PubMed Central  Google Scholar 

  36. Nagai A, Duarte LML, Chaves ALR, Peres LEP, dos Santos DYAC (2019) Tomato mottle mosaic virus in Brazil and its relationship with Tm-22 gene. Eur J Plant Pathol 155:353–359

    Article  CAS  Google Scholar 

  37. Tettey CK, Yan ZY, Ma HY, Zhao MS, Geng C, Tian YP, Li XD (2022) Tomato mottle mosaic virus: characterization, resistance gene effectiveness, and quintuplex RT-PCR detection system. J Integr Agric 21:2641–2651

    Article  CAS  Google Scholar 

  38. Kubota K, Tsuda S, Tamai A, Meshi T (2003) Tomato mosaic virus replication protein suppresses virus-targeted posttranscriptional gene silencing. J Virol 77:11016–11026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Hirai K, Kubota K, Mochizuki T, Tsuda S, Meshi T (2008) Antiviral RNA silencing is restricted to the marginal region of the dark green tissue in the mosaic leaves of Tomato mosaic virus-infected tobacco plants. J Virol 82:3250–3260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Tettey CK, Mu XQ, Ma HY, Chen XY, Geng C, Tian YP, Yan ZY, Li XD (2023) The role of different innate and environmental factors in Tm-22-mediated resistance to tomato mottle mosaic virus. Phytopathol Res 5:8

    Article  Google Scholar 

  41. Zhang S, Griffiths JS, Marchand G, Bernards MA, Wang A (2022) Tomato brown rugose fruit virus: an emerging and rapidly spreading plant RNA virus that threatens tomato production worldwide. Mol Plant Pathol 23:1262–1277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We thank the Research Center of Genetic Resources (RCGR), NARO, for providing the GCR26, GCR237, GCR236, GCR254, GCR526, and GCR267 tomato cultivars. We also thank the Biotechnology Center at Akita Prefectural University for DNA sequencing.

Funding

None.

Author information

Authors and Affiliations

  1. Department of Biological Production, Faculty of Bioresource Sciences, Akita Prefectural University, 241-438 Kaidobata-Nishi, Nakano, Shimoshinjo, Akita, 010-0195, Japan

    Tatsuya Kon, Chinami Sato & Shin-ichi Fuji

Authors
  1. Tatsuya Kon
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chinami Sato
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shin-ichi Fuji
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tatsuya Kon.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

This article does not describe any studies with human participants or animals performed by any of the authors.

Additional information

Handling Editor: Elvira Fiallo-Olivé

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

The GenBank/EMBL/DDBJ accession number for the sequence reported in this paper is LC779003 (ToMMV-SP).

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PPTX 29531 KB)

Supplementary file2 (DOCX 16 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kon, T., Sato, C. & Fuji, Si. Molecular characterization and host reaction to tomato mottle mosaic virus isolated from sweet pepper seeds in Japan. Arch Virol 169, 113 (2024). https://doi.org/10.1007/s00705-024-06035-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00705-024-06035-1

Search

Navigation