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Atmospheric-pressure plasma irradiation can disrupt tobacco mosaic virus particles and RNAs to inactivate their infectivity

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Abstract

Low-temperature atmospheric-pressure air plasma is a source of charged and neutral gas species. In this study, N-carrying tobacco plants were inoculated with plasma irradiated and non-irradiated tobacco mosaic virus (TMV) solution, resulting in necrotic local lesions on non-irradiated, but not on irradiated, TMV-inoculated leaves. Virus particles were disrupted by plasma irradiation in an exposure-dependent manner, but the viral coat protein subunit was not. TMV RNA was also fragmented in a time-dependent manner. These results indicate that plasma irradiation of TMV can collapse viral particles to the subunit level, degrading TMV RNA and thereby leading to a loss of infectivity.

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References

  1. Aboubakr HA, Gangal U, Youssef MM, Goyal SM, Bruggeman PJ (2016) Inactivation of virus in solution by cold atmospheric pressure plasma: identification of chemical inactivation pathways. J Phys D Appl Phys 49:204001

    Article  CAS  Google Scholar 

  2. Antoniw JF, White RF (1986) Changes with time in the distribution of virus and PR protein around single local lesions of TMV infected tobacco. Plant Mol Biol 6:145–149

    Article  PubMed  CAS  Google Scholar 

  3. Baker C, Adkins S (2000) Peppers, Tomatoes, and Tobamoviruses. Plant Pathol Circular No. 400

  4. Graves DB (2012) The emerging role of reactive oxygen and nitrogen species in redox biology and some implications for plasma applications to medicine and biology. J Phys D Appl Phys 45:263001

    Article  CAS  Google Scholar 

  5. Hayashi N, Yagyu Y, Yonesu A, Shiratani M (2014) Sterilization characteristics of the surfaces of agricultural products using active oxygen species generated by atmospheric plasma and UV light. Jpn J. Appl Phys. 53:05FR03-1-05FR03-5

    Google Scholar 

  6. Haramoto E, Kitajima M, Kishida N, Konno Y, Katayama H, Asami M, Akiba M (2013) Occurrence of Pepper mild mottle virus in drinking water sources in Japan. Appl Environ Microbiol 79:7413–7418

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Hebert TT (1963) Precipitation of plant viruses by polyethylene glycol. Phytopathology 53:362

    Google Scholar 

  8. ICTVdb Management. 00.071.0.01.007 (2006) Pepper mild mottle virus. In: ICTVdb—The Universal Virus Database, version 4 Buchen-Osmond C, ed. Columbia University: New York, USA

  9. Ikegashira Y, Ohki T, Ichiki UT, Higashi T, Hagiwara K, Omura T, Honda Y, Tsuda S (2004) An immunological system for the detection of Pepper mild mottle virus in soil from green pepper fields. Plant Dis 88:650–656

    Article  Google Scholar 

  10. Ishihara T, Takahashi H, Hase S, Sato T, Ikegami M, Ehara Y (2002) Ultrastructure of necrotic lesions in Nicotiana glutinosa leaves locally infected with a variant of Cucumber mosaic virus. J Phytopathol 150:553–556

    Article  Google Scholar 

  11. Konishi H, Takashima K, Kato T, Kaneko T, Inawashiro S, Seo N (2014) Sterilization effects of reactive species in atmospheric air plasma on plant pathogenic fungi. Proc. Plasma Conf, Nigata, Japan. 19aD1-3 (Abstract in English)

  12. Laroussi M, Alexeff I, Kang WL (2000) Biological decontamination by nonthermal plasmas. IEEE Transact Plasma Sci 28:184–188

    Article  Google Scholar 

  13. Luo Q-Z, D’Angelo N, Merlino RL (1998) Shock formation in a negative ion plasma. Phys Plasma 5:2868–2870

    Article  CAS  Google Scholar 

  14. Lu Q, Liu D, Song Y, Zhou R, Niu J (2014) Inactivation of the tomato pathogen Cladosporium fulvum by an atmospheric-pressure cold plasma jet. Plasma Proc Polymers 11:1028–1036

    Article  CAS  Google Scholar 

  15. Muller F (2000) The nature and mechanism of superoxide production by the electron transport chain: Its relevance to aging. J Amer Aging Association 23:227–253

    CAS  Google Scholar 

  16. Ochi A, Konishi H, Ando S, Sato K, Yokoyama K, Tsushima S, Yoshida S, Morikawa T, Kaneko T, Takahashi H (2017) Management of bakanae and bacterial seedling blight diseases in nurseries by irradiating rice seeds with atmospheric plasma. Plant Pathol 66:67–76

    Article  CAS  Google Scholar 

  17. Sakudo A, Shimizu N, Imanishi Y, Ikuta K (2013) N2 Gas plasma inactivates Influenza virus by inducing changes in viral surface morphology, protein, and genomic RNA. BioMed Res International. Article ID 694269

  18. Sambrook J, Russell DW (2001) Molecular Cloning: A Laboratory Manual, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  19. Sasaki S, Kanzaki M, Kaneko T (2014) Highly efficient and minimally invasive transfection using time-controlled irradiation of atmospheric-pressure plasma. Appl Phys Express. 7:026202.1-4

    Article  CAS  Google Scholar 

  20. Sasaki S, Kanzaki M, Kaneko T (2017) Calcium influx through TRP channels induced by short-lived reactive species in plasma-irradiated solution. Sci Rep 6:25728

    Article  CAS  Google Scholar 

  21. Schuster H, Schramm G (1958) Bestimmung der biologisch wirksamen Einheit in der Ribosenucleinsäure des Tabak mosaic virus auf chemischem Wege. Z Naturforschg 13b:697–704

    Article  CAS  Google Scholar 

  22. Shimizu T, Nosenko T, Morfill GE, Sato T, Schmidt H-U, Urayama T (2010) Characterization of low-temperature microwave plasma treatment with and without UV light for disinfection. Plasma Proc Polymers 7:288–293

    Article  CAS  Google Scholar 

  23. Shirasaki N, Matsushita T, Matsui Y, Yamashita R (2018) Evaluation of the suitability of a plant virus, pepper mild mottle virus, as a surrogate of human enteric viruses for assessment of the efficacy of coagulation-rapid sand filtration to remove those viruses. Water Res 129:460–469

    Article  PubMed  CAS  Google Scholar 

  24. Takahashi H, Sukamto Sugiyama M, Karasawa A, Hase S, Ehara Y (2000) A variant of Cucumber mosaic virus is restricted to local lesions in inoculated tobacco leaves with a hypersensitive response. J Gen Plant Pathol 66:335–344

    Article  CAS  Google Scholar 

  25. Tendero C, Tixier C, Tristant P, Desmaison J, Leprince P (2006) Atmospheric pressure plasmas. Spectrochimica Acta Part B: Atomic Spectro 61:2–30

    Article  CAS  Google Scholar 

  26. Tian W, Kushner MJ (2014) Atmospheric pressure dielectric barrier discharges interacting with liquid covered tissue. J Phys D Appl Phys 47:165201

    Article  CAS  Google Scholar 

  27. Wetter C, Conti M, Altschuh D, Tabillion R, van Regenmortel MHV (1984) Pepper mild mottle virus, a Tobamovirus infecting pepper cultivars in Sicily. Phytopathology 74:405–410

    Article  Google Scholar 

  28. Wu Y, Liang Y, Wei K, Li W, Yao M, Zhang J, Grinshpun SA (2015) MS2 virus inactivation by atmospheric-pressure cold plasma using different gas carriers and power levels. Appl Environ Microbiol 81:996–1002

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Yanagawa Y, Kawano H, Kobayashi T, Miyahara H, Okino A, Mitsuhara I (2017) Direct protein introduction into plant cells using a multi-gas plasma jet. PLoS One 12:e0171942

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Zimmermann JL, Dumler K, Shimizu T, Morfill GE, Wolf A, Boxhammer V, Schlegel J, Gansbacher B, Anton M (2011) Effects of cold atmospheric plasmas on adenoviruses in solution. J Phys D Appl Phys 44:505201

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was financially supported by grants for “Scientific Research on Innovative Areas” from the Ministry of Education, Culture, Science, Sports and Technology (MEXT), Japan (grant numbers 16H06429, 16K21723, and 16H06435), and by the Japan Society for the Promotion of Science (JSPS) through the JSPS Core-to-Core Program (Advanced Research Networks) entitled “Establishment of international agricultural immunology research-core for a quantum improvement in food safety”. This work was also supported by the Egyptian Government.

Funding

This study was funded by grants for “Scientific Research on Innovative Areas” from the Ministry of Education, Culture, Science, Sports and Technology (MEXT), Japan (grant numbers 16H06429, 16K21723, and 16H06435), and by the Japan Society for the Promotion of Science (JSPS) through the JSPS Core-to-Core Program (Advanced Research Networks) entitled “Establishment of international agricultural immunology research-core for a quantum improvement in food safety”. This work was also supported by the Egyptian Government.

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Authors and Affiliations

  1. Graduate School of Agricultural Science, Tohoku University, 468-1, Aramaki-Aza- Aoba, Sendai, 980-0845, Japan

    Sara E. Hanbal, Shuhei Miyashita, Sugihiro Ando, Kumiko Ito & Hideki Takahashi

  2. Department of Virus and Phytoplasma, Plant Pathology Research Institute, Agriculture Research Center, Giza, 12619, Egypt

    Sara E. Hanbal

  3. Graduate School of Engineering, Tohoku University, 6-6-05 Aoba, Aramaki, Aoba-ku, Sendai, 980-8579, Japan

    Keisuke Takashima & Toshiro Kaneko

  4. Department of Agricultural Botany, Faculty of Agriculture, Kafrelsheikh University, Kafrelsheikh, 33516, Egypt

    Mohsen M. Elsharkawy

Authors
  1. Sara E. Hanbal
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  2. Keisuke Takashima
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Correspondence to Toshiro Kaneko or Hideki Takahashi.

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Conflict of interest

Takahashi, H. has received research grants from the Ministry of Education, Culture, Science, Sports and Technology (MEXT), Japan and the Japan Society for the Promotion of Science (JSPS). Hanbal, S.E. has received a Shuttle Research Program from the Egyptian Government. All authors declare that they have no conflict of interest.

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

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Handling Editor: Massimo Turina.

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Hanbal, S.E., Takashima, K., Miyashita, S. et al. Atmospheric-pressure plasma irradiation can disrupt tobacco mosaic virus particles and RNAs to inactivate their infectivity. Arch Virol 163, 2835–2840 (2018). https://doi.org/10.1007/s00705-018-3909-4

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  • DOI: https://doi.org/10.1007/s00705-018-3909-4

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