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Defense response mechanisms of ginseng callus cultures induced by Yersinia pseudotuberculosis, a human pathogen

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Abstract

The effect of Yersinia pseudotuberculosis, the bacterial pathogen affecting humans and animals, on growth of ginseng (Panax ginseng C.A. Mey) cell cultures was studied. The bacteria strongly induced the expression of phenylalanine ammonia-lyase and β-1,3-glucanase, the proteins encoded by the defense-related genes of ginseng and inhibited the normal ginseng callus growth but did not affect the resistant cell cultures. The thermostable and thermolabile protein toxins of these bacteria are lethal to mice when induced parentherally, and they also induced the expression of the defense-related genes in ginseng callus cultures. At the same time, the ginseng cells completely suppressed the bacterial cell growth. These data suggest that the ginseng cells recognized the yersinia and developed the immune response to this pathogen. The interaction between the ginseng cells and Y. pseudotuberculosis is similar to the hypersensitive response of plants to plant pathogens.

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Abbreviations

Avr:

avirulence

CFU:

colony-forming unit

HR:

hypersensitive response

hrp :

hypersensitive response and pathogenicity genes

PAL:

phenylalanine ammonia-lyase

Pgglu1:

Panax ginseng β-1,3-glucanase

PgPAL:

P. ginseng PAL

TLTYp:

thermolabile toxin of Yersinia pseudotuberculosis

TSTYp:

thermostable toxine of Y. pseudotuberculosis

Yop:

Yersinia outer protein

References

  1. Rozhkova, L.P. and Sharapova, T.A., Further Inquiry of Far-East Scarlet-Like Fever, Dal’nevostochnaya skarlatinopodobnaya likhoradka (psevdotuberkulez cheloveka) (Far-East Scarlet-Like Fever(Human Pseudotuberculosis)), Somov, G.P., Ed., Leningrad: Poligraficheskii Kombinat “Rotaprint”, 1978, pp. 13–24.

    Google Scholar 

  2. Somov, G.P., Varvashevich, T.N., and Timchenko, N.F., Psikhrofil’nost’ patogennykh bakterii (Psychrophilic Pity Pathogenic Bacteria), Moscow: Nauka, Sibirskoe Otdelenie, 1991.

    Google Scholar 

  3. Kuznetsov, V.G. and Bagryantsev, V.N., Ecology of Yersinia and Yersiniosis, Okruzhayushchaya sreda i zdorov’e naseleniya Vladivostoka (Environment and the Health of Vladivostok Inhabitants), Kosolapov, A.B. and Preobrazhenskii, B.V., Eds., Vladivostok: Dal’nauka, 1998, pp. 154–164.

    Google Scholar 

  4. Somov, G.P., Dal’nevostochnaya skarlatinopodobnaya likhoradka (Far-East Scarlet-Like Fever), Moscow: Meditsina, 1979.

    Google Scholar 

  5. Gordeiko, V.A. and Shustrova, N.M., Yersinia in Plants, Zh. Mikrobiol., Epidemiol. Immun., 1990, no. 11, pp. 16–18.

  6. Markova, Yu.A., Romanenko, A.S., Igumnova, E.K., and Salyaev, R.K., Plants as Possible Reservoirs for Bacterial Pathogens of Human and Animals, Dokl. Akad. Nauk, 2002, vol. 386, pp. 277–279.

    Google Scholar 

  7. Shustrova, N.M., Misurenko, E.N., and Litvin, V.Yu., Possible Transfer of Yersinia pseudotuberculosis by Chain Soil-Plant-Animal, Zh. Mikrobiol., Epidemiol. Immun., 1992, no. 4, pp. 10–12.

  8. Litvin, V.Yu., Gintsburg, A.L., Pushkareva, V.I., Romanova, Yu.M., and Boev, B.V., Epidemiologicheskie aspekty ekologii bakterii (Epidemiological Aspects of Bacterial Ecology), Moscow: Farmus-print, 1998.

    Google Scholar 

  9. Markova, Yu.A., Romanenko, A.S., Klimov, V.T., and Chesnokova, M.V., Relationships of Yersinia pseudotuberculosis and Potato Plants In Vitro, Zh. Stress. Fiziol. Biokh., 2006, vol. 2, no. 1, pp. 22–27.

    Google Scholar 

  10. Baker, B., Zambryski, P., Staskawicz, B., and Dinesh-Kumar, S.P., Signaling in Plant-Microbe Interactions, Science, 1997, vol. 276, pp. 726–733.

    Article  PubMed  CAS  Google Scholar 

  11. Rahme, L.G., Ausubel, F.M., Cao, H., Drenkard, E., Goumnerov, B.C., Lau, G.W., Mahajan-Miklos, S., Plotnikova, J., Tan, M., Tsongalis, J., Walendziewicz, C.L., and Tompkins, R.G., Plants and Animals Share Functionally Common Bacterial Virulence Factors, Proc. Natl. Acad. Sci. USA, 2000, vol. 97, pp. 8815–8821.

    Article  PubMed  CAS  Google Scholar 

  12. Staskawicz, B.J., Mudgett, M.B., Dangl, J.L., and Galan, J.E., Common and Contrasting Themes of Plant and Animal Disease, Science, 2001, vol. 292, pp. 2285–2289.

    Article  PubMed  CAS  Google Scholar 

  13. Hammond-Kosack, K.E. and Jones, J.D.G., Resistance Gene-Dependent Plant Defense Responses, Plant Cell, 1996, vol. 8, pp. 1773–1791.

    Article  PubMed  CAS  Google Scholar 

  14. Scofield, S.R., Tobias, Ch.M., Rathjen, J.P., Chang, J.H., Lavelle, D.T., Michelmore, R.W., and Staskawicz, B.J., Molecular Basis of Gene-for-Gene Specificity in Bacterial Speck Disease of Tomato, Science, 1996, vol. 274, pp. 2063–2065.

    Article  PubMed  CAS  Google Scholar 

  15. Orth, K., Xu, Z., Mudgett, M.B., Bao, Z.Q., Palmer, L.E., Bliska, J.B., Mangel, W.F., Staskawicz, B.J., and Dixon, J.E., Disruption of Signaling by Yersinia Effector YopJ, a Ubiquitin-Like Protein Protease, Science, 2000, vol. 290, pp. 1594–1597.

    Article  PubMed  CAS  Google Scholar 

  16. Timchenko, N.F., Bulgakov, V.P., Bulakh, E.V., Yasnetskaya, E.G., and Zhuravlev, Yu.N., Relationships between Yersinia, Listeria, and Salmonella and Plant Cells, Zh. Mikrobiol., Epidemiol. Immun., 2000, no. 1, pp. 6–10.

  17. Timchenko, N., Eliseikina, M., Bulgakov, V., Bulakh, E., Yasnetskaya, E., Nedashkovskaya, E., and Zhuravlev, Yu., Yersinia pseudotuberculosis, Its Toxins and Plant Cells, Adv. Exp. Med. Biol., 2003, vol. 529, pp. 169–171.

    Article  PubMed  Google Scholar 

  18. Bulgakov, V.P., Kozyrenko, M.M., Fedoreyev, S.A., Mishenko, N.P., Denisenko, V.A., Zvereva, L.V., Pokushalova, T.V., and Zhuravlev, Yu.N., Shikonin Production by p-Fluorophenylalanine-Resistant Cells of Lithospermum erythrorhizon, Fitoterapia, 2001, vol. 72, pp. 394–401.

    Article  PubMed  CAS  Google Scholar 

  19. Alfano, J.R. and Collmer, A., Bacterial Pathogens in Plants: Life up against the Wall, Plant Cell, 1996, vol. 8, pp. 1683–1698.

    Article  PubMed  CAS  Google Scholar 

  20. Bulgakov, V.P., Khodakovskaya, M.V., Labetskaya, N.V., Chernoded, G.K., and Zhuravlev, Yu.N., The Impact of Plant rolC Oncogene on Ginsenoside Production by Ginseng Hairy Root Cultures, Phytochemistry, 1998, vol. 49, pp. 1929–1934.

    Article  CAS  Google Scholar 

  21. Kiselev, K.V., Kusaykin, M.I., Dubrovina, A.S., Bezverbny, D.A., Zvyagintseva, T.N., and Bulgakov, V.P., The rolC Gene Induces Expression of a Pathogenesis Related β-1,3-Glucanase in Transformed Ginseng Cells, Phytochemistry, 2006, vol. 67, pp. 2225–2231.

    Article  PubMed  CAS  Google Scholar 

  22. Timchenko, N.F., Nedashkovskaya, E.P., Dolmatova, L.S., and Somova-Isachkova, L.M., Toksiny Yersinia rseudotubersulosis (Yersinia pseudotuberculosis Toxins), Vladivostok: Primorskii Poligrafkombinat, 2004.

    Google Scholar 

  23. Bradford, M.M., A Rapid and Sensitive Method for the Quantitation of Microgram Quantites of Protein Utilizing the Principle of Protein-Dye Binding, Anal. Biochem., 1976, vol. 86, pp. 248–254.

    Article  Google Scholar 

  24. Yasnetskaya, E.G., Bulgakov, V.P., Gorbach, V.I., Shevchenko, N.M., Fedoreeva, L.I., Zhuravlev, Yu.N., and Kiselev, K.V., Ethephon-and Jasmonate-Elicited Pathogenesis-Related Ribonucleases in Cultured Ginseng Cells, Russ. J. Plant Physiol., 2003, vol. 50, pp. 554–560.

    Article  Google Scholar 

  25. Gorpenchenko, T.Y., Kiselev, K.V., Bulgakov, V.P., Tchernoded, G.K., Bragina, E.A., Khodakovskaya, M.V., Koren, O.G., Batygina, T.B., and Zhuravlev, Yu.N., The Agrobacterium rhizogenes rolC-Gene-Induced Somatic Embryogenesis and Shoot Organogenesis in Panax ginseng Transformed Calluses, Planta, 2006, vol. 223, pp. 457–467.

    Article  PubMed  CAS  Google Scholar 

  26. Bulgakov, V.P., Veselova, M.V., Tchernoded, G.K., Kiselev, K.V., Fedoreyev, S.A., and Zhuravlev, Yu.N., Inhibitory Effect of the Agrobacterium rhizogenes rolC Gene on Rabdosiin and Rosmarinic Acid Production in Eritrichium sericeum and Lithospermum erythrorhizon Transformed Cell Cultures, Planta, 2005, vol. 221, pp. 471–478.

    Article  PubMed  CAS  Google Scholar 

  27. Kiselev, K.V., Gorpenchenko, T.Y., Tchernoded, G.K., Dubrovina, A.S., Grishchenko, O.V., Bulgakov, V.P., and Zhuravlev, Yu.N., Calcium-Dependent Mechanism of Somatic Embryogenesis in Panax ginseng Cell Cultures Expressing the rolC Oncogene, Mol. Biol., 2008, vol. 42, pp. 275–285.

    Article  CAS  Google Scholar 

  28. Cramer, C.L., Edwards, K., Dron, M., Liang, X., Dildine, S.L., Bolwell, G.P., Dixon, R.A., Lamb, C.J., and Schuch, W., Phenylalanine Ammonia-Lyase Gene Organization and Structure, Plant Mol. Biol., 1989, vol. 12, pp. 367–383.

    Article  CAS  Google Scholar 

  29. Zhu, M., Shao, F., Innes, R.W., Dixon, J.E., and Xu, Z., The Crystal Structure of Pseudomonas Avirulence Protein AvrPphB: A Papain-Like Fold with a Distinct Substrate-Binding Site, Proc. Natl. Acad. Sci. USA, 2004, vol. 101, pp. 302–307.

    Article  PubMed  CAS  Google Scholar 

  30. Hueck, C.J., Type III Protein Secretion Systems in Bacterial Pathogens of Animals and Plants, Microbiol. Mol. Biol. Rev., 1998, vol. 62, pp. 379–433.

    PubMed  CAS  Google Scholar 

  31. Kunik, T., Tzfira, T., Kapulnik, Y., Gafni, Y., Dingwall, C., and Citovsky, V., Genetic Transformation of HeLa Cells by Agrobacterium, Proc. Natl. Acad. Sci. USA, 2001, vol. 98, pp. 1871–1876.

    Article  PubMed  CAS  Google Scholar 

  32. Lacroix, B., Tzfira, T., Vainstein, A., and Citovsky, V., A Case of Promiscuity: Agrobacterium’s Endless Hunt for New Partners, Trends Genet., 2006, vol. 22, pp. 29–37.

    Article  PubMed  CAS  Google Scholar 

  33. Bulgakov, V.P., Kiselev, K.V., Yakovlev, K.V., Zhuravlev, Yu.N., Gontcharov, A.A., and Odintsova, N.A., Agrobacterium-Mediated Transformation of Sea Urchin Embryos, Biotechnol. J., 2006, vol. 1, pp. 454–461.

    Article  PubMed  CAS  Google Scholar 

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Correspondence to E. V. Persiyanova.

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Original Russian Text © E.V. Persiyanova, K.V. Kiselev, V.P. Bulgakov, N.F. Timchenko, G.K. Chernoded, Yu.N. Zhuravlev, 2008, published in Fiziologiya Rastenii, 2008, Vol. 55, No. 6, pp. 834–841.

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Persiyanova, E.V., Kiselev, K.V., Bulgakov, V.P. et al. Defense response mechanisms of ginseng callus cultures induced by Yersinia pseudotuberculosis, a human pathogen. Russ J Plant Physiol 55, 748–755 (2008). https://doi.org/10.1134/S1021443708060034

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  • DOI: https://doi.org/10.1134/S1021443708060034

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