Abstract
Generation of reactive oxygen species (ROS) in tobacco (Nicotiana tabacum L.) cell cultures and potato (Solanum tuberosum L.) of two varieties experiencing the action of bacterial pathogen Clavibacter michiganensis ssp. sepedonicus (Cms) was investigated. The intensity and dynamics of the changes in hydrogen peroxide concentration observed in these cultures provided evidence for the development in tobacco of the effector-activated immune responses and the induction of the same type of responses but with low intensity for resistant potato variety and the inhibition of the defense mechanisms for its susceptible variety. This is in accordance with the data concerning the dynamics of plant cell culture death as well as the results obtained earlier on the whole plants. The experiments performed had also the purpose to elucidate whether the development of the above responses on the ability of bacteria Cms to form biofilms during plant infection. It was shown that this ability of Cms is significantly inhibited upon the combined cultivation of it with the plant cells exerting the responses of the effector-activated immunity and represented by the cells of tobacco and resistant potato variety. In the case of susceptible potato variety, the process of the biofilm formation was suppressed by the plant only to a slight extent. In addition, the fact concerning the participation of heat shock proteins (HSPs) in the development of the effector-activated immune responses was revealed.
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Abbreviations
- CF:
-
cell free culture filtrate
- Cms :
-
Clavibacter michiganensis ssp. sepedonicus
- DC:
-
bacterial dead culture
- ETI:
-
effectors-triggered immunity
- HR:
-
hypersensitivity reaction
- HSP:
-
heat shock proteins
- MAMP:
-
microbial-associated molecular patterns
- PTI:
-
patterns-triggered immunity
- ROS:
-
reactive oxygen species
- SAR:
-
system acquired resistance
References
Jones, J.D.G. and Dangl, J.L., The plant immune system, Nature, 2006, vol. 444, pp. 323–329.
Shafikova, T.N. and Omelichkina, Yu.V., Molecular–genetic aspects of plant immunity to phytopathogenic bacteria and fungi, Russ. J. Plant Physiol., 2015, vol. 62, pp. 571–585.
Xu, Z.S., Li, Z.Y., Chen, Y., Chen, M., Li, L.C., and Ma, Y.Z., Heat shock protein 90 in plants: molecular mechanisms and roles in stress responses, Int. J. Mol. Sci., 2012, vol. 13, pp. 15 706–15 723.
Wang, Y., Lin, S., Song, Q., Li, K., Tao, H., Huang, J., Chen, X., Que, S., and He, H., Genome-wide identification of heat shock proteins (Hsps) and Hsp interactors in rice: Hsp70s as a case study, BMC Genomics, 2014, vol. 15, p. 344.
Lee, A.H.Y., Middleton, M.A., Guttman, D.S., and Desveaux, D., Phytopathogen type III effectors as probes of biological systems, Microbiol. Biotechnol., 2013, vol. 6, pp. 230–240.
Donlan, R.M., Biofilms: microbial life on surfaces, Emerg. Infect. Dis., 2002, vol. 8, no. 9, pp. 881–890.
Mansfield, J., Genin, S., Magori, S., Citovsky, V., Sriariyanum, M., Ronald, P., Dow, M., Verdier, V., Beer, S.V., Machado, M.A., Toth, I., Salmond, G., and Foster, G.D., Top 10 plant pathogenic bacteria in molecular plant pathology, Mol. Plant Pathol., 2012, vol. 13, pp. 614–629.
Bae, Y.M., Zheng, L., Hyun, J.E., Jung, K.S., Heu, S., and Lee, S.Y., Growth characteristics and biofilm formation of various spoilage bacteria isolated from fresh produce: growth and biofilm of spoilage bacteria, J. Food Sci., 2014, vol. 79, no. 10, pp. M2072–M2080.
Murashige, T. and Skoog, F., A revised medium for rapid growth and bioassays with tobacco tissue cultures, Physiol. Plant., 1962, vol. 15, pp. 473–497.
Maximova, L.A., Nurminskaya, J.V., Kopytina, T.V., and Enikeev, A.G., Agrobacterium-mediated transformation of Nicotiana tabacum by disarmed strain at 699 resulted in considerable raising of growth and development of transgenic plants, J. Stress Physiol. Biochem., 2012, vol. 8, pp. 138–148.
Enikeev, A.G., Vysotskaya, E.F., Leonova, L.A., and Gamburg, K.Z., Viability assay with 2,3,5,-triphenyltetrazolium chloride in plant cell cultures, Russ. J. Plant Physiol., 1995, vol. 42, pp. 372–375.
Bindschedler, L.V., Minibayeva, F., Gardner, S.L., Gerrish, C., Davies, D.R., and Bolwell, G.P., Early signalling events in the apoplastic oxidative burst in suspension cultured French bean cells involve cAMP and Ca2+, New Phytol., 2001, vol. 151 P, pp. 185–194.
Merritt, J.H., Kadouri, D.E., and O’Toole, G.A., Growing and analyzing static biofilms, Curr. Protoc. Microbiol., 2005, ch. 1, pp. 1B.1.1–1B.1.18. doi 10.1002/9780471729259.mc01b01s00
Omelichkina, Yu.V., Shafikova, T.N., Rikhvanov, E.G., Enikeev, A.G., and Romanenko, A.S., The action of causal agent of potato ring rot in the suspension culture cells of tobacco and potato, Izv. Irkutsk Gos. Univ., Ser. Biologiya, Ekol., 2008, vol. 1, pp. 89–94.
Shafikova, T.N., Omelichkina, Yu.V., Soldatenko, A.S., Enikeev, A.G., Kopytina, T.V., Rusaleva, T.M., and Volkova, O.D., Tobacco cell cultures transformed by the hsp 101 gene exhibit an increased resistance to potassium fluoride, Dokl. Biol. Sci., 2010, vol. 430, pp. 29–30.
Marques, L.L.R., de Boer, S.H., Ceri, H., and Olson, M.E., Evaluation of biofilms formed by Clavibacter michiganensis subsp. sepedonicus, Phytopathology, 2003, vol. 93, no. 6 (suppl.): S57.
Boyarkina, S.V., Omelichkina, Yu.V., and Shafikova, T.N., The use of PCR in the diagnosis of potato ring rot pathogen, Izv. Irkutsk Gos. Univ., Ser. Biol., Ekol., 2008, vol. 1, no. 2, pp. 41–44.
Perfil'eva, A.I., Rymareva, E.V., and Rikhvanov, E.G., Influence of monoiodine acetate sodium and heat treatment on potato plant productivity in pot and field experiments, Agrochemistry, 2013, vol. 6, pp. 40–46.
Shkalikov, V.A., D’yakov, Yu.T., and Smirnov, A.N., Immunitet rastenii (Plant Immunity), Moscow: Kolos, 2005.
Mur, L.A.J., Kenton, P., Lloyd, A.J., Ougham, H., and Prats, E., The hypersensitive response; the centenary is upon us but how much do we know? J. Exp. Bot., 2008, vol. 59, pp. 501–520.
Omelichkina, Yu.V., Shafikova, T.N., Alekseenko, A.L., Markova, Yu.A., Enikeev, A.G., and Rikhvanov, E.G., Responses of tobacco plants and cell cultures on the Clavibacter michiganensis ssp. sepedonicus infection, World Sci. Discovery, 2010, no. 1–4, pp. 89–94.
Omelichkina, Y.V., Boyarkina, S.V., and Shafikova, T.N., Induction of systemic acquired resistance of plants by exometabolites of causal agent of potato ring rot, World Sci. Discovery, 2014, no. 10 (58), pp. 156–167.
Collmer, A., Schneider, D.J., and Lindeberg, M., Lifestyles of the effector rich: genome-enabled characterization of bacterial plant pathogens, Plant Physiol., 2009, vol. 150, pp. 1623–1630.
Bouarab, K., Melton, R., Peart, J., Baulcombe, D., and Osbourn, A., A saponin-detoxifying enzyme mediates suppression of plant defences, Nature, 2002, vol. 418, pp. 889–892.
Monteiro-Vitorello, C.B., Camargo, L.E.A., van Sluys, M.A., Kitajima, J.P., Truffi, D., Wood, D., Marino, C.L., and Menck, C.F., The genome sequence of the gram-positive sugarcane pathogen Leifsonia xyli subsp. xyli, Mol. Plant–Microbe Interact., 2004, vol. 17, pp. 827–836.
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Original Russian Text © Yu.V. Omelichkina, S.V. Boyarkina, T.N. Shafikova, 2017, published in Fiziologiya Rastenii, 2017, Vol. 64, No. 3, pp. 204–212.
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Omelichkina, Y.V., Boyarkina, S.V. & Shafikova, T.N. Effector-activated immune responses in potato and tobacco cell cultures caused by phytopathogen Clavibacter michiganensis ssp. sepedonicus . Russ J Plant Physiol 64, 423–430 (2017). https://doi.org/10.1134/S1021443717020091
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DOI: https://doi.org/10.1134/S1021443717020091