Applied Biochemistry and Microbiology

, Volume 55, Issue 1, pp 41–47 | Cite as

Strains of Bacillus spp. Regulate Wheat Resistance to Greenbug Aphid Schizaphis graminum Rond.

  • S. V. VeselovaEmail author
  • G. F. Burkhanova
  • S. D. Rumyantsev
  • D. K. Blagova
  • I. V. Maksimov


It has been found that the bacteria Bacillus subtilis Cohn. (strain 26 D) and Bacillus thuringiensis Berliner (strains V-6066 and V-5689) are able to suppress the vital activity of the greenbug aphid Schizaphis graminum Rond. The protective effects of the studied Bacillus spp. strains consisted of direct aphicidal activity, and they indirectly induce systemic resistance in wheat plants via the regulation of hydrogen peroxide generation, the activity of peroxidase and catalase, and an increased expression of defense-related genes, such us NADPH oxidases, PR-6, and PR-9. It has been shown that B. thuringiensis strains induced genes of the jasmonate-dependent signaling pathway, and B. subtilis strain induced genes of the salicylate-dependent signaling pathway. It has been found that the composition of the studied Bacillus spp. strains had an additive effect of wheat plant resistance to pests. These results support the use of these Bacillus spp. strains as a basis for the further development of a biopreparation against cereal aphids.


Bacillus subtilis Bacillus thuringiensis Schizaphis graminum Triticum aestivum L. induced systemic resistance redox metabolism defense-related genes 



  1. 1.
    Morkunas, I., Mai, V.C., and Gabrys, B., Acta Physiol. Plant., 2011, vol. 33, no. 6, pp. 2057–2073.CrossRefGoogle Scholar
  2. 2.
    Koch, K.G., Chapman, K., Louis, J., Heng-Moss, T., and Sarath, G., Front. Plant Sci., 2016, vol. 7, p. 1363.CrossRefGoogle Scholar
  3. 3.
    Burkhanova, G.F., Veselova, S.V., Sorokan’, A.V., Blagova, D.K., Nuzhnaya, T.V., and Maksimov, I.V., Appl. Biochem. Microbiol., 2017, vol. 53, no. 3, pp. 346–352. doi CrossRefGoogle Scholar
  4. 4.
    Araújo, E.O., Afr. J. Plant Sci., 2015, vol. 9, no. 9, pp. 368–373.CrossRefGoogle Scholar
  5. 5.
    Maksimov, I.V., Veselova, S.V., Nuzhnaya, T.V., Sarvarova, E.R., and Khairullin, R.M., Russ. J. Plant Physiol., 2015, vol. 62, no. 6, pp. 715–726.CrossRefGoogle Scholar
  6. 6.
    Pieterse, C.M., Zamioudis, C., Berendsen, R.L., Weller, D.M., van Wees, S.C., and Bakker, P.A., Annu. Rev. Phytopathol., 2014, vol. 52, pp. 347–375.CrossRefGoogle Scholar
  7. 7.
    Rashid, M.H. and Chung, Y.R., Front. Plant Sci., 2017, vol. 8, p. 1816. doi CrossRefGoogle Scholar
  8. 8.
    Yang, S.Y., Lim, D.J., Noh, M.Y., Kim, J.C., Kim, Y.C., and Kim, I.S., Entomol. Res., 2017, vol. 47, no. 1, pp. 55–59. doi CrossRefGoogle Scholar
  9. 9.
    Roh, J.Y., Choi, J.Y., Li, M.S., Jin, B.R., and Je, Y.H., J. Microbiol. Biotechnol., 2007, vol. 17, no. 4, pp. 547–559.Google Scholar
  10. 10.
    Porcar, M., Grenier, A.M., Federici, B., and Rahbe, Y., Appl. Environ. Microbiol., 2009, vol. 75, pp. 4897–4900.CrossRefGoogle Scholar
  11. 11.
    Hyakumachi, M., Nishimura, M., Arakawaa, T., Asano, Sh., Yoshida, Sh., Tsushima, S., and Takahashi, H., Microbes Environ., 2013, vol. 28, no. 1, pp. 128–134.CrossRefGoogle Scholar
  12. 12.
    Melatti, V.M., Praca, L.B., Martins, E.S., Sujii, E., Berry, C., and Monnerat, R.G., BioAssay, 2010, vol. 5, pp. 1–4.Google Scholar
  13. 13.
    Valenzuela-Soto, J.H., Estrada-Hernandez, M.G., Ibarra-Laclette, E., and Delano-Frier, J.P., Planta, 2010, vol. 231, pp. 397–410. doi CrossRefGoogle Scholar
  14. 14.
    Pangesti, N., Pineda, A., Pieterse, C.M., Dicke, M., and van Loon, J.J., Front. Plant Sci., 2013, vol. 4, p. 414. doi CrossRefGoogle Scholar
  15. 15.
    RF Patent no. 265469, 2018.Google Scholar
  16. 16.
    Radchenko, E.E., Cereal aphids, in Izuchenie geneticheskikh resursov zernovykh kul’tur po ustoichivosti k vrednym organizmam. Metodicheskoe posobie (The Study of the Genetic Resources of Crops by Their Pest Resistance: Manual), Moscow: Rossel’khozakademiya, 2008, pp. 214–257.Google Scholar
  17. 17.
    Veselova, S.V., Burkhanova, G.F., Nuzhnaya, T.V., and Maksimov, I.V., Russ. J. Plant Physiol., 2016, vol. 63, no. 5, pp. 609–619.CrossRefGoogle Scholar
  18. 18.
    Giovanini, M.P., Puthoff, D.P., Nemacheck, J.A., Mittapalli, O., Saltzmann, K.D., Ohm, H.W., Shukle, R.H., and Williams, C.E., Mol. Plant Microbe Interact., 2006, vol. 19, no. 9, pp. 1023–1033.CrossRefGoogle Scholar
  19. 19.
    Adhikari, T.B., Balaji, B., Breeden, J.D., and Goodwin, S.B., Physiol. Mol. Plant Pathol., 2007, vol. 71, pp. 56–68.CrossRefGoogle Scholar
  20. 20.
    Burkhanova, G.F., Yarullina, L.G., and Maksimov, I.V., Russ. J. Plant Physiol., 2007, vol. 54, no. 1, pp. 104–110.CrossRefGoogle Scholar
  21. 21.
    Gimenez, M.J., Piston, F., and Atienza, S.G., Planta, 2011, vol. 233, pp. 163–173.CrossRefGoogle Scholar
  22. 22.
    Zimmerman, C., Klein, K.C., Kiser, P.K., Singh, A.R., Firestein, B.L., Riba, S.C., and Lingappa, J.R., Nature, 2002, vol. 415, no. 6867, pp. 88–92.CrossRefGoogle Scholar
  23. 23.
    Monerrat, R.G., Soares, C.M., Capdeville, G., Jones, G., Soares, M.E., Praca, L., Cordeiro, B.A., Braz, S.V., Dos, SantosR.C., and Berry, C., Microbial. Biotechnol., 2009, vol. 2, pp. 512–520.CrossRefGoogle Scholar
  24. 24.
    Chougule, N.P. and Bonning, B.C., Toxins, 2012, vol. 4, pp. 405–429.CrossRefGoogle Scholar
  25. 25.
    Zebelo, S., Song, Y., Kloepper, J.W., and Fadamiro, H., Plant, Cell Environ., 2016, vol. 39, pp. 935–943.CrossRefGoogle Scholar
  26. 26.
    Rashid, M.H., Khan, A., Hossain, M.T., and Chung, Y.R., Front. Plant Sci., 2017, vol. 8, p. 211. doi Google Scholar
  27. 27.
    Burkhanova, G.F., Cherepanova, E.A., Blagova, D.K., and Maksimov, I.V., in Rasteniya i mikroorganizmy: biotekhnologiya budushchego. Materialy mezhd. nauchn. konf. PLAMIC 2018 (Plants and Microorganisms: Biotechnology of the Future. Proc. Int. Sci. Conf. PLAMIC 2018), Ufa, 2018, p. 15.Google Scholar
  28. 28.
    Lei, J. and Zhu-Salzman, K., Plant Signal. Behav., 2015, vol. 10, no. 4. e1010936.Google Scholar
  29. 29.
    Moloi, M.J. and van der Westhuizen, A.J., J. Plant Physiol., 2006, vol. 163, no. 11, pp. 1118–1125.CrossRefGoogle Scholar
  30. 30.
    Zhu-Salzman, K., Salzman, R.A., Ahn, J.-E., and Koiwa, H., Plant Physiol., 2004, vol. 134, pp. 420–431.CrossRefGoogle Scholar
  31. 31.
    Ahn, I.P., Lee, S.W., Kim, M.G., Park, S.R., Hwang, D.J., and Ba, S.C., Mol. Cells, 2011, vol. 32, pp. 7–14.CrossRefGoogle Scholar
  32. 32.
    Veselova, S.V., Nuzhnaya, T.V., and Maksimov, I.V., in Jasmonic Acid: Biosynthesis, Functions and Role in Plant Development. Ch. 3., Morrison, L., Ed., N.Y.: Nova Sci. Publ, 2015, pp. 33–66.Google Scholar
  33. 33.
    Kerchev, P.I., Fenton, B., Foyer, C.H., and Hancock, R.D., Plant, Cell Environ., 2012, vol. 35, pp. 441–453.CrossRefGoogle Scholar
  34. 34.
    Van Loon, L.C., Rep, M., and Pieterse, C.M., Annu. Rev. Phytopathol., 2006, vol. 44, pp. 135–162.CrossRefGoogle Scholar
  35. 35.
    Almagro, L., Gomez, RosL.V., Belchi-Navarro, S., Bru, R., Ros Barcello, A., and Pedreno, M.A., J. Exp. Bot., 2009, vol. 60, pp. 377–390.CrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Inc. 2019

Authors and Affiliations

  • S. V. Veselova
    • 1
    Email author
  • G. F. Burkhanova
    • 1
  • S. D. Rumyantsev
    • 1
  • D. K. Blagova
    • 1
  • I. V. Maksimov
    • 1
  1. 1.Institute of Biochemistry and Genetics, Ufa Federal Research Center, Russian Academy of SciencesUfaRussia

Personalised recommendations