Skip to main content
SpringerLink
Log in

Effects of Rhizobium leguminosarum bv. viceae Strains Different in Their Symbiotic Effectiveness on Changes in cAMP and Hydrogen Peroxide Concentrations in Cells of Pea Seedlings

  • RESEARCH PAPERS
  • Published:
Russian Journal of Plant Physiology Aims and scope Submit manuscript

Abstract

Changes in hydrogen peroxide and cAMP concentrations in pea (Pisum sativum L.) seedlings inoculated with Rhizobium leguminosarum bv. viceae Frank (Rlv) were evaluated as related to a sorption rate of the bacteria. The tested bacterial strains differ in effectiveness of symbiotic nitrogen fixation. Both substances were analyzed in different growth zones of the root. Planktonic cultures of the effective RCAM 1022 strain and two ineffective highly competitive RCAM 1064 and RCAM 1065 strains were used. After 6 h postinoculation, the sorption rate of all the strains markedly differed from each other in the I–V root zones that are different in their susceptibility to Rlv infection. The sorption rate of the effective 1022 strain was the most and that of the ineffective 1065 one was the least. The effective strain increased the cAMP concentration up to 120–130% in the I–III zones, while this index remained almost as low as in the noninoculated control in the IV and V zones and epicotyl. The ineffective 1064 strain behaved similarly. Another ineffective strain, 1065, caused an inversed effect: the concentration of this signal molecule was close to the control in the I–IV zones and rose in the V zone and, especially, epicotyl. The different strains led to unequal changes in the hydrogen peroxide concentration in the root zones. Upon contact with the ineffective strains, the concentration was at the control (with RCAM 1064) or lower (with RCAM 1065) level in the I–II zones; both strains significantly decreased the H2O2 content in the III zone and slightly increased it in the IV–V zones. The effective 1022 strain significantly elevated the H2O2 concentration above the control in the I–II zones but decreased it in the III–V zones. In the epicotyl, the peroxide concentration increased mainly due to activity of the ineffective strains. Therefore, upon interaction of bacterial mutualists with their host plants, the activation of plant signaling depends on the degree of effectiveness of a particular strain and directs the interaction to the path of either mutualism or pathogenesis.

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. Gourion, B., Berrabah, F., Ratet, P., and Stacey, G., Rhizobium–legume symbioses: the crucial role of plant immunity, Trends Plant Sci., 2015, vol. 20, pp. 186–194.

    Article  CAS  PubMed  Google Scholar 

  2. Makarova, L.E. and Nurminskii, V.N., Temperature impact on localization of “free” phenolic compounds in the root tissues and deformation of root hairs in pea seedlings inoculated by Rhizobium, Cell Tissue Biol., 2005, vol. 47, pp. 519–525.

    CAS  Google Scholar 

  3. Lomovatskaya, L.A., Kuzakova, O.V., Romanenko, A.S., and Goncharova, A.M., Activities of adenylate cyclase and changes in cAMP concentration in root cells of pea seedlings infected with mutualists and phytopathogens, Russ. J. Plant Physiol., 2018, vol. 65, pp. 588–597.

    Article  CAS  Google Scholar 

  4. Vasil'eva, G.G., Glyan’ko, A.K., and Mironova, N.V., Hydrogen peroxide content and catalase activity at inoculation with root tubercle bacteria of pea seedlings with the various nodulation ability, Appl. Biochem. M-icrobiol., 2005, vol. 41, pp. 621–625.

    Article  CAS  Google Scholar 

  5. Ivanova, K.A. and Tsyganov, V.E., Defense responses during the legume–Rhizobium symbiosis: induction and suppression (review), S.-kh. Biol., 2014, pp. 3–12.

    Google Scholar 

  6. Glyan'ko, A.K., Makarova, L.E., Vasil’eva, G.G., and Mironova, N.V., Possible involvement of hydrogen peroxide and salicylic acid in legume–Rhizobium symbiosis, Izv. Akad. Nauk, Ser. Biol., 2005, pp. 300–305.

  7. Terakado, I., Fujihara, S., and Yoneyama, T., Changes in cyclic nucleotides during nodule formation, Soil Sci. Plant Nutr., 2003, vol. 49, pp. 459–462.

    Article  CAS  Google Scholar 

  8. Bindschedler, L.V., Minibayeva, F., Gardner, S.L., Gerrish, C., Davies, D.R., and Bolwell, G.P., Early signaling events in the apoplastic oxidative burst in suspension cultured French bean cells involve cAMP and Ca2+, New Phytol., 2001, vol. 151, pp. 185–194.

    Article  CAS  Google Scholar 

  9. Zhao, J., Guo, Y., Fujita, K., and Sakai, K., Involvement of cAMP signaling in elicitor-induced phytoalexin accumulation in Cupressus lusitanica cell cultures, New Phytol., 2004, vol. 161, pp. 723–731.

    Article  CAS  Google Scholar 

  10. Lomovatskaya, L.A., Romanenko, A.S., Filinova, N.V., and Dudareva, L.V., Determination of cAMP in plant cells by a modified enzyme immunoassay method, Plant Cell Rep., 2011, vol. 30, pp. 125–132.

    Article  CAS  PubMed  Google Scholar 

  11. Galletti, R., Denoux, C., Gambetta, S., Dewdney, J., Ausubel, F.M., De Lorenzo, G., and Ferrari, S., The AtrbohD-mediated oxidative burst elicited by oligogalacturonides in Arabidopsis is dispensable for the activation of defense responses effective against Botrytis cinerea, Plant Physiol., 2008, vol. 148, pp. 1695–1706.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Glyan'ko, A.K. and Ishchenko, A.A., Effect of rhizobial (Rhizobium leguminosarum) inoculation and calcium ions on the activity of HADP-oxidase in the roots of etiolated Pisum sativum (L.) seedlings, Appl. Biochem. Microbiol., 2013, vol. 49, pp. 236–241.

    Google Scholar 

  13. Fujishige, N.A., Kapadia, N.N., De Hoff, P.L., and Hirsch, A.M., Investigations of Rhizobium biofilm formation, FEMS Microbiol. Ecol., 2006, vol. 56, pp. 195–206.

    Article  CAS  PubMed  Google Scholar 

  14. Janczarek, M., Rachwal, K., Marzec, A., Grza, J., and Palusinska-Szysz, M., Signal molecules and cell-surface components involved in early stages of the legume–Rhizobium interactions, Appl. Soil Ecol., 2015, vol. 85, pp. 94–113.

    Article  Google Scholar 

  15. Kumar, M.S., Swarna Lakshmi, K., and Annapurna, K., Exopolysaccharide from Rhizobium: production and role in symbiosis, in Rhizobium Biology and Biotechnology, Hansen, A.P., Ed., Germany: Springer, 2017, vol. 50, pp. 257–293.

    Google Scholar 

  16. Sidorova, K.K., Shumnyi, V.K., Vlasova, E.Yu., Glyanenko, M.N., Mishchenko, T.M., and Maistrenko, G.G., Symbiogenetics and selection of macrosymbiote to increase nitrogen fixation by Pisum sativum (L.) plant, Vestn. Vavilov Sci. Genet. Breed., vol. 14, pp. 357–374.

  17. Antipchuk, A.F. and Kosenko, L.V., The influence of lipopolysaccharides and glucanes from two Rhizobium le-guminosarum bv. viciae strains on the formation and efficiency of their symbioses with pea plants, Microbiology (Moscow), 2004, vol. 73, pp. 62–67.

    Article  CAS  PubMed  Google Scholar 

  18. Luo, L. and Lu, D., Immunosuppression during Rh-izobium–legume symbiosis, Plant Signal. Behav., 2014, vol. 9, pp. 281–292.

    Article  CAS  Google Scholar 

  19. Libault, M., Farmer, A., Brechenmacher, L., Drnevich, J., Landley, R.L., Bilgin, D.D., Radwan, O., Neece, D.J., Clough, S.J., May, G.D., and Stacey, G., Complete transcriptome of the soybean root hair cell, a single-cell model, and its alteration in response to Bradyrhizobium japonicum infection, Plant Physiol., 2010, vol. 152, pp. 541–552.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Kelly, S., Radutoiu, S., and Stougaard, J., Legume LysM receptors mediate symbiotic and pathogenic signaling, Curr. Opin. Plant Biol., 2017, vol. 39, pp. 152–158.

    Article  CAS  PubMed  Google Scholar 

  21. Gehring, C., Adenyl cyclases and cAMP in plant signaling—past and present, Cell Commun. Signal., 2010, vol. 8, no. 15, pp. 1–5.

    Article  CAS  Google Scholar 

  22. Kreslavskii, V.D., Los, D.A., Allakhverdiev, S.I., and Kuznetsov, Vl.V., Signaling role of reactive oxygen species in plants under stress, Russ. J. Plant Physiol., 2012, vol. 59, pp. 141–154.

    Article  CAS  Google Scholar 

  23. Suzuki, N. and Katano, K., Coordination between ROS regulatory systems and other pathways under heat stress and pathogen attack, Front. Plant Sci., 2018, vol. 9: 490.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Lohar, D.P., Sharopova, N., Endre, G., Penuela, S., Samac, D., Town, C., Silverstein, K.A.T., and van den Bosch, K.A., Transcript analysis of early nodulation events in Medicago truncatula, Plant Physiol., 2006, vol. 140, pp. 221–234.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Granqvist, E., Sun, J., Camp, R.O., Pujic, P., Hill, L., Normand, P., Morris, R.J., Downie, A.J., Geurts, R., and Oldroyd, G.E.D., Bacterial-induced calcium oscillations are common to nitrogen-fixing associations of nodulating legumes and non-legumes, New Phytol., 2015, vol. 207, pp. 551–558.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Ma, W., Qi, Z., Smigel, A., Walker, R.K., Verma, R., and Berkowitz, G.A., Ca2+, cAMP, and transduction of non-self-perception during plant immune responses, Proc. Natl. Acad. Sci. USA, 2009, vol. 106, pp. 20995–21000.

    Article  PubMed  Google Scholar 

  27. Venkateshwaran, M., Jayaraman, D., Chabaud, M., Genre, A., Balloon, A.J., Maeda, J., Forshey, K., den Os, D., Kwiecien, N.W., Coon, J.J., Barker, D.G., and Ané, J.M., A role for the mevalonate pathway in early plant symbiotic signaling, Proc. Natl. Acad. Sci. USA, 2015, vol. 112, no. 31, pp. 9781–9786.

    Article  CAS  PubMed  Google Scholar 

  28. Saand, M.A., Xu, Y.P., Munyampundu, J.P., Li, W., Zhang, X.R., and Cai, X.Z., Phylogeny and evolution of plant cyclic nucleotide-gated ion channel (CNGC) gene family and functional analyses of tomato CNGCs, DNA Res., 2015, vol. 22, no. 6, pp. 471–483.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Clúa, J., Roda, C., Zanetti, M.E., and Blanco, F.A., Compatibility between legumes and rhizobia for the establishment of a successful nitrogen-fixing symbiosis, Genes, 2018, vol. 125, pp. 1–21.

  30. Popp, C. and Ott, T., Regulation of signal transduction and bacterial infection during root nodule symbiosis, Curr. Opin. Plant Biol., 2011, vol. 14, pp. 458–467.

    Article  CAS  PubMed  Google Scholar 

Download references

ACKNOWLEDGMENTS

The work was performed using equipment of TsKB Bioanalitika and collections of TsKB Bioresursnyi Tsentr of the Siberian Institute of Plant Physiology and Biochemistry.

Author information

Authors and Affiliations

  1. Siberian Institute of Plant Physiology and Biochemistry, Siberian Branch, Russian Academy of Sciences, 664033, Irkutsk, Russia

    O. V. Kuzakova, L. A. Lomovatskaya, A. M. Goncharova & A. S. Romanenko

Authors
  1. O. V. Kuzakova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. L. A. Lomovatskaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. M. Goncharova
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. S. Romanenko
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to L. A. Lomovatskaya.

Ethics declarations

The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.

Additional information

Translated by A. Aver’yanov

Abbreviations: CFU—colony-forming units; EPS—exopolysaccharides; Rlv—Rhizobium leguminosarum bv. vicea.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kuzakova, O.V., Lomovatskaya, L.A., Goncharova, A.M. et al. Effects of Rhizobium leguminosarum bv. viceae Strains Different in Their Symbiotic Effectiveness on Changes in cAMP and Hydrogen Peroxide Concentrations in Cells of Pea Seedlings. Russ J Plant Physiol 66, 712–717 (2019). https://doi.org/10.1134/S1021443719050121

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1021443719050121

Keywords:

Search

Navigation