Preview

Proceedings of Universities. Applied Chemistry and Biotechnology

Advanced search

Regulation of the activity of adenylate cyclases by hydrogen peroxide in pea root cells Infected with pathogens and a mutualist

https://doi.org/10.21285/2227-2925-2020-10-3-450-458

Abstract

This study examines the effect of a range of exogenous concentrations of hydrogen peroxide on the activity of transmembrane and soluble adenylate cyclases (EC 4.6.1.1) contained in root cells of pea seedlings infected with one of the following: Rhizobium leguminosarum bv. Viciae, Pseudomonas syringae pv. Pisi, and Clavibacter michiganensis ssp. sepedonicus. The results showed that the pool of intracellular H2O2 increased when pea roots were infected with bacteria regardless of type. The study analysed the concentration of intracellular cyclic adenosine monophosphate, a product of the adenosine triphosphate cyclization reaction catalyzed by transmembrane and soluble adenylate cyclases. The concentration of intracellular cyclic adenosine monophosphate increased when infected with either Rhizobium leguminosarum bv. viciae or Clavibacter michiganensis ssp. Sepedonicus; however, the concentration decreased by 20% when infected with Pseudomonas syringae pv. Pisi. The in vitro activity of soluble and transmembrane adenylate cyclases from pea root cells inoculated with Rhizobium leguminosarum bv. viciae was H2O2 dose-dependent: 100 nM of H2O2 reduced the activity of soluble and transmembrane adenylate cyclases slightly, while 26 µM inhibited their activity by 50–60%. When infected with Pseudomonas syringae pv. pisi, the reduction in the activity of soluble and transmembrane adenylate cyclases was independent of the concentrations of H2O2 in the range investigated. When infected with Clavibacter michiganensis ssp. sepedonicus, 100 nM of H2O2 inhibited the activity of transmembrane adenylate cyclases, although enhancing the activity of soluble adenylate cyclases. On the contrary, concentrations of H2O2 of 2.6 and 26 µM increased the activity of transmembrane adenylate cyclases and inhibited the activity of soluble adenylate cyclases. It can be concluded that the specific concentration of second messengers in plant cells depends on the specificity of the biotic stressor and forms, inter alia, by their mutual influence on the components of other plant signaling systems.

About the Authors

O. V. Kuzakova
Siberian Institute of Plant Physiology and Biochemistry, SB RAS
Russian Federation

Olga V. Kuzakova, Cand. Sci. (Biology), Junior Researcher

132, Lermontov St., Irkutsk, 664033



L. A. Lomovatskaya
Siberian Institute of Plant Physiology and Biochemistry, SB RAS
Russian Federation

Lidia A. Lomovatskaya, Dr. Sci. (Biology), Leading Researcher

132, Lermontov St., Irkutsk, 664033



A. S. Romanenko
Siberian Institute of Plant Physiology and Biochemistry, SB RAS
Russian Federation

Anatoly S. Romanenko, Dr. Sci. (Biology), Professor, Chief Researcher

132, Lermontov St., Irkutsk, 664033



A. M. Goncharova
Siberian Institute of Plant Physiology and Biochemistry, SB RAS
Russian Federation

Alena M. Goncharova, Leading Engineer

132, Lermontov St., Irkutsk, 664033



References

1. Kuzakova OV, Lomovatskaya LA, Goncharova AM., Romanenko AS. Influence of strains of different symbiotic efficacy Rhizobium leguminosarum bv. viciae on changes in the concentration of cAMP and hydrogen peroxide in the cells of pea seedlings. Fiziologiya rastenii. 2019;66(5):360–366. (In Russian)

2. Jiang J, Fan LW, Wu WH. Evidences for involvement of endogenous cAMP in Arabidopsis defense responses to Verticillium toxins. Cell Research. 2005;15(8):585–592. https://doi.org/10.1038/SJ.CR.7290328

3. Lomovatskaya LA, Kuzakova OV, Romanenko AS, Goncharova AM. Adenylate cyclase activity and a change in cAMP concentration in pea seed root cells upon infection by mutualists and phytopathogens. Fiziologiya rastenii. 2018;65(4):310–320. (In Russian)

4. Bianchet C, Wong A, Quaglia M, Alqurashi M, Gehring C, Ntoukakis V, et al. An Arabidopsis thaliana leucine-rich repeat protein harbors an adenylyl cyclase catalytic center and affects responses to pathogens. Journal of Plant Physiology. 2019;232:12–22. https://doi.org/10.1016/j.jplph.2018.10.025

5. Filinova NV, Lomovatskaya LA, Romanenko AS, Salyayev RK. Calcium as a modulator of adenylate cyclase activity of potato plant cells during bacterial pathogenesis. Doklady Akademii nauk. 2018;483(6):687–689. (In Russian) https://doi.org/10.31857/S086956520003458-6

6. Molodchenkova OO. The activity of NADPH oxidase, the content of hydrogen peroxide and salicylic acid in seedlings of spring barley with fusarium infection and the action of salicylic acid. Fiziologiya i biokhimiya kul'turnykh rastenii = Physiology and Biochemistry of Cultivated Plants. 2009;41(4):321–326. (In Russian)

7. Tkachuk VA, Tyurin-Kuzmin PA, Belousov VV, Vorotnikov AV. Hydrogen peroxide as a new second messenger. Biologicheskiye membrany. 2012; 29(1-2):21–37. (In Russian)

8. Černý M, Habánová H, Berka M, Luklová M, Brzobohatý B. Hydrogen peroxide: its role in plant biology and crosstalk with signalling networks. International Journal of Molecular Sciences. 2018;19(9): 2812. https://doi.org/10.3390/ijms19092812

9. Lomovatskaya LA, Romanenko AS, Rykun OV. Effect of Ca 2+ and H 2 O 2 on the change in cAMP level in vacuoles of beet root crops cells under biotic stress. Biologicheskiye membrany. 2014;31(3):194–203. (In Russian) https://doi.org/10.7868/s0233475514020042

10. Romanenko AS, Lomovatskaya LA, Shafikova TN, Borovskii GB, Krivolapova NV. Potato cell membrane receptors to ring rot pathogen extracellular polysaccharides. Journal of Phytopathology. 2003;151(1). 6 p. https://doi.org/10.1046/j.1439-0434.2003.00667.x

11. Lomovatskaya LA, Romanenko AS, Filinova NV, Dudareva L.V. Determination of cAMP in plant cells by a modified enzyme immunoassay method. Plant Cell Reports. 2011;30(1):125–132. https://doi.org/10.1007/s00299-010-0950-5

12. Galletti R, Denoux C, Gambetta S, Dewdney J, Ausubel FM, De Lorenzo G, et al. The AtrbohD-mediated oxidative burst elicited by oligogalacturonides in Arabidopsis is dispensable for the activation of defense responses effective against Botrytis cinerea. Plant Physiology. 2008;148(3):1695–1706. https://doi.org/10.1104/pp.108.127845

13. Glyan’ko AK, Vasil’eva GG. Reactive oxygen and nitrogen species in legume-rhizobial symbiosis: A review. Applied biochemistry and microbiology. 2010;46(1):15–22. https://doi.org/10.1134/S0003683810010023

14. Jamet A, Mandon K, Puppo A, Hérouart D. H 2 O 2 is required for optimal establishment of the Medicago sativa/Sinorhizobium meliloti symbiosis. Journal of Bacteriology. 2007;187(23):8741–8745. https://doi.org/10.1128/JB.01130-07

15. Suzuki N, Katano K. Coordination between ROS regulatory systems and other pathways under heat stress and pathogen attack. Frontiers in Plant Science. 2018;9:490. https://doi.org/10.3389/fpls.2018.00490

16. Veselov AP, Chumankina EA, Markina IV. The effect of exogenous hydrogen peroxide on lipid peroxidation and antioxidant enzymes of isolated pea chloroplasts. Vestnik of Lobachevsky University of Nizhni Novgorod. 2001;1:164–167. (In Russian)

17. Lukatkin AS. Contribution of oxidative stress to the development of cold damage in the leaves of heat-loving plants. Damage to cell membranes during cooling of thermophilic plants. Fiziologiya rastenii. 2003;50(2):271–274. (In Russian)

18. Stadtman ER, Levine RL. Free radicalmediated oxidation of free amino acids and amino acid residues in proteins. Amino Acids. 2003;25;207–218. https://doi.org/10.1007/s00726-003-0011-2

19. Al-Younis I, Wong A, Gehring G. The Arabidopsis thaliana K+-uptake permease 7 (AtKUP7) contains a functional cytosolic adenylate cyclase catalytic centre. FEBS Letters. 2015;589(24):3848–3852. https://doi.org/10.1016/j.febslet.2015.11.038

20. Chatukuta P, Dikobe TB, Kawadza DT, Sehlabane KS, Takundwa MM, Wong A, et al. An Arabidopsis clathrin assembly protein with a predicted role in plant defense can function as an adenylate cyclase. Biomolecules. 2018;8(2). 15 p. https://doi.org/10.3390/biom8020015

21. Gehring C. Adenyl cyclases and cAMP in plant signaling – past and present. Cell Communication and Signaling. 2010;8. 5 p. https://doi.org/10.1186/1478-811X-8-15

22. Chang JH, Desveaux D, Creason AL. The ABCs and 123s of bacterial secretion systems in plant pathogenesis. Annual Review Phytopathology. 2014;52:317–345. https://doi.org/10.1146/annurev-phyto-011014-015624

23. Demidchik V. ROS-Activated ion channels in plants: biophysical characteristics, physiological functions and molecular nature. International Journal of Molecular Sciences. 2018;19(4):1263. https://doi.org/10.3390/ijms19041263

24. Eichenlaub R, Gartemann K-H. The Clavibacter michiganensis subspecies: molecular investigation of gram-positive bacterial plant pathogens. Annual Review Phytopathology. 2011;49:445–64. https://doi.org/10.1146/annurev-phyto-072910-095258

25. Romanenko AS, Graskova IA, Rifel AA, Kopytchuk VN, Rachenko MA. Potato roots stabilization of the medium pH displaced by ring rot pathogen. Fiziologiya rastenii. 1996;43(5):707–712. (In Russian)

26. Pyatygin SS. Features of the signal role of action potential in higher plants. Uspekhi sovremennoi biologii. 2007;127(3):293–298. (In Russian)


Review

For citations:


Kuzakova O.V., Lomovatskaya L.A., Romanenko A.S., Goncharova A.M. Regulation of the activity of adenylate cyclases by hydrogen peroxide in pea root cells Infected with pathogens and a mutualist. Proceedings of Universities. Applied Chemistry and Biotechnology. 2020;10(3):450-458. https://doi.org/10.21285/2227-2925-2020-10-3-450-458

Views: 425


Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 License.


ISSN 2227-2925 (Print)
ISSN 2500-1558 (Online)