Skip to main content
Log in

The Effect of Neurotransmitters on Programmed Cell Death and Formation of Reactive Oxygen Species in the Pea Leaf Epidermis

  • RESEARCH ARTICLE
  • Published:
Moscow University Biological Sciences Bulletin Aims and scope Submit manuscript

Abstract

Neurotransmitters are found not only in animals, but also in other living organisms, including plants. However, the data on the functions of these compounds in the plant world are far from being comprehensive. In particular, the issue concerning their impact on plant cell death still demands further research. In the present study, we tested the effects of neurotransmitters on programmed cell death and the formation of reactive oxygen species (ROS) in plants. Programmed cell death was estimated from the destruction of cell nuclei. ROS was determined using 2′,7′-dichlorofluorescein. Dopamine, norepinephrine, serotonin, histamine, acetylcholine and acetylthiocholine (its synthetic analog) were used. The catecholamines dopamine and norepinephrine suppressed KCN-induced destruction of guard cell nuclei in the pea leaf epidermis at concentrations of 0.01–1 mM. In contrast, serotonin and acetylcholine (1–3 mM) promoted the destruction of nuclei that was induced by KCN. Histamine and acetylthiocholine had no effect on KCN-induced destruction of nuclei at concentrations of 0.01–3 mM. Unlike natural neurotransmitters, acetylthiocholine (3 mM), caused the destruction of guard cell nuclei even when KCN was absent. Dopamine, norepinephrine, and serotonin reduced menadione-induced ROS formation in the pea leaf epidermis. No similar effect was observed with histamine, acetylcholine, and acetylthiocholine. Therefore, dopamine, norepinephrine, and serotonin possess antioxidant properties in plants. In addition, dopamine and norepinephrine prevent cell death.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.

Similar content being viewed by others

REFERENCES

  1. Roshchina, V.V., Neirotransmittery – biomediatory i regulyatory rastenii (Neurotransmitters—Biomediators and Plant Regulators), Pushchino: Inst. Biofiz. Kletki Ross. Akad. Nauk, 2010.

  2. Simons, F.E.R. and Simons, K.J., Histamine and H1-antihistamines: Celebrating a century of progress, J. Allergy Clin. Immunol., 2011, vol. 128, no. 6, pp. 1139–1150.E4.

  3. Roshchina, V.V., Evolutionary considerations of neurotransmitters in microbial, plant, and animal cells, in Microbial Endocrinology: Interkingdom Signaling in Infectious Disease and Health, Lyte, M., and Freestone, P.P.E., Eds., New York: Springer-Verlag, 2010, pp. 17–52.

    Google Scholar 

  4. Kulma, A. and Szopa, J., Catecholamines are active compounds in plants, Plant Sci., 2007, vol. 172, no. 3, pp. 433–440.

    Article  CAS  Google Scholar 

  5. Erland, L.A.E. and Saxena, P.K., Melatonin and serotonin in plant morphogenesis and development, in Neurotransmitters in Plants: Perspectives and Applications, Ramakrishna, A., and Roshchina, V.V., Eds., Boca Raton: CRC Press, 2018, pp. 57–70.

    Google Scholar 

  6. Ramakrishna, A. and Mukherjee, S., New insights on neurotransmitter signaling mechanisms in plants, Plant Signaling Behav., 2020, vol. 5, no. 6, p. 1737450.

    Google Scholar 

  7. Vitale, I., Pietrocola, F., Guilbaud, E., et al., Apoptotic cell death in disease – Current understanding of the NCCD 2023, Cell Death Differ., 2023, vol. 30, no. 5, pp. 1097–1154.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Mukhtar, M.S., McCormack, M.E., Argueso, C.T., and Pajerowska-Mukhtar, K.M., Pathogen tactics to manipulate plant cell death, Curr. Biol., 2016, vol. 26, no. 13, pp. R608–R619.

    Article  CAS  PubMed  Google Scholar 

  9. Van Hautegem, T., Waters, A.J., Goodrich, J., and Nowack, M.K., Only in dying, life: programmed cell death during plant development, Trends Plant Sci., 2015, vol. 20, no. 2, pp. 102–113.

    Article  CAS  PubMed  Google Scholar 

  10. Pitsili, E., Phukan, U.J., and Coll, N.S., Cell death in plant immunity, Cold Spring Harbor Perspect. Biol., 2020, vol. 12, no. 6, p. a036483.

    Article  CAS  Google Scholar 

  11. Ye, C., Zheng, S., Jiang, D., Lu, J., Huang, Z., Liu, Z., Zhou, H., Zhuang, C., and Li, J., Initiation and execution of programmed cell death and regulation of reactive oxygen species in plants, Int. J. Mol. Sci., 2021, vol. 22, no. 23, p. 12942.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Samuilov, V.D., Lagunova, E.M., Kiselevsky, D.B., Dzyubinskaya, E.V., Makarova, Ya.V., and Gusev, M.V., Participation of chloroplasts in plant apoptosis, Biosci. Rep., 2003, vol. 23, nos. 2–3, pp. 103–117.

    Article  CAS  PubMed  Google Scholar 

  13. LeBel, C.P., Ischiropoulos, H., and Bondy, S.C., Evaluation of the probe 2',7'-dichiorofluorescin as an indicator of reactive oxygen species formation and oxidative stress, Chem. Res. Toxicol., 1992, vol. 5, no. 2, pp. 227–231.

    Article  CAS  PubMed  Google Scholar 

  14. Wrona, M., Patel, K., and Wardman, P., Reactivity of 2',7'-dichlorodihydrofluorescein and dihydrorhodamine 123 and their oxidized forms toward carbonate, nitrogen dioxide, and hydroxyl radicals, Free Radical Biol. Med., 2005, vol. 38, no. 2, pp. 262–270.

    Article  CAS  Google Scholar 

  15. Karlsson, M., Kurz, T., Brunk, U.T., Nilsson, S.E., and Frennesson, C.I., What does the commonly used DCF test for oxidative stress really show?, Biochem. J., 2010, vol. 428, no. 2, pp. 183–190.

    Article  CAS  PubMed  Google Scholar 

  16. Goldberg, B. and Stern, A., Production of superoxide anion during the oxidation of hemoglobin by menadione, Biochim. Biophys. Acta, 1976, vol. 437, no. 2, pp. 628–632.

    Article  CAS  PubMed  Google Scholar 

  17. Hassan, H.M. and Fridovich, I., Intracellular production of superoxide radical and of hydrogen peroxide by redox active compounds, Arch. Biochem. Biophys., 1979, vol. 196, no. 2, pp. 385–395.

    Article  CAS  PubMed  Google Scholar 

  18. Szilagyi, J.T., Fussell, K.C., Wang, Y., Jan, Y.H., Mishin, V., Richardson, J.R., Heck, D.E., Yang, S., Aleksunes, L.M., Laskin, D.L., and Laskin, J.D., Quinone and nitrofurantoin redox cycling by recombinant cytochrome b5 reductase, Toxicol. Appl. Pharmacol., 2018, vol. 359, pp. 102–107.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Kobayashi, Y. and Heber, U., Rates of vectorial proton transport supported by cyclic electron flow during oxygen reduction by illuminated intact chloroplasts, Photosynth. Res., 1994, vol. 41, no. 3, pp. 419–428.

    Article  CAS  PubMed  Google Scholar 

  20. Huseynova, I.M., Aliyeva, D.R., and Aliyev, J.A., Subcellular localization and responses of superoxide dismutase isoforms in local wheat varieties subjected to continuous soil drought, Plant Physiol. Biochem., 2014, vol. 81, pp. 54–60.

    Article  CAS  PubMed  Google Scholar 

  21. Dzyubinskaya, E.V., Kiselevsky, D.B., Bakeeva, L.E., and Samuilov, V.D., Programmed cell death in plants: Effect of protein synthesis inhibitors and structural changes in pea guard cells, Biochemistry (Moscow), 2006, vol. 71, no. 4, pp. 395–405.

    CAS  PubMed  Google Scholar 

  22. Dzyubinskaya, E.V., Kiselevsky, D.B., Lobysheva, N.V., Shestak, A.A., and Samuilov, V.D., Death of stoma guard cells in leaf epidermis under disturbance of energy provision, Biochemistry (Moscow), 2006, vol. 71, no. 10, pp. 1120–1127.

    CAS  PubMed  Google Scholar 

  23. Tunçel, N., Aydin, Y., and Tikiz, H., The effect of three products of cigarette smoke (cyanide, thiocyanate and nicotine) on the concentration-response curves of 5-hydroxytryptamine, norepinephrine and epinephrine in the isolated human umbilical veins and arteries, Pharmacol. Toxicol., 1994, vol. 74, no. 2, pp. 84–88.

    Article  PubMed  Google Scholar 

  24. Held, K.D., Sylvester, F.C., Hopcia, K.L., and Biaglow, J.E., Role of Fenton chemistry in thiol-induced toxicity and apoptosis, Radiat. Res., 1996, vol. 145, no. 5, pp. 542–553.

    Article  CAS  PubMed  Google Scholar 

  25. Van Noorden, C.J. and Butcher, R.G., The involvement of superoxide anions in the nitro blue tetrazolium chloride reduction mediated by NADH and phenazine methosulfate, Anal. Biochem., 1989, vol. 176, no. 1, pp. 170–174.

    Article  CAS  PubMed  Google Scholar 

  26. Kagan, V.E. and Tyurina, Y.Y., Recycling and redox cycling of phenolic antioxidants, Ann. N. Y. Acad. Sci., 1998, vol. 854, no. 1, pp. 425–434.

    Article  CAS  PubMed  Google Scholar 

  27. Duthie, G. and Crozier, A., Plant-derived phenolic antioxidants, Curr. Opin. Lipidol., 2000, vol. 11, no. 1, pp. 43–47.

    Article  CAS  PubMed  Google Scholar 

  28. Rahman, M.M., Rahaman, M.S., Islam, M.R., Rahman, F., Mithi, F.M., Alqahtani, T., Almikhlafi, M.A., Alghamdi, S.Q., Alruwaili, A.S., Hossain, M.S., Ahmed, M., Das, R., Emran, T.B., and Uddin, M.S., Role of phenolic compounds in human disease: current knowledge and future prospects, Molecules, 2021, vol. 27, no. 1, p. 233.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Liu, Q., Gao, T., Liu, W., Liu, Y., Zhao, Y., Liu, Y., Li, W., Ding, K., Ma, F., and Li, C., Functions of dopamine in plants: a review, Plant Signal. Behav., 2020, vol. 15, no. 12, p. 1827782.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Yen, G.-C. and Hsieh, C.-L., Antioxidant effects of dopamine and related compounds, Biosci. Biotechnol. Biochem., 1997, vol. 61, no. 10, pp. 1646–1649.

    Article  CAS  PubMed  Google Scholar 

  31. Erland, L.A.E., Turi, C.E., and Saxena, P.K., Serotonin: An ancient molecule and an important regulator of plant processes, Biotechnol. Adv., 2016, vol. 34, no. 8, pp. 1347–1361.

    Article  CAS  PubMed  Google Scholar 

  32. Huether, G. and Schuff-Werner, P., Platelet serotonin acts as a locally releasable antioxidant, Adv. Exp. Med. Biol., 1996, vol. 398, pp. 299–306.

    Article  CAS  PubMed  Google Scholar 

  33. Kalyanaraman, B., Felix, C.C., and Sealy, R.C., Peroxidatic oxidation of catecholamines. A kinetic electron spin resonance investigation using the spin stabilization approach, J. Biol. Chem., 1984, vol. 259, no. 12, pp. 7584–7589.

    Article  CAS  PubMed  Google Scholar 

  34. Siraki, A.G. and O’Brien, P.J., Prooxidant activity of free radicals derived from phenol-containing neurotransmitters, Toxicology, 2002, vol. 177, no. 1, pp. 81–90.

    Article  CAS  PubMed  Google Scholar 

  35. Sango, J., Kakihana, T., Takahashi, M., Katsuragi, Y., Anisimov, S., Komatsu, M., and Fujii, M., USP10 inhibits the dopamine-induced reactive oxygen species-dependent apoptosis of neuronal cells by stimulating the antioxidant Nrf2 activity, J. Biol. Chem., 2022, vol. 298, no. 1, p. 101448.

    Article  CAS  PubMed  Google Scholar 

  36. Jodko-Piórecka, K. and Litwinienko, G., Antioxidant activity of dopamine and L-DOPA in lipid micelles and their cooperation with an analogue of α-tocopherol, Free Radical Biol. Med., 2015, vol. 83, pp. 1–11.

    Article  Google Scholar 

  37. Gomes, B.R., Siqueira-Soares, R.de C., Dos Santos, W.D., Marchiosi, R., Soares, A.R., and Ferrarese-Filho, O., The effects of dopamine on antioxidant enzymes activities and reactive oxygen species levels in soybean roots, Plant Signaling Behav., 2014, vol. 9, no. 12, p. e977704.

    Article  Google Scholar 

Download references

Funding

The research was carried out as part of the Scientific Project of the State Order of the Government of Russian Federation to Lomonosov Moscow State University no. 121042600047-9.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to D. B. Kiselevsky.

Ethics declarations

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

This work does not contain any studies involving human and animal subjects.

CONFLICT OF INTEREST

The authors of this work declare that they have no conflicts of interest.

Additional information

Translated by D. Martynova

Publisher’s Note.

Allerton Press remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kiselevsky, D.B., Oleskin, A.V. & Samuilov, V.D. The Effect of Neurotransmitters on Programmed Cell Death and Formation of Reactive Oxygen Species in the Pea Leaf Epidermis. Moscow Univ. Biol.Sci. Bull. 78, 205–211 (2023). https://doi.org/10.3103/S0096392523600710

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.3103/S0096392523600710

Keywords:

Navigation