TSitologiya i Genetika 2018, vol. 52, no. 6, 10-17
Cytology and Genetics 2018, vol. 52, no. 6, 400–405, doi: https://www.doi.org/10.3103/S0095452718060129

Methyl jasmonate and nitric oxide in regulation of stomatal apparatus of Arabidopsis thaliana

Yastreb Т.О., Kolupaev Yu.Е., Kokorev А.I., Horielova Е.I., Dmitriev А.P.

SUMMASRY. Effect of methyl jasmonate, donors and antagonists of nitric oxide (NO) on the state of stomata of Arabidopsis thaliana plants (Col-0) was studied. Treatment of the epidermis of leaves with a 50–400 µM solution of methyl jasmonate (MJ) caused a decrease in size of stomatal aperture and percentage of open stomata. These effects were completely eliminated after preliminary treatment of epidermis cells with NO scavenger PTIO (2-phenyl-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide) and partially after treatment with inhibitors of animal NO synthase (NG-nitro-L-arginine methyl ester, L-NAME) and nitrate reductase (sodium tungstate). NO donors (L-arginine and sodium nitrite) in concentrations of 0,5–2,0 mM also caused a decrease in number of open stomata and size of stomatal aperture. Action of L-arginine on state of stomata was leveled by pretreatment of cells with L-NAME, and effects of sodium nitrite were eliminated by pre-action of sodium tungstate. A conclusion was made about a possible participation of nitrogen oxide, forming both along the pathway of L-arginine oxidation, and during nitrate/nitrite reduction, in regulation of stomatal apparatus, and about its role in realization of MJ effect on state of stomata in A. thaliana.

Keywords: Arabidopsis thaliana, stomata, methyl jasmonate, nitric oxide, L- arginine, nitrite, signaling

TSitologiya i Genetika
2018, vol. 52, no. 6, 10-17

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Cytology and Genetics
2018, vol. 52, no. 6, 400–405,
doi: 10.3103/S0095452718060129

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References

1. Acharya, B.R. and Assmann, S.M., Hormone interactions in stomatal function, Plant Mol. Biol., 2009, vol. 69, no. 4, pp. 451–462. doi 10.1007/s11103-008-9427-0

2. Sarwat, M. and Tuteja, N., Hormonal signaling to control stomatal movement during drought stress, Plant Gene, 2017, vol. 11, pt. B, pp. 143–53. doi.org/10.1016/ j.plgene.2017.07.007

3. Brosche, M., Merilo, E., Mayer, F., Pechter, P., Puzorjova, I., Brader, G., Kangasjarvi, J., and Kollist, H., Natural variation in ozone sensitivity among Arabidopsis thaliana accessions and its relation to stomatal conductance, Plant Cell Environ., 2010, vol. 33, no. 6, pp. 914–925. doi 10.1111/j.1365-3040.2010.02116.x

4. Montillet, J.L., Leonhardt, N., Mondy, S., Tranchimand, S., Rumeau, D., Boudsocq, M., Garcia, A.V., Douki, T., Bigear, J., Lauriere, C., Chevalier, A., Castresana, C., and Hirt, H., An abscisic acid-independent oxylipin pathway controls stomatal closure and immune defense in Arabidopsis, PLoS Biol., 2013, vol. 11, no. 3. e1001513. doi 10.1371/journal.pbio.1001513Central

5. Miura, K., Okamoto, H., Okuma, E., Shiba, H., Kamada, H., Hasegawa, P.M., and Murata, Y., SIZ1 deficiency causes reduced stomatal aperture and enhanced drought tolerance via controlling salicylic acid-induced accumulation of reactive oxygen species in Arabidopsis, Plant J., 2013, vol. 73, no. 1, pp. 91–104. doi 10.1111/tpj.12014

6. de Ollas, C. and Dodd, I.C., Physiological impacts of ABA–JA interactions under water-limitation, Plant Mol. Biol., 2016, vol. 91, pp. 641–650. doi 10.1007/ s11103-016-0503-6Central

7. Melotto, M., Underwood, W., and He, S.Y., Role of stomata in plant innate immunity and foliar bacterial diseases, Annu. Rev. Phytopathol., 2008, vol. 46, pp. 101–122. doi 10.1146/annurev.phyto.121107.104959Central

8. Munemasa, S., Mori, I.C., and Murata, Y., Methyl jasmonate signaling and signal crosstalk between methyl jasmonate and abscisic acid in guard cells, Plant Signal. Behav., 2011, vol. 6, no. 7, pp. 939–941. doi 10.4161/psb.6.7.15439Central

9. Liu, X., Shi, W., Zhang, S., and Lou, C., Nitric oxide involved in signal transduction of jasmonic acid-induced stomatal closure of Vicia faba L., Chinese Sci. Bull., 2005, vol. 50, no. 6, pp. 520–525. doi 10.1360/982004-794

10. Munemasa, S., Oda, K., Watanabe-Sugimoto, M., Nakamura, Y., Shimoishi, Y., and Murata, Y., The coronatine-insensitive 1 mutation reveals the hormonal signaling interaction between abscisic acid and methyl jasmonate in Arabidopsis guard cells. Specific impairment of ion channel activation and second messenger production, Plant Physiol., 2007, vol. 143, no. 3, pp. 1398–1407. doi 0.1104/pp.106.091298Central

11. Krasylenko, Y.A., Yemets, A.I., and Blume, Y.B., Functional role of nitric oxide in plants, Russ. J. Plant Physiol., 2010, vol. 57, no. 4, pp. 451–461. doi 10.1134/S1021443710040011

12. Roszer, T., Biosynthesis of nitric oxide in plants, in Nitric Oxide in Plants: Metabolism and Role in Stress Physiology, 2014, pp. 17–32. doi 10.1007/978-3-319-06710-0_2

13. Santolini, J., Andrea, F., Jeandroz, S., and Wendehenne, D., Nitric oxide synthase in plants: where do we stand?, Nitric Oxide, 2017, vol. 63, pp. 30–38. doi 10.1016/j.niox.2016.09.005

14. Desikan, R., Griffiths, R., Hancock, J., and Neill, S., A new role for an old enzyme: nitrate reductasemediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Arabidopsis thaliana, Proc. Natl. Acad. Sci. U. S. A., 2002, vol. 99, no. 25, pp. 16314–16318. doi 10.1073/pnas.252461999Central

15. Neill, S.J., Desikan, R., Clarke, A., and Hancock, J.T., Nitric oxide is a novel component of abscisic acid signaling in stomatal guard cells, Plant Physiol., 2002, vol. 128, no. 1, pp. 13–16. doi 10.1104/pp.010707Central

16. Gibeaut, D.M., Hulett, J., Cramer, G.R., and Seemann, J.R., Maximal biomass of Arabidopsis thaliana using a simple, low-maintenance hydroponic method and favorable environmental conditions, Plant Physiol., 1997, vol. 115, no. 2, pp. 317–319. doi 10.1104/pp.115.2.317Central

17. Yastreb, T.O., Kolupaev, Yu.E., Shvidenko, N.V., Lugovaya, A.A., and Dmitriev, A.P., Salt stress response in Arabidopsis thaliana plants with defective jasmonate signaling, Appl. Biochem. Microbiol., 2015, vol. 51, no. 4, pp. 451–454. doi 10.1134/S000368381504016X

18. Ramírez, V., Coego, A., López, A., Agorio, A., Flors, V., and Vera, P., Drought tolerance in Arabidopsis is controlled by the OCP3 disease resistance regulator, Plant J., 2009, vol. 58, no. 4, pp. 578–591. doi 10.1111/ j.1365-313X.2009.03804.x

19. Yastreb, T.O., Kolupaev, Yu.E., Lugovaya, A.A., and Dmitriev, A.P., Formation of adaptive reactions in Arabidopsis thaliana wild-type and mutant jin1 plants under action of abscisic acid and salt stress, Cytol. Genet., 2017, vol. 51, no. 5, pp. 325–330. doi 10.3103/ S0095452717050115

20. Chamizo-Ampudia, A., Sanz-Luque, E., Llamas, A., Galvan, A., and Fernandez, E., Nitrate reductase regulates plant nitric oxide homeostasis, Trends Plant Sci., 2017, vol. 22, no. 2, pp. 163–174. doi 10.1016/ j.tplants.2016.12.001

21. Corpas, F.J. and Barroso, J.B., Nitric oxide synthase-like activity in higher plants, Nitric Oxide, 2017, vol. 68, pp. 5–6. doi 10.1016/j.niox.2016.10.009

22. Farnese, F.S., Menezes-Silva, P.E., Gusman, G.S., and Oliveira, J.A., When bad guys become good ones: the key role of reactive oxygen species and nitric oxide in the plant responses to abiotic stress, Front. Plant Sci., 2016, vol. 7, p. 471. doi 10.3389/fpls.2016.00471Central

23. Sami, F., Faizan, M., Faraz, A., Siddiqui, H., Yusuf, M., and Hayat, S., Nitric oxidemediated integrative alterations in plant metabolism to confer abiotic stress tolerance, NO crosstalk with phytohormones and NO-mediated post translational modifications in modulating diverse plant stress, Nitric Oxide, 2018, vol. 73, pp. 22–38. doi 10.1016/j.niox.2017.12.005

24. Gayatri, G., Agurla, S., and Raghavendra, A.S., Nitric oxide in guard cells as an important secondary messenger during stomatal closure, Front. Plant Sci., 2013, vol. 4, p. 425. doi 10.3389/fpls.2013.00425Central

25. Laxalt, A.M., García-Mata, C., and Lamattina, L., The dual role of nitric oxide in guard cells: promoting and attenuating the ABA and phospholipid-derived signals leading to the stomatal closure, Front. Plant Sci., 2016, vol. 7, p. 476. doi 10.3389/fpls.2016.00476Central

26. Hao, F., Zhao, S., Dong, H., Zhang, H., Sun, L., and Miao, C., Nia1 and Nia2 are involved in exogenous salicylic acid-induced nitric oxide generation and stomatal closure in Arabidopsis, J. Integr. Plant Biol., 2010, vol. 52, no. 3, pp. 298–307. doi 10.1111/j.1744-7909.2010.00920.x

27. Fancy, N.N., Bahlmann, A.K., and Loake, G.J., Nitric oxide function in plant abiotic stress, Plant Cell Environ., 2017, vol. 40, no. 4, pp. 462–72. doi 10.1111/pce.12707

28. Scuffi, D., Lamattina, L., and Garcia-Mata, C., Decoding the interaction between nitric oxide and hydrogen sulfide in stomatal movement, in Gasotransmitters in Plants: The Rise of a New Paradigm in Cell Signaling, 2016, pp. 271–288. doi 10.1007/978-3-319-40713-5_13

29. He, J.M., Ma, X.G., Zhang, Y., Sun, T.F., Xu, F.F., Chen, Y.P., Liu, X., and Yue, M., Role and interrelationship of Gα protein, hydrogen peroxide, and nitric oxide in ultraviolet B-induced stomatal closure in Arabidopsis leaves, Plant Physiol., 2013, vol. 161, no. 3, pp. 1570–1583. doi 10.1104/pp.112.211623Central

30. Wimalasekera, R., Villar, C., Begum, T., and Scherer, G.F., Copper amine oxidase1 (CuAO) of Arabidopsis thaliana contributes to abscisic acid- and polyamine-induced nitric oxide biosynthesis and abscisic acid signal transduction, Mol. Plant., 2001, vol. 4, no. 4, pp. 663–678. doi 10.1093/mp/ssr023

31. Gupta, K.J. and Kaiser, W.M., Production and scavenging of nitric oxide by barley root mitochondria, Plant Cell Physiol., 2010, vol. 51, no. 4, pp. 576–584. doi 10.1093/pcp/pcq022

32. Glyan’ko, A.K., Initiation of nitric oxide (NO) synthesis in roots of etiolated seedlings of pea (Pisum sativum L.) under the influence of nitrogen-containing compounds, Biochemistry (Moscow), 2013, vol. 78, no. 5, pp. 471–476. doi 10.1134/S0006297913050052