Skip to main content
SpringerLink
Log in

Calcium and Components of Lipid Signaling in Implementation of Hydrogen Sulfide Influence on the State of Stomata in Arabidopsis thaliana

  • Published:
Cytology and Genetics Aims and scope Submit manuscript

Abstract—

A time and concentration dependence of the hydrogen sulfide donor sodium hydrosulfide (NaHS) influence on the state of stomata of Arabidopsis thaliana (Col-0) leaves, as well as the role of calcium and phospholipases in the implementation of its effects, was studied. Treatment of leaves with NaHS in the concentration range of 5–250 μM caused a decrease in the size of the stomatal aperture. The maximal effect of the stomatal closure was observed 90 min after the beginning of the treatment with H2S donor, and the stomatal aperture in NaHS variants was, on the contrary, much wider than in the control after 180 min of exposure. The effect of treatment with NaHS solutions on the stomata state was completely eliminated by hydroxylamine, the hydrogen sulfide scavenger, which indicates the specificity of NaHS effects as an H2S donor. The decrease in stomatal aperture and relative number of open stomata caused by the donor of hydrogen sulfide was almost completely leveled off by the pretreatment of leaves with the calcium channel blocker lanthanum chloride, the extracellular calcium chelator EGTA, the phospholipase C inhibitor neomycin, and the antagonist of the formation of cyclic adenosine-5'-diphosphate ribose—nicotinamide. In addition, the stomatal effect of theH2S donor was partially eliminated by the calmodulin antagonist chlorpromazine. The leveling of the hydrogen sulfide donor action on the state of stomatal apparatus of Arabidopsis leaves was also noted at the pretreatment of leaves with butanol-1, an inhibitor of phospholipase D-dependent formation of phosphatidic acid. A conclusion about the importance of calcium intake into the cytosol from various compartments, as well as lipid signaling mediators formed with the involvement of phospholipases C and D, in the implementation of hydrogen sulfide action on the state of stomata was made.

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.
Fig. 4.

Similar content being viewed by others

REFERENCES

  1. Lisjak, M., Teklic, T., Wilson, I.D., Whiteman, M., and Hancock, J.T., Hydrogen sulfide: environmental factor or signalling molecule?, Plant Cell Environ., 2013, vol. 36, no. 9, pp. 1607–1616. https://doi.org/10.1111/pce.12073

    Article  PubMed  CAS  Google Scholar 

  2. Zhang, H., Hydrogen sulfide in plant biology, in Signaling and Communication in Plants. Gasotransmitters in Plants, Lamattina, L. and Garcia-Mata, C., Eds., Switzerland: Springer Int. Publ., 2016, pp. 23–51. https://doi.org/10.1007/978-3-319-40713-5_2.

  3. Jin, Z.P., Shen, J.J., Qiao, Z.J., Yang, G.D., Wang, R., and Pei, Y.X., Hydrogen sulfide improves drought resistance in Arabidopsis thaliana, Biochem. Biophys. Res. Commun., 2011, vol. 414, no. 3, pp. 481–486.  https://doi.org/10.1016/j.bbrc.2011.09.090

    Article  PubMed  CAS  Google Scholar 

  4. Lai, D.W., Mao, Y., Zhou, H., Li, F., Wu, M., Zhang, J., He, Z., Cui, W., and Xie, Y., Endogenous hydrogen sulfide enhances salt tolerance by coupling the reestablishment of redox homeostasis and preventing salt-induced K+ loss in seedlings of Medicago sativa, Plant Sci., 2014, vol. 225, pp. 117–129. https://doi.org/10.1016/j.plantsci.2014.06.006

    Article  PubMed  CAS  Google Scholar 

  5. Fang, H.H., Pei, Y.X., Tian, B.H., Zhang, L.P., Qiao, Z.J., and Liu, Z.Q., Ca2+ participates in H2S induced Cr6+ tolerance in Setaria italica, Chin. J. Cell Biol., 2014, vol. 36, no. 6, pp. 758–765.

    CAS  Google Scholar 

  6. Shi, H., Ye, T., and Chan, Z., Nitric oxide-activated hydrogen sulfide is essential for cadmium stress response in bermudagrass (Cynodon dactylon (L). Pers.), Plant Physiol. Biochem., 2014, vol. 74, pp. 99–107. https://doi.org/10.1016/j.plaphy.2013.11.001

    Article  PubMed  CAS  Google Scholar 

  7. Li, Z.G. and Zhu, L.P., Hydrogen sulfide donor sodium hydrosulfide-induced accumulation of betaine is involved in the acquisition of heat tolerance in maize seedlings. Braz. J. Bot., 2014, vol. 38, no. 1, pp. 31–38. https://doi.org/10.1007/s40415-014-0106-x

  8. Yang, M., Qin, B.P., Ma, X.L., Wang, P., Li, M.L., Chen, L.L., Chen, L.T., Sun, A.Q., Wang, Z.L., and Yin, Y.P., Foliar application of sodium hydrosulfide (NaHS), a hydrogen sulfide (H2S) donor, can protect seedlings against heat stress in wheat (Triticum aestivum L.), J. Integr. Agricult., 2015. V. 15. no. 12. P. 2745–58. https://doi.org/10.1016/S2095-3119(16)61358-8

  9. Kolupaev, Yu.E., Firsova, E.N., Yastreb, T.O., and Lugovaya, A.A., The participation of calcium ions and reactive oxygen species in the induction of antioxidant enzymes and heat resistance in plant cells by hydrogen sulfide donor. Appl. Biochem. Microbiol., 2017, vol. 53, no. 5, pp. 573–579.https://doi.org/10.1134/S0003683817050088

  10. Wang, Y., Li, L., Cui, W., Xu, S., Shen, W., and Wang, R., Hydrogen sulfide enhances alfalfa (Medicago sativa) tolerance against salinity during seed germination by nitric oxide pathway, Plant Soil., 2012, vol. 351, nos. 1–2, pp. 107–119. https://doi.org/10.1007/s11104-011-0936-2

  11. Lai, D.W., Mao, Y., Zhou, H., Li, F., Wu, M., Zhang, J., He, Z., Cui, W., and Xie, Y., Endogenous hydrogen sulfide enhances salt tolerance by coupling the reestablishment of redox homeostasis and preventing salt-induced K+ loss in seedlings of Medicago sativa, Plant Sci., 2014, vol. 225, pp. 117–129. https://doi.org/10.1016/j.plantsci.2014.06.006

    Article  PubMed  CAS  Google Scholar 

  12. Shi, H., Ye, T., and Chan, Z., Exogenous application of hydrogen sulfide donor sodium hydrosulfide enhanced multiple abiotic stress tolerance in bermudagrass (Cynodon dactylon (L.). Pers.), Plant Physiol. Biochem., 2013, vol. 71, pp. 226–234. https://doi.org/10.1016/j.plaphy.2013.07.021

    Article  PubMed  CAS  Google Scholar 

  13. Li, Z.G., Min, X., and Zhou, Z.H., Hydrogen sulfide: a signal molecule in plant cross-adaptation, Front. Plant Sci., 2016, vol. 7, p. 1621. https://doi.org/10.3389/fpls.2016.01621

    Article  PubMed  PubMed Central  Google Scholar 

  14. Zhang, H., Ye, Y.K., Wang, S.H., Luo, J.P., Tang, J., and Ma, D.F., Hydrogen sulfide counteracts chlorophyll loss in sweet potato seedling leaves and alleviates oxidative damage against osmotic stress, Plant Growth Regul., 2009, vol. 58, no. 3, pp. 243–250. https://doi.org/10.1007/s10725-009-9372-1

  15. Kolupaev, Yu.E., Firsova, E.N., Yastreb, T.O., Kirichenko, V.V., and Ryabchun, N.I., Influence of hydrogen sulfide donor on state of antioxidant system and resistance of wheat plants to soil drought. Russ. J. Plant Physiol., 2019, vol. 66, no. 1, pp. 59–66. doi 10.1134/S1021443719010084

  16. Jin, Z., Wang, Z., Ma, Q., Sun, L., Zhang, L., Liu, Z., Liu, D., Hao, X., and Pei, Y., Hydrogen sulfide mediates ion fluxes inducing stomatal closure in response to drought stress in Arabidopsis thaliana, Plant Soil, 2017, vol. 419, nos. 1–2, pp. 141–152. https://doi.org/10.1007/s11104-017-3335-5

  17. Scuffi, D., Nietzel, T., Di Fino, L.M., Meyer, A.J., Lamattina, L., Schwarzländer, M., Laxalt, A.M., and García-Mata, C., Hydrogen sulfide increases production of NADPH oxidase-dependent hydrogen peroxide and phospholipase D-derived phosphatidic acid in guard cell signaling, Plant Physiol., 2018, vol. 176, no. 3, pp. 2532–2542. https://doi.org/10.1104/pp.17.01636

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  18. Hu, K.D., Tang, J., Zhao, D.L., Hu, L.Y., Li, Y.H., Liu, Y.S., Jones, R., and Zhang, H., Stomatal closure in sweet potato leaves induced by sulfur dioxide involves H2S and NO signaling pathways, Biol. Plant., 2014, vol. 58, no. 4, pp. 676–680. https://doi.org/10.1007/s10535-014-0440-7

  19. Lisjak, M., Srivastava, N., Teklic, T., Civale, L., Lewandowski, K., Wilson, I., Wood, M.E., Whiteman, M., and Hancock, J.T., A novel hydrogen sulfide donor causes stomatal opening and reduces nitric oxide accumulation, Plant Physiol. Biochem., 2010, vol. 48, no. 12, pp. 931–935. https://doi.org/10.1016/j.plaphy.2010.09.016

    Article  PubMed  CAS  Google Scholar 

  20. Lisjak, M., Teklić, T., Wilson, I.D., Wood, M.E., Whiteman, M., and Hancock, J.T., Hydrogen sulfide effects on stomatal apertures, Plant Signal. Behav., 2011, vol. 6, no. 10, pp. 1444–1446. https://doi.org/10.4161/psb.6.10.17104

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  21. Duan, B., Ma, Y., Jiang, M., Yang, F., Ni, L., and Lu, W., Improvement of photosynthesis in rice (Oryza sativa L.) as a result of an increase in stomatal aperture and density by exogenous hydrogen sulfide treatment, Plant Growth Regul., 2015, vol. 75, no. 1, pp. 33–44. https://doi.org/10.1007/s10725-014-9929-5

  22. Honda, K., Yamada, N., Yoshida, R., Ihara, H., Sawa, T., Akaike, T., and Iwai, S., 8-Mercapto-Cyclic GMP mediates hydrogen sulfide-induced stomatal closure in Arabidopsis, Plant Cell Physiol., 2015, vol. 56, no. 8, pp. 1481–1489. https://doi.org/10.1093/pcp/pcv069

    Article  PubMed  CAS  Google Scholar 

  23. Papanatsiou, M., Scuffi, D., Blatt, M.R., and Garcia-Mata, C., Hydrogen sulfide regulates inward-rectifying K+ channels in conjunction with stomatal closure, Plant Physiol., 2015, vol. 168, no. 1, pp. 29–35. https://doi.org/10.1104/pp.114.256057

  24. Wang, L., Ma, X., Che, Y., Hou, L., Liu, X., and Zhang, W., Extracellular ATP mediates H2S-regulated stomatal movements and guard cell K+ current in a H2O2-dependent manner in Arabidopsis, Sci. Bull., 2015, vol. 60, no. 4, pp. 419–27. doi.org/https://doi.org/10.1007/s11434-014-0659-x

  25. Suhita, D., Kolla, V.A., Vavasseur, A., and Raghavendra, A.S., Different signaling pathways involved during the suppression of stomatal opening by methyl jasmonate or abscisic acid, Plant Sci., 2003, vol. 164, no. 4, pp. 481–488. https://doi.org/10.1016/S0168-9452(02)00432-6

  26. Marino, D., Dunand, C., Puppo, A., and Pauly, N., A burst of plant NADPH oxidases, Trends Plant Sci., 2012, vol. 17, no. 1, pp. 9–15. https://doi.org/10.1016/j.tplants.2011.10.001

    Article  PubMed  CAS  Google Scholar 

  27. 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. https://doi.org/10.1134/S000368381504016X

  28. 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. https://doi.org/10.3103/S0095452717050115

  29. Neill, S., Bright, J., Desikan, R., Hancock, J., Harrison, J., and Wilson, I., Nitric oxide, evolution and perception, J. Exp. Bot., 2008, vol. 59, no. 1, pp. 25–35. https://doi.org/10.1093/jxb/erm218

  30. Lanteri, M.L., Laxalt, A.M., and Lamattina, L., Nitric oxide triggers phosphatidic acid accumulation via phospholipase D during auxin-induced adventitious root formation in cucumber, Plant Physiol., 2008, vol. 147, no. 1, pp. 188–198. https://doi.org/10.1104/pp.107.111815

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  31. Liu, H.T., Huang, W.D., Pan Q.H., Weng F.H., Zhan J.C., Liu Y., Wan S.B., Liu Y.Y. Contributions of PIP2-specific-phospholipase C and free salicylic acid to heat acclimation-induced thermotolerance in pea leaves, J. Plant Physiol., 2006, vol. 163, no. 4, pp. 405–416. https://doi.org/10.1016/j.jplph.2005.04.027

  32. Lee, Y. and Lee, Y., Roles of phosphoinositides in regulation of stomatal movements, Plant Signal. Behav., 2008, vol. 3, no. 4, pp. 211–213.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Lecourieux, D., Mazars, C., Pauly, N., Ranjeva, R., and Pugin, A., Analysis and effects of cytosolic free calcium increases in response to elicitors in Nicotiana plumbaginifolia cells, Plant Cell, 2002, vol. 14, no. 10, pp. 2627–2641. https://doi.org/10.1105/tpc.005579

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  34. Iakovenko, O.M., Kretynin, S.V., Kabachevskaya, E.M., Lyakhnovich, G.V., Volotovski, D.I., and Kravets, V.S., Role of phospholipase C in ABA regulation of stomata function, Ukr. Bot. J., 2008, vol. 65, no. 4, pp. 605–613.

    Google Scholar 

  35. Arisz, S.A., Wijk, R., Roels, W., Zhu, J.K., Haring, M.A., and Munnik, T., Rapid phosphatidic acid accumulation in response to low temperature stress in Arabidopsis is generated through diacylglycerol kinase, Front. Plant Sci., 2013, vol. 4, p. 1. https://doi.org/10.3389/fpls.2013.00001

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  36. Pappan, K., Zheng, S., and Wang, X., Identification and characterization of a novel plant phospholipase D that requires polyphosphoinositides and submicromolar calcium for activity in Arabidopsis, J. Biol. Chem., 1997, vol. 272, no. 11, pp. 7048–7054. https://doi.org/10.1074/jbc.272.11.7048

    Article  PubMed  CAS  Google Scholar 

Download references

COMPLIANCE WITH ETHICAL STANDARDS

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.

Author information

Authors and Affiliations

  1. Dokuchaev Kharkiv National Agrarian University, 62483, Kharkiv, Ukraine

    T. O. Yastreb, Yu. E. Kolupaev, E. N. Havva & M. A. Shkliarevskyi

  2. Karazin Kharkiv National University, 61022, Kharkiv, Ukraine

    Yu. E. Kolupaev

  3. Institute of Cell Biology and Genetic Engineering, National Academy of Sciences of Ukraine, 03143, Kyiv, Ukraine

    A. P. Dmitriev

Authors
  1. T. O. Yastreb
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yu. E. Kolupaev
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. E. N. Havva
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. A. Shkliarevskyi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. A. P. Dmitriev
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to T. O. Yastreb, Yu. E. Kolupaev, E. N. Havva, M. A. Shkliarevskyi or A. P. Dmitriev.

Additional information

Translated by V. Mittova

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yastreb, T.O., Kolupaev, Y.E., Havva, E.N. et al. Calcium and Components of Lipid Signaling in Implementation of Hydrogen Sulfide Influence on the State of Stomata in Arabidopsis thaliana. Cytol. Genet. 53, 99–105 (2019). https://doi.org/10.3103/S0095452719020099

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.3103/S0095452719020099

Search

Navigation