Skip to main content
SpringerLink
Log in

Cytosolic acidification precedes nitric oxide removal during inhibition of ABA-induced stomatal closure by fusicoccin

  • Research Papers
  • Published:
Russian Journal of Plant Physiology Aims and scope Submit manuscript

Abstract

The role of nitric oxide (NO) and the relationship between NO and cytosolic pH during inhibition of ABA effect by fusicoccin (FC) in guard cells of Vicia faba were analyzed. ABA induced NO generation and stomatal closure, but FC inhibited the effects of ABA. Treatment with 2-(4-carboxyphenyl)-4,4,5,5-tetra-methylimidazoline-1-oxyl-3-oxide (cPTIO) and NG-nitro-L-Arg-methyl ester (L-NAME) mimicked the effects of FC. These data suggest that inhibition of ABA effect by FC is possibly related to the decreasing in the NO level. Furthermore, like cPTIO, FC not only suppressed stomatal closure and NO level in guard cells treated with NO donor sodium nitroprusside (SNP), but also reopened stomata, which had been closed by ABA, and reduced the level of NO in guard cells that had been produced by ABA, indicating that FC caused NO removal. Butyric acid simulated the effects of FC on the stomatal aperture and increased NO levels in guard cells treated with SNP and had been closed by ABA, and both FC and butyric acid surely reduced cytosolic pH, which demonstrates that cytosolic acidification mediates FC-induced NO removal. Taken together, our results show that FC induces NO removal and reduces NO level via cytosolic acidification in guard cells, thus inhibiting ABA effect.

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

Similar content being viewed by others

Abbreviations

te]BCECF-AM:

2′,7′-bis(2-carboxyethyl)-5(6)-car-boxy fluorescein-acetoxy methyl ester

cPTIO:

2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide

DAF-2DA:

4,5-diaminofluorescein diacetate

DMSO:

dimethyl sulfoxide

FC:

fusicoccin

L-NAME:

NG-nitro-L-arg-methyl ester

MJ:

methyl jasmonate

SNP:

sodium nitroprusside

References

  1. García-Mata, C. and Lamattina, L., Nitric Oxide Induces Stomatal Closure and Enhances the Adaptive Plant Responses against Drought Stress, Plant Physiol., 2001, vol. 126, pp. 1196–1204.

    Article  PubMed  Google Scholar 

  2. Lee, Y., Choi, Y.B., Suh, S., Lee, J., Assmann, S.M., Joe, C.O., Kelleher, J.F., Richard, C., and Crain, R.C., Abscisic Acid-Induced Phosphoinositide Turnover in Guard Cell Protoplasts of Vicia faba, Plant Physiol., 1996, vol. 110, pp. 987–996.

    PubMed  CAS  Google Scholar 

  3. Leckie, C.P., McAinsh, M.R., Allen, G.J., Sanders, D., and Hetherington, A.M., Abscisic Acid-Induced Stomatal Closure Mediated by Cyclic ADP-Ribose, Proc. Natl. Acad. Sci. USA, 1998, vol. 95, pp. 15 837–15 842.

    Article  CAS  Google Scholar 

  4. Allen, G.J., Kwak, J.M., Chu, S.P., Llopis, J., Tsien, R.Y., Harper, J.F., and Schroeder, J.I., Cameleon Calcium Indicator Reports Cytoplasmic Calcium Dynamics in Arabidopsis Guard Cells, Plant J., 1999, vol. 19, pp. 735–747.

    Article  PubMed  CAS  Google Scholar 

  5. Murata, Y., Pei, Z.M., Mori, I.C., and Schroeder, H.I., Abscisic Acid Activation of Plasma Membrane Ca2+ Channels in Guard Cells Requires Cytosolic NAD(P)H and Is Differentially Disrupted Upstream and Down-stream of Reactive Oxygen Species Production in abi1-1 and abi2-1 Protein Phosphatase 2C Mutants, Plant Cell, 2001, vol. 13, pp. 2513–2523.

    PubMed  CAS  Google Scholar 

  6. Suhita, D., Raghavendra, A.S., Kwak, J.M., and Vavasseur, A., Cytoplasmic Alkalization Precedes Reactive Oxygen Species Production during Methyl Jasmonate- and Abscisic Acid-Induced Stomatal Closure, Plant Physiol., 2004, vol. 134, pp. 1536–1545.

    Article  PubMed  CAS  Google Scholar 

  7. Irving, H.R., Gehring, C.A., and Parish, R.W., Changes in Cytosolic pH and Calcium of Guard Cells Precede Stomatal Movements, Proc. Natl. Acad. Sci. USA, 1992, vol. 89, pp. 1790–1794.

    Article  PubMed  CAS  Google Scholar 

  8. Assmann, S.M. and Schwartz, A., Synergistic Effect of Light and Fusicoccin on Stomatal Opening, Plant Physiol., 1992, vol. 98, pp. 1349–1355.

    Article  PubMed  CAS  Google Scholar 

  9. Braunsgaard, L., Fuglsang, A.T., Jahn, T., Korthout, H.A.A.J., de Boer, A.H., and Palmgren, M.G., The 14-3-3 Proteins Associate with Plant Plasma Membrane H+-ATPase to Generate a Fusicoccin Binding Complex and a Fusicoccin Responsive System, Plant J., 1998, vol. 13, pp. 661–671.

    Article  Google Scholar 

  10. 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, pp. 13–16.

    Article  PubMed  CAS  Google Scholar 

  11. Zhang, X., Takemiya, A., Kinoshita, T., and Shimazaki, K., Nitric Oxide Inhibits Blue Light-Specific Stomatal Opening via Abscisic Acid Signaling Pathways in Vicia Guard Cells, Plant Cell Physiol., 2007, vol. 48, pp. 715–723.

    Article  PubMed  CAS  Google Scholar 

  12. Gonugunta, V.K., Srivastava, N., Puli, M.R., and Raghavendra, A.S., Nitric Oxide Production Occurs after Cytosolic Alkalinization during Stomatal Closure Induced by Abscisic Acid, Plant Cell Environ., 2008, vol. 31, pp. 1717–1724.

    Article  PubMed  CAS  Google Scholar 

  13. Marrè, E., Fusicoccin: A Tool in Plant Physiology, Annu. Rev. Plant Physiol., 1979, vol. 30, pp. 273–288.

    Article  Google Scholar 

  14. Beffagna, N., Cocucci, S., and Marrè, E., Stimulating Effect of Fusicoccin on K+-Activated ATPase in Plasmalemma Preparations from Higher Plant Tissues, Plant Sci. Lett., 1977, vol. 8, pp. 91–98.

    Article  CAS  Google Scholar 

  15. She, X.P. and Song, X.G., Cytokinin- and Auxin-Induced Stomatal Opening Is Related to the Change of Nitric Oxide Levels in Guard Cells in Broad Bean, Physiol. Plant., 2006, vol. 128, pp. 569–579.

    Article  CAS  Google Scholar 

  16. McAinsh, M.R., Clayton, H., Mansfield, T.A., and Hetherington, A.M., Changes in Stomatal Behavior and Guard Cell Cytosolic Free Calcium in Response to Oxidative Stress, Plant Physiol., 1996, vol. 111, pp. 1031–1042.

    PubMed  CAS  Google Scholar 

  17. Kojima, H., Nakatsubo, N., Kikuchi, K., Kawahara, S., Kirino, Y., Nagoshi, H., Hirata, Y., and Nagano, T., Detection and Imaging of Nitric Oxide with Novel Fluorescent Indicators: Diaminofluoresceins, Anal. Chem., 1998, vol. 70, pp. 2446–2453.

    Article  PubMed  CAS  Google Scholar 

  18. García-Mata, C. and Lamattina, L., Nitric Oxide and Abscisic Acid Cross Talk in Guard Cells, Plant Physiol., 2002, vol. 128, pp. 790–792.

    Article  PubMed  Google Scholar 

  19. Foissner, I., Wendehenne, D., Langebartels, C., and Durner, J., In Vivo Imaging of an Elicitor-Induced Nitric Oxide Burst in Tobacco, Plant J., 2000, vol. 23, pp. 817–824.

    Article  PubMed  CAS  Google Scholar 

  20. Gonugunta, V.K., Srivastava, N., and Raghavendra, A.S., Cytosolic Alkalinization Is a Common and Early Messenger Preceding the Production of ROS and NO during Stomatal Closure by Variable Signals, Including Abscisic Acid, Methyl Jasmonate and Chitosan, Plant Signal. Behav., 2009, vol. 4, pp. 561–564.

    Article  PubMed  CAS  Google Scholar 

  21. Malerba, M., Crosti, P., and Cerana, R., The Fusicoccin-Induced Accumulation of Nitric Oxide in Sycamore Cultured Cells Is Not Required for the Toxin-Stimulated Stress-Related Reponses, Plant Sci., 2005, vol. 168, pp. 381–387.

    Article  CAS  Google Scholar 

  22. Malerba, M., Contran, N., Tonelli, M., Crosti, P., and Cerana, R., Role of Nitric Oxide in Actin Depolymerization and Programmed Cell Death Induced by Fusicoccin in Sycamore (Acer pseudoplatanus) Cultured Cells, Physiol. Plant., 2008, vol. 133, pp. 449–457.

    Article  PubMed  CAS  Google Scholar 

  23. Zhang, X., Dong, F.C., Gao, J.F., and Song, C.P., Hydrogen Peroxide-Induced Changes in Intracellular pH of Guard Cells Precede Stomatal Closure, Cell Res., 2001, vol. 11, pp. 37–43.

    Article  PubMed  Google Scholar 

  24. Palmgren, M.G., Plant Plasma Membrane H+-ATPases: Powerhouses for Nutrient Uptake, Annu. Rev. Plant Physiol. Plant Mol. Biol., 2001, vol. 52, pp. 817–845.

    Article  PubMed  CAS  Google Scholar 

  25. Zhang, X., Wang, H.B., Takemiya, A., Song, C.P., Kinoshita, T., and Shimazaki, K.I., Inhibition of Blue Light-Dependent H+ Pumping by Abscisic Acid through Hydrogen Peroxide-Induced Dephosphorylation of the Plasma Membrane H+-ATPase in Guard Cell Protoplasts, Plant Physiol., 2004, vol. 136, pp. 4150–4158.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Key Laboratory of Medicinal Plant Resource and Natural Pharmaceutical Chemistry of Ministry of Education, College of Life Sciences, Shaanxi Normal University, Xi’an, 710062, China

    A. X. Huang

  2. College of Life Sciences, Shaanxi Normal University, Xi’an, 710062, China

    A. X. Huang, X. P. She, Y. Y. Zhang & J. L. Zhao

Authors
  1. A. X. Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. X. P. She
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Y. Y. Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. L. Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to X. P. She.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Huang, A.X., She, X.P., Zhang, Y.Y. et al. Cytosolic acidification precedes nitric oxide removal during inhibition of ABA-induced stomatal closure by fusicoccin. Russ J Plant Physiol 60, 60–68 (2013). https://doi.org/10.1134/S1021443712060076

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1021443712060076

Keywords

Search

Navigation