Skip to main content
SpringerLink
Log in

Regulation of blue-light-induced proton pumping by Vicia faba L. guard-cell protoplasts: Energetic contributions by chloroplastic and mitochondrial activities

  • Published:
Planta Aims and scope Submit manuscript

Abstract

An initial response during signal transduction in guard cells, following absorption of blue light, is the extrusion of protons. Translocation of protons across the guard-cell plasmalemma is an energy-requiring activity. The present study has investigated the energetic contribution from guard-cell chloroplasts and mitochondria to blue-light-induced proton pumping by Vicia faba guard-cell protoplasts. The addition of 3(3,4-dichlorophenyl)-1,1-dimethylurea to the protoplast suspension had a minimal effect on rates of acidification when oxygen concentrations of the medium were maintained close to near-saturating levels. Under the same conditions, oligomycin reduced both the rates of blue-light-induced acidification and total proton efflux. Lowering the oxygen concentration of the suspending medium to approximately 20 μM resulted in complete inhibition of blue-light-induced acidification activity. Swelling of protoplasts induced by blue light was also inhibited by low oxygen levels. Levels of ATP from whole-protoplast extracts were reduced by about 64% when exposed to low levels of oxygen. Increasing oxygen levels to near-saturating levels restored both blue-light-induced acidification rates and swelling of the protoplasts within a 60-min recovery period. Levels of ATP also increased during the recovery period. Addition of 3(3,4-dichlorophenyl)-1,1-dimethylurea or oligomycin to the suspending medium prior to increasing the oxygen concentration caused a reduction in acidification rates after the recovery period by 40 and 80%, respectively. Levels of ATP in guard-cell protoplasts were also reduced by both inhibitors after a 60-min recovery period. The results demonstrate that both guard-cell chloroplasts and mitochondria contribute energetically to blue-light-induced proton pumping by guard-cell protoplasts. Furthermore, both energy sources are inhibited by low oxygen concentrations, suggesting coordinated metabolic regulation between photo- and oxidative phosphorylation in guard cells.

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

BL:

blue light

Chl:

chlorophyll

DCMU:

3(3,4-dichlorophenyl)-1,1-dimethylurea

GCPs:

guard-cell protoplasts

References

  • Amodeo, G., Srivastava, A., Zeiger, E. (1992) Vanadate inhibits blue light-stimulated swelling of Vicia guard cell protoplasts. Plant Physiol. 100, 1567–1570

    Google Scholar 

  • Anderson, J., Beardall, J. (1991) Molecular activities of plant cells. Blackwell Scientific Publication, Oxford

    Google Scholar 

  • Arnon, D.I. (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol. 24, 1–15

    Google Scholar 

  • Assmann, S.M., Zeiger, E. (1987) Guard cell bioenergetics. In: Stomatal function, pp 165–194, Zeiger, E. Farquhar, G.D., Cowan, I., eds. Stanford University Press, Stanford, USA

    Google Scholar 

  • Assmann, S.M., Simoncini, L., Schroeder, J.I. (1985) Blue light activates electrogenic ion pumping in guard cell protoplasts of Vicia faba L. Nature 318, 285–287

    Google Scholar 

  • Couchat, P., Lasceve, G., Vavasseur, A. (1988) Oxygen-requiring processes in stomatal movement. Plant Physiol. (Life Sci. Adv.) 7, 187–190

    Google Scholar 

  • Dahse, I., Schnabl, H., Hampp, R., Zeigler, H., Muller, E., Liebremann, B. (1988) Inhibition of light-induced stomatal opening and of guard-cell-protoplast swelling in Vicia faba L. by tentoxin, an inhibitor of photophosphorylation. Planta 73, 391–396

    Google Scholar 

  • Gautier, H., Vavasseur, A., Gans, P., Lasceve, G. (1991) Relationship between respiration and photosynthesis in guard cell and mesophyll cell protoplasts of Commelina commuais L. Plant Physiol. 95, 636–641

    Google Scholar 

  • Gautier, H., Vavasseur, A., Lasceve, G., Boudet, A.M. (1992) Redox processes in the blue light response of guard cell protoplasts of Commelina communis L. Plant Physiol. 98, 34–38

    Google Scholar 

  • Gepstein, S., Jacobs, M. Taiz, L. (1982) Inhibition of stomata opening in Vicia faba epidermal tissue by vanadate and abscisic acid. Plant Sci. Lett. 28, 63–72

    Google Scholar 

  • Gotow, K., Sakaki, T., Kondo, N., Kobayashi, K., Syono, K. (1985) Light-induced alkalinization of the suspending medium of guard cell protoplasts from Vicia faba L. Plant Physiol. 79, 825–828

    Google Scholar 

  • Iino, M., Ogawa, T., Zeiger, E. (1985) Kinetic properties of the blue-light response of stomata. Proc. Natl. Acad. Sci. USA 81, 7103–7107

    Google Scholar 

  • Karlsson, P.E. (1986) Blue light regulation of stomata in wheat seedings. I. Influence of red background illumination and initial conductance level. Physiol. Plant. 66, 202–206

    Google Scholar 

  • Kromer, S., Heldt, H.W. (1991) On the role of mitochondrial oxidative phosphorylation in photosynthesis metabolism as studied by the effect of oligomycin on photosynthesis in protoplasts and leaves of barley (Hordeum vulgare). Plant Physiol. 95, 1270–1276

    Google Scholar 

  • Kruse, T., Tallman, G., Zeiger, E. (1989) Isolation of guard cell protoplasts from mechanically prepared epidermis of Vicia faba leaves. Plant Physiol. 90, 1382–1386

    Google Scholar 

  • Mawson, B.T. (1993) Modulation of photosynthesis and respiration in guard and mesophyll cell protoplasts by oxygen concentration. Plant Cell Environ. 16, 207–214

    Google Scholar 

  • Michalke, B., Schnabl, H. (1987) The status of adenine nucleotides and malate in chloroplasts, mitochondria, and supernatant of guard cell protoplasts from Vicia faba. J. Plant Physiol. 130, 243–253

    Google Scholar 

  • Raghavendra, A.S. (1981) Energy supply for stomatal opening in epidermal strips of Commelina benghalensis. Plant Physiol. 67, 385–387

    Google Scholar 

  • Raghavendra, A.S. (1990) Blue light effects on stomata are mediated by the guard cell plasma membrane redox system distinct from the proton translocating ATPase. Plant Cell Environ. 13, 105–110

    Google Scholar 

  • Schwartz, A., Zeiger, E. (1984) Metabolic energy for stomatal opening. Roles of photophosphorylation and oxidative phosphorylation. Planta 161, 129–136

    Google Scholar 

  • Serrano, E.E., Zeiger, E. (1989) Sensory transduction and electrical signaling in guard cells. Plant Physiol. 91, 795–799

    Google Scholar 

  • Serrano, E.E., Zeiger, E., Hagiwara, S. (1988) Red light stimulates an electrogenic proton pump in Vicia guard cell protoplasts. Proc. Natl. Acad. Sci. USA 85, 436–440

    Google Scholar 

  • Sharkey, T.D., Raschke, K. (1981) Effect of light quality on stomatal opening in leaves of Xanthium strumarium L. Plant Physiol. 68, 1170–1174

    Google Scholar 

  • Sharkey, T.D., Ogawa, T. (1987) Stomatal responses to light. In: Stomatal function, pp. 195–208, Zeiger, E., Farquhar, G.D., Cowan, I. eds. Stanford University Press, Stanford, USA

    Google Scholar 

  • Shimazaki, K., Gotow, K., Sakaki, T., Kondo, N. (1983) High respiratory activity of guard cell protoplasts from Vicia faba L. Plant Cell Physiol. 24, 1049–1056

    Google Scholar 

  • Shimazaki, K., Iino, M., Zeiger, E. (1986) Blue light-dependent proton extrusion by guard-cell protoplasts of Vicia faba. Nature 319, 324–326

    Google Scholar 

  • Shimazaki K., Terada, J., Tanaka, K., Kondo, N. (1989) Calvin-Benson cycle enzymes in guard-cell protoplasts from Vicia faba L. Implications for the greater utilization of phosphoglycerate/dihydroxyacetone phosphate shuttle between chloroplasts and the cytosol. Plant Physiol. 90, 1057–1064

    Google Scholar 

  • Slater, E.C. (1967) Application of inhibitors and uncouplers for a study of oxidative phosphorylation. Methods Enzymol. 10, 48–57

    Google Scholar 

  • Tallman, G. (1992) The chemiosmotic model of stomatal opening revisited. Crit. Rev. Plant Sci. 11(1), 35–57

    Google Scholar 

  • Vavasseur, A., Lascere, G., Couchat, P. (1990) Different stomatal responses of maize leaves after blue and red illumination under anoxia. Plant Cell Environ. 13, 389–394

    Google Scholar 

  • Zeiger, E. (1983) The biology of stomatal cells. Annu. Rev. Plant Physiol. 34, 441–475

    Google Scholar 

  • Zeiger, E. (1991) Light perception in guard cells. Plant Cell Environ. 13, 739–747

    Google Scholar 

  • Zeiger, E., Iino, M., Shimazaki, K., Ogawa, T. (1987) The blue-light response of stomata: Mechanism and function. In: Stomatal function, pp. 209–227, Zeiger, E., Farquhar, G.D., Cowan, I. eds. Stanford University Press, Stanford, USA

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Plant Physiology Research Group, Department of Biological Sciences, The University of Calgary, T2N 1N4, Calgary, Alberta, Canada

    B. T. Mawson

Authors
  1. B. T. Mawson
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

This research was supported by an operating grant from the Natural Sciences and Engineering Research Council of Canada and a University Research Grant from The University of Calgary. Dr. L. Gedamu (University of Calgary) is thanked for providing access to the bioluminometer. Technical assistance by C. Chmielewski, C. Turnnir, S. Ham and K. Meyer is gratefully acknowledged.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mawson, B.T. Regulation of blue-light-induced proton pumping by Vicia faba L. guard-cell protoplasts: Energetic contributions by chloroplastic and mitochondrial activities. Planta 191, 293–301 (1993). https://doi.org/10.1007/BF00195685

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00195685

Key words

Search

Navigation