Abstract
The effects of exogenous phytohormones (IAA, ABA, and GA3) on the intracellular (cytoplasmic) pH (pHc) in ungerminating and germinating petunia (Petunia hybrida L.) pollen grains were studied. The pHc values were measured with fluorescein diacetate. In ungerminating pollen grains, all phytohormones reduced pHc relatively rapidly; after 10–15 min, initial value was restored. In germinating pollen grains, IAA and ABA induced a relatively rapid cytosol alkalization, which was not reversed during experiment. GA3 acidified the cytosol, i.e., exerted the effect similar to that in ungerminating pollen grains. Sodium orthovanadate suppressed completely the hormone-induced pHc shift toward alkaline values in germinating pollen grains, whereas this inhibitor did not affect pHc in the absence of phytohormones. Sodium orthovanadate also slowed the recovery of pHc after hormone-induced cytoplasm acidification in ungerminating pollen grains, reduced pHc in control ungerminating grains, and weakened substantially the effects of all phytohormones on these pollen grains. On the basis of these results, we suggested that physiological activities of phytohormones in this system were mediated by pHc modulation, namely, a transient disturbance in the cytosolic pH homeostasis, which could trigger further phytohormone-induced cell responses. We concluded that a hormone-induced cytoplasm alkalization in pollen grains was mediated by the activity of their plasma membrane H+-ATPase and that this proton pump was involved in the control of pHc in both germinating and ungerminating pollen grains.
Similar content being viewed by others
Abbreviations
- pHc :
-
intracellular (cytoplasmic) pH
- BCECFAM:
-
2′,7′-bis-(2-carboxyethyl)-5(6′)-carboxyfluorescein acetoxymethyl ester
References
Heslop-Harrison, J., Pollen Germination and Pollen-Tube Growth, Int. Rev. Cytol., 1987, vol. 107, pp. 1–78.
Taylor, L.P. and Hepler, P.K., Pollen Germination and Tube Growth, Annu. Rev. Plant Physiol. Plant Mol. Biol., 1997, vol. 48, pp. 461–491.
De Graaf, B.H.J., Derksen, J.W.M., and Mariani, C., Pollen and Pistil in the Progamic Phase, Sex. Plant Reprod., 2001, vol. 14, pp. 41–55.
Lord, E.M., Adhesion and Guidance in Compatible Pollination, J. Exp. Bot., 2003, vol. 54, pp. 47–54.
Feijo, J.A., Malho, R., and Obermeyer, G., Ion Dynamics and Its Possible Role during In Vitro Pollen Germination and Tube Growth, Protoplasma, 1995, vol. 187, pp. 155–167.
Holdaway-Clarke, T.L. and Hepler, P.K., Control of Pollen Tube Growth: Role of Ion Gradients and Fluxes, New Phytol., 2003, vol. 159, pp. 539–563.
Stanley, R.G. and Linskens, H.F., Pollen (Biology, Biochemistry, Management), Berlin: Springer-Verlag, 1974.
Singh, S. and Sawhney, V.K., Plant Hormones in Brassica napus and Lycopersicon esculentum Pollen, Phytochemistry, 1992, vol. 31, pp. 4051–4053.
Kovaleva, L. and Zakharova, E., Hormonal Status of the Pollen-Pistil System at the Progamic Phase of Fertilization after Compatible and Incompatible Pollination in Petunia hybrida L., Sex. Plant Reprod., 2003, vol. 16, pp. 191–196.
Kovaleva, L.V., Zakharova, E.V., Minkina, Yu.V., Timofeeva, G.V., and Andreev, I.M., Germination and In Vitro Growth of Petunia Male Gametophyte Are Affected by Exogenous Hormones and Involve the Changes in the Endogenous Hormone Level, Russ. J. Plant Physiol., 2005, vol. 52, pp. 521–526.
Cheng, H., Qin, L., Lee, S., Fu, X., Richards, D.E., Cao, D., Luo, D., Harberd, N.P., and Peng, J., Gibberellin Regulates Arabidopsis Floral Development via Suppression of DELLA Protein Function, Development, 2004, vol. 131, pp. 1055–1064.
Levchenko, V., Konrad, K.R., Dietrich, P., Roelfsema, M.R.G., and Hedrich, R., Cytosolic Abscisic Acid Activates Guard Cell Anion Channels without Preceding Ca2+ Signals, Proc. Natl. Acad. Sci. USA, 2005, vol. 102, pp. 4203–4208.
Graber, M.L., DiLillo, D.C., Friedman, B.L., and Pastoriza-Munoz, E., Characteristics of Fluoroprobes for Measuring Intracellular pH, Anal. Biochem., 1986, vol. 156, pp. 202–212.
Fricker, M.D., White, N.S., and Obermeyer, G., pH Gradients Are Not Associated with Tip Growth in Pollen Tubes of Lilium longiflorum, J. Cell Sci., 1997, vol. 110, pp. 1729–1740.
Tanasugarn, L., McNeil, P., Reynolds, G.T., and Taylor, L., Microspectrofluorometry by Digital Image Processing: Measurement of Cytoplasmic pH, J. Cell Biol., 1984, vol. 98, pp. 717–724.
D’Agostino, I.B. and Kieber, J.J., Molecular Mechanisms of Cytokinin Action, Curr. Opin. Plant Biol., 1999, vol. 2, pp. 359–364.
Walker, L. and Estelle, M., Molecular Mechanisms of Auxin Action, Curr. Opin. Plant Biol., 1998, vol. 1, pp. 434–439.
Robertson, M., Swain, S.M., Chandler, P.M., and Olszewski, N.E., Identification of a Negative Regulator of Gibberellin Action, HvSPY, in Barley, Plant Cell, 1998, vol. 10, pp. 995–1007.
Weijers, D. and Jurgens, G., Funneling Auxin Action: Specificity in Signal Transduction, Curr. Opin. Plant Biol., 2004, vol. 7, pp. 687–693.
Kulaeva, O.N. and Prokoptseva, O.S., Up-to-Date Progress in the Investigation of Phytohormone Action Mechanism, Biokhimiya, 2004, vol. 69, pp. 293–310.
Nemhauser, J.L., Hong, F., and Chory, J., Different Plant Hormones Regulate Similar Processes through Largely Nonoverlapping Transcriptional Responses, Cell, 2006, vol. 126, pp. 467–475.
Brault, M., Amiar, Z., Pennarun, A.-M., Monestiez, M., Zhang, Z., Cornel, D., Dellis, O., Knight, H., Bouteau, F., and Rona, J.-P., Plasma Membrane Depolarization Induced by Abscisic Acid in Arabidopsis Suspension Cells Involves Reduction of Proton Pumping in Addition to Anion Channel Activation, Which Are Both Ca2+ Dependent, Plant Physiol., 2004, vol. 135, pp. 231–243.
Zalejski, C., Zhang, Z., Quettier, A.L., Maldiney, R., Bonnet, M., Brault, M., Demandre, C., Rona, J.-P., Sotta, B., and Jeannette, E., Diacylglycerol Pyrophosphate Is a Second Messenger of Abscisic Acid Signaling in Arabidopsis thaliana Suspension Cells, Plant J., 2005, vol. 42, pp. 145–152.
Zhang, Z., Ramirez, J., Reboutier, D., Brault, M., Trouverie, J., Pennarun, A.M., Amiar, Z., Biligui, B., and Galagovsky, L., Brassinosteroids Regulate Plasma Membrane Anion Channels in Addition to Proton Pumps during Expansion of Arabidopsis thaliana Cells, Plant Cell Physiol., 2005, vol. 46, pp. 1494–1504.
Zalejski, C., Paradis, S., Maldiney, R., Habricot, Y., Miginiac, E., and Rona, J.-P., Induction of ABA-Regulated Gene Expression by Diacylglycerol Pyrophosphate Involves Ca2+ and Anion Currents in Arabidopsis thaliana Suspension Cells, Plant Physiol., 2006, vol. 141, pp. 1555–1562.
Matveeva, N.P., Andreyuk, D.S., Voitsekh, O.O., and Ermakov, I.P., Regulatory Changes in the Intracellular pH and Cl− Efflux at Early Stages of Pollen Grain Germination In Vitro, Russ. J. Plant Physiol., 2003, vol. 50, pp. 318–323.
Obermeyer, G., Lutzelschwab, M., Heumann, H.-G., and Weisenseel, M.H., Immunolocalization of H+-ATPase in the Plasma Membrane of Pollen Grains and Pollen Tubes of Lilium longiflorum, Protoplasma, 1992, vol. 171, pp. 55–63.
Pertl, H., Himly, M., Gehwolf, R., Kriechbaumer, R., Strasser, D., Michalke, W., Ferreira, F., and Obermeyer, G., Molecular and Physiological Characterization of a 14-3-3 Protein from Lily Pollen Grains Regulating the Activity of the Plasma Membrane H+-ATPase during Pollen Grain Germination and Tube Growth, Planta, 2001, vol. 213, pp. 132–141.
Felle, H., Brummer, B., Bertl, A., and Parish, R.W., Indole-3-Acetic Acid and Fusicoccin Cause Cytosolic Acidification of Corn Coleoptile Cells, Proc. Natl. Acad. Sci. USA, 1986, vol. 83, pp. 8992–8995.
Gehring, C.A., Irving, H.R., and Parish, R.W., Gibberellic Acid Induces Cytoplasmic Acidification in Maize Coleoptiles, Planta, 1994, vol. 194, pp. 532–540.
Kramer, E.M., How Far Can a Molecule of Weak Acid Travel in the Apoplast or Xylem? Plant Physiol., 2006, vol. 141, pp. 1233–1236.
Yang, Y., Hammes, U.Z., Taylor, C.G., Schachtman, D.P., and Nielsen, E., High-Affinity Auxin Transport by the AUX1 Influx Carrier Protein, Curr. Biol., 2006, vol. 16, pp. 1123–1127.
Author information
Authors and Affiliations
Corresponding author
Additional information
Original Russian Text © I.M. Andreev, G.V. Timofeeva, Yu.V. Minkina, L.V. Kovaleva, 2007, published in Fiziologiya Rastenii, 2007, Vol. 54, No. 5, pp. 707–714.
Rights and permissions
About this article
Cite this article
Andreev, I.M., Timofeeva, G.V., Minkina, Y.V. et al. Effects of exogenous phytohormones on intracellular pH of Petunia hybrida pollen grains. Russ J Plant Physiol 54, 626–632 (2007). https://doi.org/10.1134/S1021443707050093
Received:
Issue Date:
DOI: https://doi.org/10.1134/S1021443707050093