Skip to main content
SpringerLink
Log in

Gibberellic acid induces cytoplasmic acidification in maize coleoptiles

  • Published:
Planta Aims and scope Submit manuscript

Abstract

Indole-3-acetic acid (IAA), fusicoccin and weak acids all lower the cytoplasmic pH (pHi) and induce elongation growth of maize (Zea mays L.) coleoptiles. Gibberellic acid (GA3) also induces elongation growth and we have used confocal laser scanning microscopy to study the effects of GA3 on pHi employing the pH-indicator dyes, 2′,7′-bis(2-carboxyethyl)-5-(and-6) carboxyfluorescein and carboxy-semi-naphthorhodafluor-1. We confirm that GA3 induces growth significantly in light-grown but only slightly or not at all in dark-grown coleoptiles. The growth induced by IAA treatment was similar in light- and dark-grown coleoptiles. The pHi decreased by up to 0.6 units during the first 7 min of GA3 or IAA treatment of both light- and dark-grown coleoptiles. Gibberellic acid inhibited IAA-induced growth of dark-grown coleoptiles. Hence, in dark-grown coleoptiles GA3 may activate either directly or indirectly reactions that interfere with the signalling pathway leading to elongation growth. The possible role of pHi in growth is discussed.

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

ABA:

abscisic acid

AM:

acetoxymethyl ester

BCECF:

2′,7′-bis(2-carboxyethyl)-5-(and-6) carboxyfluorescein

[Ca2+]i :

cytoplasmic free calcium

GA(n) :

gibberellin A(n)

GA3 :

gibberellic acid

IAA:

indole-3-acetic acid

PGR:

plant growth regulator

pHi :

cytoplasmic pH

Pipes:

piperazine-N,N′-bis[2-ethanesulfonic acid]

Snarf-1:

carboxy-semi-naphthorhodafluor-1

References

  • Armstrong, C., Gehring, C.A., Irving, H.R., Parish, R.W. (1993) Do changes in cytosolic pH modulate transcription of a dehydrin gene?. Abstr. Aust. Soc. Plant Physiol. 33, P38

    Google Scholar 

  • Adams, P.A., Montague, M.J., Tepfer, M., Rayle D.L., Ikuma, H., Kaufman, P.B. (1975) Effect of gibberellic acid on the plasticity and elasticity of Avena stem segments. Plant Physiol. 56, 757–760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bassnett, S., Reinisch, L., Beebe, D.C. (1990) Intracellular pH measurement using single excitation-dual emission fluorescence ratios. Am. J. Physiol. 258, 171–178

    Google Scholar 

  • Blatt, M.R., Armstrong, F. (1993) K+ channels of stomatal guard cells: abscisic-acid-evoked control of the outward rectifier by cytoplasmic pH. Planta191, 330–341

    Article  CAS  Google Scholar 

  • Brummer, B., Felle, H., Parish, R.W. (1984a) Evidence that acid solutions induce plant cell elongation by acidifying the cytosol and stimulating the proton pump. FEBS Letts. 174, 223–227

    Article  CAS  Google Scholar 

  • Brummer, B., Potrykus, I., Parish, R.W. (1984b) The roles of cell-wall acidification and proton-pump stimulation in auxin-induced growth: studies using monensin. Planta162, 345–352

    Article  CAS  PubMed  Google Scholar 

  • Brummer, B., Bertl, A., Potrykus, I., Felle, H., Parish, R.W. (1985) Evidence that fusicoccin and indole-3-acetic acid induce cytosolic acidification of Zea mays cells. FEBS Letts. 189, 109–113

    Article  CAS  Google Scholar 

  • Busa, W.B. (1986) Mechanisms and consequences of pH-mediated cell regulation. Annu. Rev. Physiol. 48, 389–402

    Article  CAS  PubMed  Google Scholar 

  • Busa, W.B., Nuccitelli, R. (1984) Metabolic regulation via intracellular pH. Am. J. Physiol. 246, 409–438

    Google Scholar 

  • Cosgrove, D.J., Sovonick-Dunford, S.A. (1989) Mechanism of gibberellin-dependent stem elongation in peas. Plant Physiol. 89, 184–191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davies, P.J. (1987) plant hormones: their nature, occurrence, and functions. In Plant hormones and their role in plant growth and development, pp. 1–12, Davies, P.J., ed. Martinus Nijhoff, Dordrecht, The Netherlands

    Chapter  Google Scholar 

  • Felle, H. (1988a) Auxin causes oscillations of cytosolic free calcium and pH in Zea mays coleoptiles. Planta174, 495–499

    Article  CAS  PubMed  Google Scholar 

  • Felle, H. (1988b) Cytoplasmic free calcium in Riccia fluitans L. andZea mays L.: Interactions of Ca2+ and pH? Planta176, 248–255

    Article  CAS  PubMed  Google Scholar 

  • Felle, H., Brummer, B., Bertl, A., Parish, R.W. (1986) Indole-3-acetic acid and fusicoccin cause cytosolic acidification of corn coleoptile cells. Proc. Natl. Acad. Sci. USA83, 8992–8995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gehring, C.A., Irving, H.R., Parish, R.W. (1990) Effects of auxin and abscisic acid on cytosolic calcium and pH in plant cells. Proc. Natl. Acad. Sci. USA87, 9645–9649

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gilroy, S., Jones, R.L. (1992) Gibberellic acid and abscisic acid coordinately regulate cytoplasmic calcium and secretory activity in barley aleurone protoplasts. Proc. Natl. Acad. Sci. USA89, 3591–3595

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hager, A., Menzel, H., Krauss, A. (1971) Versuche und Hypothese zur Primärwirkung des Auxines beim Streckungswachstum. Planta100, 47–75

    Article  CAS  PubMed  Google Scholar 

  • Hooley, R., Beale, M.H., Smith, S. (1991) Gibberellin perception at the plasma membrane of Avena fatua aleurone protoplasts. Planta183, 274–280

    Article  CAS  PubMed  Google Scholar 

  • Irving, H.R., Gehring, C.A., Parish, R.W. (1992a) Changes in cytosolic pH and calcium of guard cells precede stomatal movement. Proc. Natl. Acad. Sci. USA89, 1790–1794

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Irving, H.R., Gehring, C.A., Parish, R.W. (1992b) Gibberellic acid induces changes of cytosolic free calcium and pH. (Abstr. no. 836). Plant Physiol. 99, Suppl., 140

    Article  Google Scholar 

  • Jacobsen, J.V., Beach, L.R. (1985) Control of transcription of α-amylase and rRNA genes in barley aleurone protoplasts by gibberellin and abscisic acid. Nature316, 275–277

    Article  CAS  Google Scholar 

  • Keyes, G., Sorrells, M.E., Setter, T.L. (1990) Gibberellic acid regulates cell wall extensibility in wheat (Triticum aestivum L.). Plant Physiol. 92, 242–245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kutschera, U., Schopfer, P. (1986) Effects of auxin and abscisic acid on cell wall extensibility in maize coleoptiles. Planta167, 527–535

    Article  CAS  PubMed  Google Scholar 

  • Marra, M., Ballio, A., Fullone, M.R., Aducci, P. (1992) Some properties of a functional reconstituted plasmalemma H+-ATPase activated by fusicoccin. Plant Physiol. 98, 1029–1034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marrè, E. (1979) Fusicoccin: a tool in plant physiology. Annu. Rev. Plant. Physiol. 30, 273–288

    Article  Google Scholar 

  • Moll, C., Jones, R.L. (1981a) Short-term kinetics of elongation growth of gibberellin-responsive lettuce hypocotyl sections. Planta152, 442–449

    Article  CAS  PubMed  Google Scholar 

  • Moll, C., Jones, R.L. (1981b) Calcium and gibberellin-induced elongation of lettuce hypocotyl sections. Planta152, 450–456

    Article  CAS  PubMed  Google Scholar 

  • Phinney, B.O. (1985) Gibberellin A1 dwarfism and shoot elongation in higher plants. Biol. Plant. 27, 172–179

    Article  CAS  Google Scholar 

  • Pierre, J.N., Pacquit, V., Vidal, J., Gadal, P. (1992) Regulatory phosphorylation of phosphoenolpyruvate carboxylase in protoplasts fromSorghum mesophyll cells and the role of pH and Ca2+ as possible components of the light transduction pathway. Eur. J. Biochem. 210, 531–537

    Article  CAS  PubMed  Google Scholar 

  • Rayle, D.L., Cleland, R.E. (1992) The acid growth theory of auxin-induced cell elongation is alive and well. Plant Physiol. 99, 1271–1274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Read, N.D., Allan, W.T.G., Knight, H., Knight, M.R., Malho, R., Russell, A., Shacklock, P.S., Trewavas, A.J. (1992) Imaging and measurement of cytosolic free calcium in plant and fungal cells. J. Microscopy166, 57–86

    Article  CAS  Google Scholar 

  • Reid, J.B., Ross, J.J. (1989) Internode length in Pisum. Two further gibberellin-insensitivity genes,lka andlkb. Physiol. Plant. 75, 81–88

    Article  CAS  Google Scholar 

  • Rink, T.J., Tsien, R.Y., Pozzan, T. (1982) Cytoplasmic pH and free Mg2+ in lymphocytes. J. Cell Biol. 95, 189–196

    Article  CAS  PubMed  Google Scholar 

  • Rood, S.B., Buzzell, R.I., Mander, L.N., Pearce, D., Pharis, R.P. (1988) Gibberellins: a phytohormonal basis for heterosis in maize. Science241, 1216–1218

    Article  CAS  PubMed  Google Scholar 

  • Roos, W. (1992) Confocal pH topography in plant cells — acidic layers in the peripheral cytoplasm and apoplast. Bot. Acta105, 253–259

    Article  CAS  Google Scholar 

  • Seksek, O., Henry-Toulmé, N., Sureau, F., Bolard, J. (1991) SNARF-1 as an intracellular pH indicator in laser microspectrofluorometry: a critical assessment. Anal. Biochem. 193, 49–54

    Article  CAS  PubMed  Google Scholar 

  • Silk, W.K., Jones, R.L. (1975) Gibberellin response in lettuce hypocotyl sections. Plant Physiol. 56, 267–272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stuart, D.A., Jones, R.L. (1977) Roles of extensibility and turgor in gibberellin- and dark-stimulated growth. Plant Physiol. 59, 61–68

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stuart, D.A., Jones, R.L. (1978) The role of acidification in gibberellic acid- and fusicoccin-induced elongation growth of lettuce hypocotyl sections. Planta142, 135–145

    Article  CAS  PubMed  Google Scholar 

  • Taylor, A., Cosgrove, D.J. (1989) Gibberellic acid stimulation of cucumber hypocotyl elongation. Plant Physiol. 90, 1335–1340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van der Veen, R., Heimovaara-Dijkstra, S., Wang, M. (1992) Cytosolic alkalinization mediated by abscisic acid is necessary, but not sufficient, for abscisic acid-induced gene expression in barley aleurone protoplasts. Plant Physiol. 100, 699–705

    Article  PubMed  PubMed Central  Google Scholar 

  • Wolosin, J.M., Chen, M., Gordon, R.E., Stegman, Z., Butler, G.A.D. (1993) Separation of the rabbit ciliary epithelial layers in viable form: identification of differences in bicarbonate transport. Exp. Eye Res. 56, 401–409

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Author notes

  1. Heien R. Irving

    Present address: School of Pharmacology, Victorian College of Pharmacy, Monash University, Parkville Campus, 3052, Melbourne, Australia

Authors and Affiliations

  1. School of Botany, La Trobe University, Bundoora Campus, 3083, Melbourne, Australia

    Christoph A. Gehring, Heien R. Irving & Roger W. Parish

Authors
  1. Christoph A. Gehring
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Heien R. Irving
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Roger W. Parish
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

We thank Dr R. King (CSIRO, Canberra) for providing the GA1 and T. Phillips for processing the photographic material. H.R. Irving was supported by an Australian Research Council Research Fellowship and the work was supported by an Australian Research Council grant.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gehring, C.A., Irving, H.R. & Parish, R.W. Gibberellic acid induces cytoplasmic acidification in maize coleoptiles. Planta 194, 532–540 (1994). https://doi.org/10.1007/BF00714467

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00714467

Key words

Search

Navigation