Skip to main content
SpringerLink
Log in

Rapid alterations in growth rate and electrical potentials upon stem excision in pea seedlings

  • Published:
Planta Aims and scope Submit manuscript

Abstract

Excision of the epicotyl base of pea (Pisum sativum L.) seedlings in air results in a fast drop in the growth rate and rapid transient membrane depolarization of the surface cells near the cut. Subsequent immersion of the cut end into solution leads to a rapid, transient rise in the epicotyl growth rate and an acropetally propagating depolarization with an amplitude of about 35 mV and a speed of approx. 1 mm · s−1. The same result can be achieved directly by excision of the pea epicotyl under water. Shape, amplitude and velocity of the depolarization characterize it as a “slow-wave potential”. These results indicate that the propagating depolarization is caused by a surge in water uptake. Neither a second surge in water uptake (measured as a rapid increase in growth rate when the cut end was placed in air and then back into solution) nor another cut can produce the depolarization a second time. Cyanide suppresses the electrical signal at the treated position without inhibiting its transmission through this area and its development in untreated parts of the epicotyl. The large depolarization and repolarization which occur in the epidermal and subepidermal cells are not associated with changes in cell input resistance. Both results indicate that it is a transient shut-down of the plasma-membrane proton pump rather than large ion fluxes which is causing the depolarization. We conclude that the slow wave potential is spread in the stem via a hydraulic surge occurring upon relief of the negative xylem pressure after the hydraulic resistance of the root has been removed by excision.

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

GR:

growth rate

Px :

xylem pressure

Rin :

cell input resistance

SWP:

slow wave potential

Vm :

membrane potential

Vs :

surface potential

References

  • Acevedo, E., Hsiao, T.C., Henderson, D.W. (1971) Immediate and subsequent growth responses of maize leaves to changes in water status. Plant Physiol. 48, 631–636

    Google Scholar 

  • Bentrup, F.-W. (1989) Cell electrophysiology and membrane transport. Progr. Bot. 5, 70–79

    Google Scholar 

  • Bertl, A., Gradmann, D. (1987) Current-voltage relationships of potassium channels in the plasmalemma of Acetabalaria. J. Membr. Biol. 99, 41–49

    Google Scholar 

  • Blatt, M.R. (1987) Electrical characteristics of stomatal guard cells: the ionic basis of the membrane potential and the consequence of potassium chloride leakage from microelectrodes. Planta 170, 272–287

    Google Scholar 

  • Chastain, C.J., Hanson, J.B. (1982) Control of proton efflux from corn root tissue by an injury-sensing mechanism. Plant Sci. Lett. 24, 97–104

    Google Scholar 

  • Cosgrove, D.J. (1982) Rapid inhibition of hypocotyl growth by blue light in Sinapis alba L. Plant Sci. Lett. 25, 305–312

    Google Scholar 

  • Cosgrove, D.J. (1987) Wall relaxation in growing stems: comparison of four species and assessment of measurement techniques. Planta 171, 266–278

    Google Scholar 

  • Cosgrove, D.J. (1988) Mechanism of rapid suppression of cell expansion in cucumber hypocotyls after blue-light irradiation. Planta 176, 109–116

    Google Scholar 

  • Cosgrove, D.J., Hedrich, R. (1991) Stretch-activated chloride, potassium, and calcium channels coexist in plasma membranes of guard cells. Planta 186, 143–153

    Google Scholar 

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

    Google Scholar 

  • Coster, H.G., Steudle, E., Zimmermann, U. (1977) Turgor pressure sensing in plant cell membranes. Plant Physiol. 58, 636–643

    Google Scholar 

  • Davies, E. (1987) Action potentials as multifunctional signals in plants: a unifying hypothesis to explain apparently disparate wound responses. Plant Cell and Envir. 10, 623–631

    Google Scholar 

  • Davies, E., Schuster, A. (1981) Intercellular communication in plants: Evidence for a rapidly generated, bidirectionally transmitted wound signal. Proc. Natl. Acad. Sci. USA, 78, 2422–2426

    Google Scholar 

  • Drake, G.A., Carr, D.J., Anderson, W.P. (1978) Plasmolysis, plasmodesmata, and the electrical coupling of oat coleoptile cells. J. Exp. Bot. 29, 1205–1214

    Google Scholar 

  • Eschrich, W., Fromm, J., Evert, R.F. (1988) Transmission of electric signals in sieve tubes of zucchini plants. Bot. Acta 101, 327–331

    Google Scholar 

  • Falk, S.O. (1966) Quantitative determinations of the effect of excision on transpiration. Physiol. Plant. 19, 493–522

    Google Scholar 

  • Falke, L.C., Edwards, K.L., Pickard, B.G., Misler, S. (1988) A stretch-activated anion channel in tobacco protoplasts. FEBS Lett. 77, 141–144

    Google Scholar 

  • Felle, H. (1981) A study of the current-voltage relationships of electrogenic active and passive membrane elements in Riccia fluitans. Biochim. Biophys. Acta 646, 151–160

    Google Scholar 

  • Frachisse, J.-M., Desbiez, M.-O. (1989) Investigation of the wave of electric depolarization induced by wounding in Bidens pilosus L.: effects of weak acids on the transmembrane potential and on the elicitation of the wave. Biochem. Physiol. Pflanz. 185, 357–368

    Google Scholar 

  • Gradmann D. (1976) “Metabolic” action potentials in Acetabularia. J. Membr. Biol. 29, 23–45

    Google Scholar 

  • Haberlandt, G. (1914) Physiological plant anatomy, repr. 1965 by Today & Tomorrows Book Agency, New Delhi, India

  • Heydt, H., Steudle, E. (1991) Measurement of negative pressure in the xylem of excised roots. Effects on water and solute relations. Planta 184, 389–396

    Google Scholar 

  • Higinbotham, N., Hope, A.B., Findlay, G.P. (1964) Electrical resistance of cell membranes of Avena coleoptiles. Science 143, 1448–1449

    Google Scholar 

  • Julien, J.L., Desbiez, M.O., de Jaegher, G., Frachisse, J.M. (1991) Characteristics of the wave of depolarization induced by wounding in Bidens pilosa L. J. Exp. Bot. 42, 131–137

    Google Scholar 

  • Kawano, K. (1955) Electrical change caused by blazing in a non-sensitive plant. Bot. Mag. Tokyo 68, 337–341

    Google Scholar 

  • Kinraide, T.B., Wyse, R.E. (1986) Electrical evidence for turgor inhibition of proton extrusion in sugar beet taproot. Plant Physiol. 82, 1148–1150

    Google Scholar 

  • Koopowitz, H., Dhyse, R., Fosket, D.E. (1975) Cell membrane potentials of higher plants: changes induced by wounding. J. Exp. Bot. 26, 131–137

    Google Scholar 

  • Malone, M., Stankowic, B (1991) Surface potentials and hydraulic signals in wheat leaves following localised wounding by heat. Plant Cell Environ. 14, 431–436

    Google Scholar 

  • McIntyre, G.I., Boyer, J.S. (1984) The effect of humidity, root excision, and potassium supply on hypocotyl elongation in dark-grown seedlings of Helianthus annuus. Can. J. Bot. 62, 420–428

    Google Scholar 

  • Mertz, S.M., Higinbotham, N. (1976) Transmembrane electropotential in barley roots as related to cell type, cell location, and cutting and aging effects. Plant Physiol. 57, 123–128

    Google Scholar 

  • Molz, F.J., Boyer, J.S. (1978) Growth-induced water potentials in plant cells and tissues. Plant Physiol. 62, 423–429

    Google Scholar 

  • Morris, C.E. (1990) Mechanosensitive ion channels. J. Membr. Biol. 113, 93–107

    Google Scholar 

  • Nonami, H., Boyer, J.S. (1990) Primary events regulating stem growth at low water potentials. Plant Physiol. 94, 1601–1609

    Google Scholar 

  • Okamoto, H., Mizuno, A., Katou, K., Ono, Y., Matsumura, Y., Kojima, H. (1984) A new method in growth electro-physiology: pressurized intraorgan perfusion. Plant Cell Environ. 7, 139–147

    Google Scholar 

  • Okamoto, H., Liu, Q., Nakahori, K., Katou, K. (1989) A pressurejump method as a new tool in growth physiology for monitoring physiological wall extensibility and effective turgor. Plant Cell Physiol. 30, 979–985

    Google Scholar 

  • Pickard, B.G. (1971) Action potentials resulting from the mechanical stimulation of pea epicotyls. Planta 97, 106–115

    Google Scholar 

  • Pierce, W.S., Hendrix, D.L. (1981) Electrochemical aging responses in Pisum: cellular adaptations or recovery from injury? Plant Physiol. 67, 864–868

    Google Scholar 

  • Racusen, R.H. (1976) Phytochrome control of electrical potentials and intercellular coupling in oat-coleoptile tissue. Planta 132, 25–29

    Google Scholar 

  • Raschke, K. (1970) Stomatal responses to pressure changes and interruptions in the water supply of detached leaves of Lea mays L. Plant Physiol. 45, 415–423

    Google Scholar 

  • Retivin, V.G., Opritov, V.A. (1987) Cable properties of the stem of higher plants. Fiziol. Rast. 34, 5–12

    Google Scholar 

  • Roblin, G., Bonnemain, J.-L. (1985) Propagation in Vicia faba stem of a potential variation by wounding. Plant Cell Physiol. 26, 1273–1283

    Google Scholar 

  • Rubinstein, B. (1977) Osmotic shock inhibits auxin-stimulated acidification and growth. Plant Physiol. 59, 369–371

    Google Scholar 

  • Rubinstein, B. (1982) Regulation of H+ excretion. Plant Physiol. 69, 939–944

    Google Scholar 

  • Savage, M.J., Cass, A., Wiebe, H.H. (1984) Effect of excision on leaf water potential. J. Exp. Bot. 35, 204–208

    Google Scholar 

  • Schildknecht, H. (1984) Turgorins — new chemical messengers for plant behaviour. Endeavour N.S. 8, 113–117

    Google Scholar 

  • Schmalstig, J.G., Cosgrove, D.J. (1990) Coupling of solute transport and cell expansion in pea stems. Plant Physiol. 94, 1625–1633

    Google Scholar 

  • Sibaoka, T. (1953) Some aspects on the slow conduction of stimuli in the leaf of Mimosa pudica. Sci. Rep. Tohoku Univ. 20, 72–88

    Google Scholar 

  • Sibaoka, T. (1966) Action potentials in plant organs. Symp. Soc. Exp. Biol. 20, 49–73

    Google Scholar 

  • Sibaoka, T., Tabata, T. (1981) Electrotonic coupling between adjacent internodal cells of Chara braunii: transmission of action potentials beyond the node. Plant Cell Physiol. 22, 397–411

    Google Scholar 

  • Sinyukhin, A.M. (1964) Electrophysiological investigations in phloem cells in higher plants [In Russ.]. Izvest. Timiryazevskoi Sel'sko-khoz. Akad. (Moscow) 3, 59–69

    Google Scholar 

  • Spanswick, R.M. (1972) Electrical coupling between cells of higher plants: A direct demonstration of intercellular communication. Planta 102, 215–227

    Google Scholar 

  • Spanswick, R.M., Costerton, J.W.F. (1967) Plasmodesmata in Nitella translucens: Structure and electrical resistance. J. Cell Sci. 2, 451–464

    Google Scholar 

  • Stahlberg, R. (1980) Elektrische Potentiale im Zusammenhang mit Wachstumsprozessen bei Pflanzen. Ber. Humboldt Univ. Berlin 1, 13–20

    Google Scholar 

  • Stahlberg, R., Cosgrove, D.J. (1990) Rapid alterations in stem growth rate and surface electric potentials upon excision. (Abstr.) Plant Physiol. 93, Suppl., 74

    Google Scholar 

  • Stahlberg, R., Polevoi, V.V. (1979) Nature of rhythmic oscillations of the membrane potential in corn coleoptile cells. Dokl. Akad. Nauk SSSR 247, 74–76

    Google Scholar 

  • Umrath, K. (1927) Ueber die Erregungssubstanz der Mimosoideen. Planta 4, 812–817 Tsaplev, Yu.B., Zatsepina, G.N. (1980) Electrical nature of the spread of a variable potential in Tradescantia. Biofizika 25, 723–728

    Google Scholar 

  • Van Sambeek, J.W., Pickard, B.G., Ulbright, C.E. 1976. Mediation of rapid electrical, metabolic, transpirational and photosynthetic changes by factors released from wounds. II. Mediation of the variation potential by Ricca's factor. Can. J. Bot. 54, 2651–2661

    Google Scholar 

  • Zerrenthin, U., Stahlberg, R. (1981) Die Nutzung der bioelektrischen Kurzzeitreaktion auf mechanische Reizung zur Ermittlung von Kennwerten und Sortenunterschieden bei Getreidekeimpflanzen. Arch. Acker-Pflanzenbau Bodenkd. 25, 197–203

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biology, Pennsylvania State University, 208 Mueller Laboratory, 16802, University Park, PA, USA

    Rainer Stahlberg & Daniel J. Cosgrove

Authors
  1. Rainer Stahlberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Daniel J. Cosgrove
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

This work was supported by grants to D.J.C. from the National Science Foundation and the U.S. Department of Energy.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Stahlberg, R., Cosgrove, D.J. Rapid alterations in growth rate and electrical potentials upon stem excision in pea seedlings. Planta 187, 523–531 (1992). https://doi.org/10.1007/BF00199972

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00199972

Key words

Search

Navigation