Abstract
Slow wave potentials (SWPs) are transient depolarizations which propagate substantial distances from their point of origin. They were induced in the epidermal cells of pea epicotyls by injurious methods such as root excision and heat treatment, as well as by externally applied, defined steps in xylem pressure (Px)at in the absence of wounding. The common principle of induction was a rapid increase in Px. Such a stimulus appeared under natural conditions after (i) bending of the epicotyl, (ii) wounding of the epidermis, (iii) rewatering of dehydrated roots, and (iv) embolism. The induced depolarization was not associated with a change in cell input resistance. This result and the ineffectiveness of ion channel blockers point to H+-pumps rather than ion channels as the ionic basis of the SWP. Stimuli such as excision, heat treatment and pressure steps, which generate SWPs, caused a transient increase in the fluorescence intensity of epicotyls loaded with the pH-indicator DM-NERF, a 2′, 7′-dimethyl derivative of rhodol, but not of those loaded with the pH indicator 2′,7′-bis-(2-carboxyethyl)-5-(and-6)-carboxyfluorescein (BCECF). Matching kinetics of depolarization and pH response identify a transient inactivation of proton pumps in the plasma membrane as the causal mechanism of the SWP. Feeding pump inhibitors to the cut surface of excised epicotyls failed to chemically simulate a SWP; cyanide, azide and 2,4-dinitrophenol caused sustained, local depolarizations which did not propagate. Of all tested substances, only sodium cholate caused a transient and propagating depolarization whose arrival in the growing region of the epicotyl coincided with a transient growth rate reduction.
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Abbreviations
- AP:
-
action potential
- BCECF:
-
2′,7′-bis-(2-carboxyethyl)-5-(and-6)-carboxyfluorescein
- DM-NERF 2′,7′:
-
dimethyl derivative of rhodol
- GR:
-
growth rate
- Px :
-
xylem pressure
- Rin :
-
cell input resistance
- SWP:
-
slow wave potential
- Vm :
-
membrane potential
- Vs :
-
surface potential
References
Alarcon J-J, Malone M (1994) Substantial hydraulic signals are triggered by leaf-biting insects in tomato. J Exp Bot 45: 953–957
Boari F, Malone M (1993) Rapid and systemic hydraulic signals are induced by localized wounding in a wide range of species. J Exp Bot 44: 741–746
Cheeseman JM, Pickard BG (1977) Depolarization of cell membranes in leaves of Lycopersicon by extract containing Ricca's factor. Can J Bot 55: 511–519
Cosgrove DJ (1981) Rapid suppression of growth by blue light. Occurrence, time course, and general characteristics. Plant Physiol 67: 584–590
Davies E, Zawadzki T, Witters D (1991) Electrical activity and signal transmission in plants: How do plants know? In: Penel C, Grepin H (eds) Plant signalling, plasma membrane and change of state. Université de Geneve, pp 119–137
Felle H (1988) Short-term pH regulation in plants. Physiol Plant 74: 583–591
Gradmann D (1976) “Metabolic” action potentials in Acetabularia. J Membr Biol 29: 23–45
Haugland RP (1992) Handbook of fluorescent probes and research chemicals. Molecular Probes, Eugene USA
Hodick D, Sievers A (1988) The action potential of Dionea muscipula Ellis. Planta 174: 8–18
Houwinck AL (1935) The conduction of excitation in Mimosa pudica. Rec Trav Bot Neerl 32: 51–91
Julien JL, Desbiez MO, de Jaeger G, Frachisse JM (1991) Characteristics of the wave of depolarization induced by wounding in Bidens pilosa L. J Exp Bot 42: 131–137
Kawano K (1955) Electrical change caused by blazing in a nonsensitive plant. Bot Mag 68: 337–341
Kourie JI (1994) Transient Cl and K currents during the action potential in Chara inflata. Effects of external sorbitol, cations, and ion channel blockers. Plant Physiol 106: 651–660
Kurkdijan M, Guern J (1989) Intracellular pH: measurement and importance in cell activity. Annu Rev Plant Physiol Mol Biol 40: 271–303
Malone M (1992) Kinetic of wound-induced hydraulic signals and variation potentials in wheat seedlings. Planta 187: 505–510
Malone M (1996) Rapid, long-distance signal transmission in higher plants. Adv Bot Res 22: 163–228
Malone M, Stankovic B (1991) Surface potentials and hydraulic signals in wheat leaves following localized wounding by heat. Plant Cell Environ 14: 431–436
Moyen C, Johannes E (1996) Systemin transiently depolarizes the tomato mesophyll cell membrane and antagonizes fusicoccininduced extracellular acidification of mesophyll tissue. Plant Cell Environ 19: 464–470
Reinhold L, Seiden A, Volokita M (1984) Is modulation of the rate of proton pumping a key event in osmoregulation? Plant Physiol 75: 846–849
Ricca U (1916) Soluzione d'un problema di fisiologia. La propagazione di stimulo nella Mimosa. Nuovo Giorn Bot Ital 23: 51–170
Roblin G, Bonnemain J-L (1985) Propagation in Vicia faba stem of a potential variation by wounding. Plant Cell Physiol 26: 1273–1283
Rubinstein B (1977) Osmotic shock inhibits auxin-stimulated acidification and growth. Plant Physiol 59: 369–371
Rubinstein B (1982) Regulation of H excretion. Plant Physiol 69: 939–944
Schildknecht H (1978) Über die Chemie der Sinnpflanze Mimosa pudica L. Springer, Berlin
Schildknecht H (1984) Turgorins -new chemical messengers for plant behaviour. Endeavor 8: 113–117.
Spanjers AW (1981) Bioelectric potential changes in the style of Lilium longiflorum Thunb. after self- and cross-pollination of the stigma. Planta 153: 1–5
Stahlberg R, Cosgrove DJ (1992) Rapid alterations in growth rate and electrical potentials upon stem excision in pea seedlings. Planta 187: 523–531
Stahlberg R, Cosgrove DJ (1994) Comparison of electric and growth responses to excision in cucumber and pea seedlings. I. Shortdistance effects are due to wounding. Plant Cell Environ 17: 1143–1151
Stahlberg R, Cosgrove DJ (1995) Comparison of electric and growth responses to excision in cucumber and pea seedlings. II. Longdistance effects are due to hydraulic signals. Plant Cell Environ 18: 33–41
Tester M (1990) Plant ion channels: whole-cell and single-channel studies. New Phytol 114: 305–3
Thain JF, Grubb IR, Wildon DC (1995) Depolarization of tomato leaf cells by oligogalacturonide elicitors. Plant Cell Environ 18: 2111–214
Tsaplev YB, Zatsepina GN (1980) Electrical nature of the propagation of a variation potential in Tradescantia. Biofizika 25: 723–728
Umrath K (1959) Der Erregungsvorgang. In: Ruhland W (eds) Handbuch der Pflanzenphysiologie 17, 24–110, Springer, Berlin
Van Sambeek JW, Pickard BG, Ulbright W (1976) Mediation of rapid elelctrical, metabolic, transpirational and photosynthetic changes by factors released from wounds. Mediation of the variation potential by Ricca's factor. Can J Bot 54: 2651–2661
Wayne R (1994) The excitability of plant cells: with a special enphasis on Characean internode cells. Bot Rev 60: 265–367
Wendler S, Zimmermann U, Bentrup, FW (1983) Relationship between cell turgor pressure, electrical membrane potential, and chloride efflux in Acetabularia mediterranea. J Membr Biol 72: 75–84
Wildon DC, Doherty HM, Eagles G, Bowles DJ, Thain JF (1989) Systemic responses arising from localized heat stimuli in tomato plants. Ann Bot 64: 691–695
Wildon DC, Thain JF, Minchin PEH, Gubb IR, Reilly AJ, Skipper YD, Doherty HM, O'Donnell PJ, Bowles DJ (1992) Electrical signalling and systemic proteinase inhibitor induction in the wounded plant. Nature 360: 62–65
Zimmermann U, Beckers F (1978) Generation of action potentials in Chara corallina by turgor pressure changes. Planta 138: 173–179
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This work was supported by grants to D.J.C. from the U.S. Department of Energy. We wish to thank R. Cyr, S. Gilroy, J. Lynch, R. Snyder and the Root biology group of the Pennsylvania State University for help and permission to use their equipment, R.E. Cleland and E. Van Volkenburgh for helpful comments on the manuscript.
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Stahlberg, R., Cosgrove, D.J. Induction and ionic basis of slow wave potentials in seedlings of Pisum sativum L.. Planta 200, 416–425 (1996). https://doi.org/10.1007/BF00231397
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DOI: https://doi.org/10.1007/BF00231397