Rapid response of the plasma-membrane potential in oat coleoptiles to auxin and other weak acids

Bates, George W.; Goldsmith, Mary Helen M.

doi:10.1007/bf00397530

Cited by 128 publications

(73 citation statements)

References 33 publications

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“…10-3. V.g-' fresh wt (1) where the amount of extruded protons AH' is expressed as eqg-' fresh weight and V is the incubation volume in ml. In other words, the buffer system at the end of incubation may be thought of as a mixture of the weak acid at the final C, concentration and the final strong base concentration B, as defined above.…”

Section: Methodsmentioning

confidence: 99%

H⁺ Extrusion and Potassium Uptake Associated with Potential Hyperpolarization in Maize and Wheat Root Segments Treated with Permeant Weak Acids

Romani

Marré²,

Bellando³

et al. 1985

Plant Physiol.

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ABSTRACFThe rapid uptake of weak acids permnt in the unchaged form is accompanied in maize and wheat root segments by a hyperpolariztion of the transmembrane electrial potential and an increase in K uptake, suggesting a stimulation of the plasmalemma H' pump. The evalation of weak acid-induced H' extrsion must take into account the alkalinization of the medium due to the rapid uptake of the uncagd form of the acid, partially masking the proton pump-mediated extrusion of H+. The data corrected for this interference show that the lipophilic butyric acid and trimethyl acetic acid induce in maize and in wheat root segts a significant increase in 're H+ extrusion, roughly matching the ise in net K+ uptake. The presence of KV significantly incrases the rte of uptake of the weak acid, possibly as a consequence of an alkinitio of the cytosol associated with K absorption. In maize root seents, the effects of fusicoccin and those of butyric acid on both K+ uptake and H+ extrusion are clearly synergistic, thus suggesting distinct modes of action.These results support the view that the activity of the plasmalemma H+ pump is regulated by the value of cytosolic pH.We have previously reported that the treatment with permeant weak acids (such as butyric, isobutyric, trimethylacetic acids, and DMO2) induces in maize root segments a marked hyperpolarization of the PD (12, 14, 15; see also, for similar results in other materials, 1, 3, 6, 16, and 17). The finding that PD hyperpolarization is associated with an increase in the rate of K+ uptake and is correlated with the rate of penetration of the weak acid and with a decrease in cell sap pH suggested that, in these experiments, the electrogenic proton pump at the plasmalemma is stimulated by the acidification of the cytoplasm consequent to the penetration and the dissociation of the weak acid in the cytosol (compare Sanders et al. [16] for the same conclusion from experiments in Neurospora).If this interpretation is correct, the hyperpolarization associated with weak acid uptake should also be associated with an increase in proton secretion, which had not been demonstrated ' in the above-mentioned investigations. On the other hand, the demonstration of weak acid-induced changes in the rate of H+ extrusion presents some experimental difficulties due in part to the strong buffering action of the weak acids, and also, even more seriously, to the fact that the rapid uptake ofthe uncharged form of the weak acid by the tissue results in an alkalinization of the medium, which may mask the acidification due to the secretion of H+. Thus, for a correct evaluation of the 'true' HI movement across the plasmalemma, the titration values must be corrected for the changes in weak acid concentration.Starting from these premises, in the present work we investigated the changes in 'real' H+ extrusion induced in root segments by treatment with permeant weak acids. The proton extrusion values thus obtained were then compared with the results of experiments in which we invesfigated the effects of wea...

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Section: Methodsmentioning

confidence: 99%

H⁺ Extrusion and Potassium Uptake Associated with Potential Hyperpolarization in Maize and Wheat Root Segments Treated with Permeant Weak Acids

Romani

Marré²,

Bellando³

et al. 1985

Plant Physiol.

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“…As an early event in signal transduction, many physiological stimuli including light signals, plant hormones, elicitors, and pathogens induce membrane depolarization (9)(10)(11)(12)(13)(14)(15)(16) from the normal range of resting potentials found in higher plant cells (approximately -120 to -160 mV). These depolarizations occur transiently, lasting for durations of several tens of seconds, or are sustained and have been shown to be accompanied by anion efflux in several cases (1,2,9,(14)(15)(16).…”

Section: Introductionmentioning

confidence: 99%

Two types of anion channel currents in guard cells with distinct voltage regulation.

Schroeder

Keller

1992

Proc. Natl. Acad. Sci. U.S.A.

254

232

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Transpirational water loss by plants is reduced by closing of stomatal pores in the leaf epidermis. Anion channels in the plasma membrane of guard cells may provide a key molecular mechanism for control of stomatal closing in leaves. However, central questions regarding the regulation, diversity, and function of anion channels in guard cells and other higher plant cells remain unanswered. We show here that two highly distinct types of depolarization-activated anion currents operate in the plasma membrane of Viciafaba guard cells. One described type of anion channel was activated rapidly within 50 ms by depolarization, inactivated during prolonged stimulation, and deactivated rapidly at hyperpolarized potentials (R-type anion current). The other depolarizationactivated anion current showed extremely slow voltagedependent activation and deactivation (S-type anion current) and lacked inactivation. The distinct voltage and time dependencies of R-type and S-type anion channels suggest that they may play a role during depolarization-associated signal transduction in higher plant cells and that these anion channels may contribute to different processes in the regulation of stomatal movements. In particular, the slow and sustained nature of S-type anion channel activation revealed here leads us to hypothesize that S-type anion channels may provide a central molecular mechanism for control of stomatal closing, which is accompanied by long-term anion efflux and depolarization.Stomatal pores in the epidermis of leaves control diffusion of CO2 into leaves for carbon fixation and transpiration of H20 to the atmosphere. In darkness or in response to environmental stress factors such as drought, stomata close to minimize water loss of plants. Closing of stomata is induced by long-term anion and K+ efflux from guard cell pairs, which surround stomatal pores (1-3). Recent studies suggest that stomatal closing may be mediated by simultaneous opening of Ca2+-and nucleotide-regulated anion channels (4-6) and depolarization-activated K+ channels (7,8).Anion channels in guard cells may provide a central control mechanism for regulation of stomatal closing, as anion channel activation causes depolarization (4, 5), which in turn drives K+ efflux through K+ channels (7,8) in the plasma membrane of guard cells. Anion channels in guard cells are permeable to the major anionic nutrients nitrate and malate (5), which are transported across plant membranes.In addition to stomatal regulation, anion channels may play a central role in initiation of many signal transduction processes in higher plant cells. As an early event in signal transduction, many physiological stimuli including light signals, plant hormones, elicitors, and pathogens induce membrane depolarization (9-16) from the normal range of resting potentials found in higher plant cells (approximately -120 to -160 mV). These depolarizations occur transiently, lasting for durations of several tens of seconds, or are sustained and have been shown to be accompanied by anion efflu...

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“…The extrusion of H+ by the proton pump at the plasmalemma activated by the cytoplasmic acidification (1,7,18), the metabolic consumption of protons by the 'biochemical pH-stat' described by Davies (9) and a transfer of protons from the cytoplasm to the vacuole as suggested by the observed vacuolar acidification are possible candidates. The second paper of this series will be devoted to a study of the possible involvement of these mechanisms and their cooperative action in the resistance to acid-loads.…”

Section: Discussionmentioning

confidence: 97%

“…Acid-loading of plant cells now appears to be as a useful tool to stimulate the plasmalemma proton pump (1,7,18,28) and to study the relationship between pH, and growth (7).…”

Section: Abstracimentioning

confidence: 99%

Cytoplasmic pH Regulation in Acer pseudoplatanus Cells

Guern

Mathieu²,

Péan³

et al. 1986

Plant Physiol.

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ABSTRACIModifications of cytoplasmic pH in Acer pseudoplatanus L. cells cultivated in suspension have been induced by acid-loads and studied by using 31P nuclear magnetic resonance spectroscopy. The initial drop of cytoplasmic pH, observed in the first minutes of exposure to weak lipophilic acids, was followed by a slow recovery to reach a plateau phase with a pH value lower than the initial one. Conversely, removal of the acid led to a sharp increase of cytoplasmic pH with in most cases an overshoot toward more alkaline values than the initial one and a subsequent decrease to more acidic values. This shows that A. pseudoplatanus cells powerfully regulate their cytoplasmic pH both on the acid side of their normal pH, during the acid-load, and on the alkaline side, after removal of acid. Similar results were obtained with different types of acid-loads, i.e. treatments with propionic or benzoic acid or bubbling with C02-enriched air. This indicates that the occurrence of pH regulation does not depend upon the method used to acid-load the cells. The time courses of cytoplasmic pH observed for A. pseudoplatanus and also Catharanthus roseus cells are similar to those recorded for animal cells but different from those described for other plant materials for which no recovery phase was observed. This can be explained by different balances between the initial rate of proton influx brought in by the acids, and the capacity of proton consumption by the regulatory mechanisms. The existence of the recovery phase offers a unique possibility to study the regulation of the cytoplasmic pH of plant cells, as it has been done in animal systems.The study of transient changes in pHi2 has brought considerable progress in the understanding of pHi regulation in animal cells (27) (7), and root hair cells from Sinapis alba (2). During the last few years, the 3P NMR technique has been adapted to plant material, allowing simultaneous determinations of vacuolar and cytoplasmic pH values (24). The hypoxic acidification of the cytoplasm of maize root tips under hypoxia has been very elegantly studied by Roberts et al. (22,23). These authors used acetic acid (22) and CO2 (23) as acidifying agents and demonstrated large cytoplasmic acidifications.The effects of acid-loads have been also indirectly studied (i.e.without measuring the pH, by their effect on the electrogenic proton pump at the plasmalemma and the subsequent modifications of ionic exchanges. Weak acids like butyric acid induce a hyperpolarization associated with a K+ influx in maize roots (18). Butyric and benzoic acids hyperpolarize oat coleoptiles (1).These results are in good agreement with more recent ones associating pH and potential measurements with microelectrodes in maize (7) and S. alba roots (2) which demonstrate unambiguously that the hyperpolarization is a consequence of cytoplasmic acidification. Acid-loading of plant cells now appears to be as a useful tool to stimulate the plasmalemma proton pump (1,7,18,28) and to study the relationship between pH, and growth (7).W...

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Rapid response of the plasma-membrane potential in oat coleoptiles to auxin and other weak acids

Cited by 128 publications

References 33 publications

H⁺ Extrusion and Potassium Uptake Associated with Potential Hyperpolarization in Maize and Wheat Root Segments Treated with Permeant Weak Acids

H⁺ Extrusion and Potassium Uptake Associated with Potential Hyperpolarization in Maize and Wheat Root Segments Treated with Permeant Weak Acids

Two types of anion channel currents in guard cells with distinct voltage regulation.

Cytoplasmic pH Regulation in Acer pseudoplatanus Cells

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Rapid response of the plasma-membrane potential in oat coleoptiles to auxin and other weak acids

Cited by 128 publications

References 33 publications

H+ Extrusion and Potassium Uptake Associated with Potential Hyperpolarization in Maize and Wheat Root Segments Treated with Permeant Weak Acids

H+ Extrusion and Potassium Uptake Associated with Potential Hyperpolarization in Maize and Wheat Root Segments Treated with Permeant Weak Acids

Two types of anion channel currents in guard cells with distinct voltage regulation.

Cytoplasmic pH Regulation in Acer pseudoplatanus Cells

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Resources

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H⁺ Extrusion and Potassium Uptake Associated with Potential Hyperpolarization in Maize and Wheat Root Segments Treated with Permeant Weak Acids

H⁺ Extrusion and Potassium Uptake Associated with Potential Hyperpolarization in Maize and Wheat Root Segments Treated with Permeant Weak Acids