Evidence that acid solutions induce plant cell elongation by acidifying the cytosol and stimulating the proton pump

Brummer, Benno; Felle, Hubert; Parish, Roger W.

doi:10.1016/0014-5793(84)81162-x

Cited by 67 publications

(27 citation statements)

References 31 publications

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“…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).…”

supporting

confidence: 92%

“…Thus, the mechanisms responsible for the overall 'consumption' of protons in the cytoplasm exceed the entry of protons brought by propionic acid uptake during the period of recovery. However, Table I shows that suspension cultured cells apparently behave peculiarly compared to the other plant materials already described for which the time courses of pHc changes during an acid-load gave no evidence for a pH recovery (2,7,22,29).…”

Section: Pi -G6pmentioning

confidence: 83%

“…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: 98%

“…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%

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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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supporting

confidence: 92%

Section: Pi -G6pmentioning

confidence: 83%

Section: Discussionmentioning

confidence: 98%

“…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%

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Cytoplasmic pH Regulation in Acer pseudoplatanus Cells

Guern

Mathieu²,

Péan³

et al. 1986

Plant Physiol.

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“…Since it has been shown that electrogenic H+ extrusion in vivo (6,15,28) well as the plasma membrane H+-ATPase in vitro (10,14,20,29) are strongly stimulated by small decreases in pH in the range of cytoplasmic pH values, these data have been interpreted as indicating that FC-induced stimulation ofelectrogenic H' extrusion is a consequence of the acidification of the cytoplasm (5,7,15).…”

mentioning

confidence: 99%

H⁺-Pumping Driven by the Plasma Membrane ATPase in Membrane Vesicles from Radish: Stimulation by Fusicoccin

Rasi‐Caldogno¹,

Michelis²,

Pugliarello³

et al. 1986

Plant Physiol.

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ABSTRAC1The effect of fusicoccin on Mg:ATP-dependent H -pumping in microsomal vesicles from 24-hour-old radish (Raphanus sativus L.) seedlings was investigated by measuring the initial rate of decrease in the absorbance of the ApH probe acridine orange. Fusicoccin stimulated Mg:ATPdependent Hf-pumping when the pH of the assay medium was in the range 7.0 to 7.6 while no effect of fusicoccin was detected between pH 6.6 and pH 6.0. Both basal and fusicoccin-stimulated Hf-pumping were completely inhibited by vanadate and almost unaffected by nitrate. Fusicoccin did not change membrane permeability to protons and fusicoccininduced stimulation of Mg:ATP-dependent H -pumping was not affected by changes in the buffer capacity of the incubation medium. Deacetylfusicoccin stimulated Hf-pumping as much as fusicoccin, while the physiologically inactive derivative 8-oxo-9-epideacetylfusicoccin did not. Stimulation of Hf-pumping was saturated by 100 nanomolar fusicoccin. These data indicate that fusicoccin activates the plasma membrane H -ATPase by acting at the membrane level independently of the involvement of other cell components. The percent stimulation by fusicoccin was the same at all ATP concentrations tested (0.5-5.0 millimolar), thus suggesting that with fusicoccin there is an increase in V.. of the plasma membrane H'-ATPase rather than a decrease in its apparent K. for Mg:ATP.All of the physiological responses to FC2 appear to be related to a stimulation of electrogenic H+ extrusion mediated by the plasma membrane H+-ATPase. Stimulation ofthe plasma membrane H+-ATPase has been proposed as a primary step in the action of the toxin on the basis of evidence such as lack of a lag in the stimulating effect of FC on H+ extrusion and on hyperpolarization of AI, insensitivity of FC effects to inhibitors of RNA and protein synthesis, identification of specific FC-binding proteins at the plasma membrane and some stimulation by FC of the ATPase activity measured in microsomal fractions (for a review, see Refs. 17 and 18).In contrast to this view, it has been recently reported that FC induces in root hairs and in coleoptiles an early acidification of the cytoplasm, evident before any hyperpolarization of AI or stimulation of H+ extrusion is detectable (5, 7, 15). Since it has been shown that electrogenic H+ extrusion in vivo (6, 15, 28) well as the plasma membrane H+-ATPase in vitro (10,14,20,29) A more direct insight into the mechanism of action of FC can be provided by the study of its effects in vitro. This approach allows FC effects on membrane bound activities to be studied in the absence of other cell components. Recently, Rasi-Caldogno and Pugliarello (25), showed that FC strongly and reproducibly stimulated the H+-pumping and, to a lesser extent, the hydrolytic activity of the plasma membrane H+-ATPase in membrane vesicles isolated from radish seedlings. In this paper, we present a more detailed characterization of the stimulating effect of FC on the H+-pumping activity ofthe plasma membrane H+-ATPase ofradish. The ...

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Effects of cultivar and culture conditions on γ-aminobutyric acid accumulation in germinated fava beans (Vicia faba L.)

Bai

Jin

et al. 2009

J. Sci. Food Agric.

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Evidence that acid solutions induce plant cell elongation by acidifying the cytosol and stimulating the proton pump

Cited by 67 publications

References 31 publications

Cytoplasmic pH Regulation in Acer pseudoplatanus Cells

Cytoplasmic pH Regulation in Acer pseudoplatanus Cells

H⁺-Pumping Driven by the Plasma Membrane ATPase in Membrane Vesicles from Radish: Stimulation by Fusicoccin

Effects of cultivar and culture conditions on γ-aminobutyric acid accumulation in germinated fava beans (Vicia faba L.)

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Evidence that acid solutions induce plant cell elongation by acidifying the cytosol and stimulating the proton pump

Cited by 67 publications

References 31 publications

Cytoplasmic pH Regulation in Acer pseudoplatanus Cells

Cytoplasmic pH Regulation in Acer pseudoplatanus Cells

H+-Pumping Driven by the Plasma Membrane ATPase in Membrane Vesicles from Radish: Stimulation by Fusicoccin

Effects of cultivar and culture conditions on γ-aminobutyric acid accumulation in germinated fava beans (Vicia faba L.)

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H⁺-Pumping Driven by the Plasma Membrane ATPase in Membrane Vesicles from Radish: Stimulation by Fusicoccin