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Acetic acid esters and permeable weak acids induce active proton extrusion and extension growth of coleoptile segments by lowering the cytoplasmic pH

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Abstract

In Avena coleoptile segments a decrease of cytoplasmic pH activates energy-dependent H+ extrusion into the apoplast, thereby triggering extension growth. This sequence of events cannot be inhibited by cycloheximide and is induced by the following conditions and compounds. (i) A short anaerobic treatment of coleoptile segments results in the formation of lactic acid and an intracellular decrease of pH. For a period of 20 min after transfer to normal air, the growth rate is up to six times higher than the rate before anaerobiosis. (ii) Similarly, incubation of segments with CN− (0.1 mM) in the presence of oxygen causes and accumulation of lactic acid and a fall in cell-sap pH. After removing CN− a growth burst occurs. (iii) Higher concentrations of permeable acids (≧10 mM in buffer pH 5.8) induce extension growth. This growth is O2-dependent and therefore differs from the acid growth, which can be triggered under anaerobic conditions by acid buffers of pH≦5 via the direct increase of cell-wall plasticity. (iv) A short application of CO2-saturated buffer (pH 5.8) causes CO2-induced elongation growth; after a 3-min pulse the growth rate is enhanced for about 15 min. (v) Lipophilic esters of acetic acid or propionic acid, such as naphthylacetate, naphthylpropionate, phenylacetate, benzylacetate induce elongation growth. These compounds, when taken up into the cell, are hydrolized by esterases; the acids released lower the cytoplasmic pH (shown by the pH indicator, fluorescein). The highest esterase activity was found in a microsomal membrane fraction of coleoptiles. While the carboxyester-induced extension growth is completely inhibited under anoxia, the initial acidification of the bathing solution can still be observed. This decrease in external pH is obviously the result of ester hydrolysis, caused by damaged cells, and is not the result of pH changes within the cell-wall compartment. It is suggested that a fast uptake of carboxyesters and the shift in equilibrium caused by their internal hydrolysis leads to a continuous formation of acids which lowers the cytoplasmic pH and activates the ATP-dependent H+ extrusion. In most experiments fusicoccin (a diacetic acid ester) acts similarly to naphthylacetate and the other carboxyesters, although quantitative differences exist. Therefore, it is possible that fusicoccin is effective partly on the basis of its ester characteristic. The effects observed are discussed with regard to the very narrow pH optimum of plasma-membrane H+-ATPases exhibiting their highest levels of activity at pH 6.5 (Hager and Biber 1984, Z. Naturforsch. C 39, 927–937).

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Abbreviations

CHM:

cycloheximide

DMO:

dimethadione (5.5-dimethyl-2,4-oxazolidinedione)

FC:

fusicoccin

IAA:

indole-3-acetic acid

Mes:

2-(N-morpholino)ethanesulfonic acid

NA:

α(or β)-naphthylacetate (acetic acid-1(or-2-)naphthylester)

NAA:

α(or β)-naphthaleneacetic acid

PA:

phenylacetate (acetic acid phenylester)

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  1. Institut für Biologie I der Universität, Auf der Morgenstelle 1, D-7400, Tübingen 1, Federal Republic of Germany

    Achim Hager & Ilse Moser

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  1. Achim Hager
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Hager, A., Moser, I. Acetic acid esters and permeable weak acids induce active proton extrusion and extension growth of coleoptile segments by lowering the cytoplasmic pH. Planta 163, 391–400 (1985). https://doi.org/10.1007/BF00395148

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