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Light-dependent pH changes in leaves of C4 plants Comparison of the pH response to carbon dioxide and oxygen with that of C3 plants

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Abstract

Cytosolic and vacuolar pH changes caused by illumination or a changed composition of the gas phase were monitored in leaves of the NAD malic-enzyme-type C4 plant Amaranthus caudatus L. and the C3 plant Vicia faba L. by recording changes in the fluorescence of pH-indicating dyes which had been fed to the leaves. Light-dependent cytosolic alkalization and vacuolar acidification were maximal in the mesophyll cells under high-fluence-rate illumination and in the absence of CO2. Under the same conditions, measurements of light scattering and electrochromic absorption changes at 518 nm revealed maximum thylakoid energization. The results show an intimate relationship between the energization of the photosynthetic apparatus by light, an increase in cytosolic pH and a decrease in vacuolar pH. This was true for both the C4 and the C3 plant, although kinetics, extent and even direction of cytosolic pH changes differed considerably in these plants, reflecting the differences in photosynthetic carbon metabolism. Darkening produced rapid acidification in Vicia, but not in Amaranthus. Continued alkalization in Amaranthus is interpreted to be the result of the decarboxylation of a C4 intermediate and the release of liberated CO2. In the presence of CO2, energy consumption by carbon reduction decreased thylakoid energization, cytosolic alkalization and vacuolar acidification. Under low-fluence-rate illumination, thylakoid energization and light-dependent cytosolic and vacuolar pH changes were decreased in CO2-free air compared with thylakoid energization and pH changes in 1% oxygen/99% nitrogen not only in the C3 plant, but also in Amaranthus. Since oxygenation of ribulose bisphosphate initiates energy-consuming photorespiratory reactions in 21% oxygen, but not in 1% oxygen, this shows that photorespiratory reactions are active not only in the C3 but also in the C4 plant in the absence of external CO2. Photorespiratory conditions appeared to decrease energization not only in the chloroplasts, but also in the cytosol. This is indicated by decreased transfer of protons from the cytosol into the vacuole, a process which is energy-dependent.

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Abbreviations

CDCF:

5-(and 6-)carboxy-2′,7′-dichlorofluorescein

P700 :

electron-donor pigment in the reaction center of photosystem I

RuBP:

ribulose-1,5-bisphosphate

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Author notes

  1. A. S. Raghavendra

    Present address: School of Life Sciences, University of Hyderabad, 500134, Hyderabad, India

  2. Zu-Hua Yin

    Present address: Institut für Biochemische Pflanzenpathologie, GSF München, Ingolstädter Landstrasse 1, W-8042, Neuherberg, FRG

Authors and Affiliations

  1. Julius-von-Sachs-Institut für Biowissenschaften der Universität Würzburg, Mittlerer Dallenbergweg 64, W-8700, Würzburg, FRG

    A. S. Raghavendra, Zu-Hua Yin & Ulrich Heber

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  1. A. S. Raghavendra
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  2. Zu-Hua Yin
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  3. Ulrich Heber
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This work was supported, within the framework of the Sonderforschungsbereiche 176 and 251 of the University of Würzburg, by the Gottfried-Wilhelm-Leibniz Program of the Deutsche Forschungsgemeinschaft. A.S.R. was the recipient of a fellowship from the Alexander-von-Humboldt-Foundation. We are grateful to Mr. Carsten Werner and Mrs. Spidola Neimanis for cooperation.

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Raghavendra, A.S., Yin, ZH. & Heber, U. Light-dependent pH changes in leaves of C4 plants Comparison of the pH response to carbon dioxide and oxygen with that of C3 plants. Planta 189, 278–287 (1993). https://doi.org/10.1007/BF00195087

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  • DOI: https://doi.org/10.1007/BF00195087

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