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. 1995 Jul;108(3):1059–1066. doi: 10.1104/pp.108.3.1059

Stimulation by Light of Rapid pH Regulation in the Chloroplast Stroma in Vivo as Indicated by CO2 Solubilization in Leaves.

M Hauser 1, H Eichelmann 1, V Oja 1, U Heber 1, A Laisk 1
PMCID: PMC157457  PMID: 12228527

Abstract

Leaves of Brassica oleracea, Helianthus annuus, and Nicotiana rustica were exposed for 20 s to high concentrations of CO2. CO2 uptake by the leaf, which was very fast, was measured as a transient increase in the concentration of oxygen. Rapid solubilization of CO2 in excess of that which is physically dissolved in aqueous phases is proposed to be caused by bicarbonate formation in the stroma of chloroplasts, which contain carbonic anhydrase. On this basis, pH values and bicarbonate accumulation in the chloroplast stroma were calculated. Buffer capacities were far higher than expected on the basis of known concentrations in the chloroplast stroma. Moreover, apparent buffer capacities increased with the time of exposure to high CO2, and they were higher when the measurements were performed in the light than in the dark. During prolonged exposure of leaves to 16% CO2, calculated bicarbonate concentrations in the chloroplast stroma exceeded 90 mM in the dark and 120 mM in the light. The observations are interpreted as indicating that under acid stress protons are rapidly exported from the chloroplasts in exchange for cations, which are imported. The data are discussed in terms of effective metabolic pH control by ion transport, first across the chloroplast envelope and, then, across the tonoplast of leaf mesophyll cells. The direct involvement of the vacuole in the regulation of the chloroplast pH in leaf cells is suggested.

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Selected References

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  1. Arnon D. I. COPPER ENZYMES IN ISOLATED CHLOROPLASTS. POLYPHENOLOXIDASE IN BETA VULGARIS. Plant Physiol. 1949 Jan;24(1):1–15. doi: 10.1104/pp.24.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Berkowitz G. A., Peters J. S. Chloroplast Inner-Envelope ATPase Acts as a Primary H+ Pump. Plant Physiol. 1993 May;102(1):261–267. doi: 10.1104/pp.102.1.261. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Burnell J. N., Gibbs M. J., Mason J. G. Spinach chloroplastic carbonic anhydrase: nucleotide sequence analysis of cDNA. Plant Physiol. 1990 Jan;92(1):37–40. doi: 10.1104/pp.92.1.37. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Demmig B., Gimmler H. Properties of the Isolated Intact Chloroplast at Cytoplasmic K Concentrations : I. Light-Induced Cation Uptake into Intact Chloroplasts is Driven by an Electrical Potential Difference. Plant Physiol. 1983 Sep;73(1):169–174. doi: 10.1104/pp.73.1.169. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Douce R., Holtz R. B., Benson A. A. Isolation and properties of the envelope of spinach chloroplasts. J Biol Chem. 1973 Oct 25;248(20):7215–7222. [PubMed] [Google Scholar]
  6. Douce R., Joyard J. Biochemistry and function of the plastid envelope. Annu Rev Cell Biol. 1990;6:173–216. doi: 10.1146/annurev.cb.06.110190.001133. [DOI] [PubMed] [Google Scholar]
  7. Enser U., Heber U. Metabolic regulation by pH gradients. Inhibition of photosynthesis by indirect proton transfer across the chloroplast envelope. Biochim Biophys Acta. 1980 Oct 3;592(3):577–591. doi: 10.1016/0005-2728(80)90102-4. [DOI] [PubMed] [Google Scholar]
  8. Gerhardt R., Stitt M., Heldt H. W. Subcellular Metabolite Levels in Spinach Leaves : Regulation of Sucrose Synthesis during Diurnal Alterations in Photosynthetic Partitioning. Plant Physiol. 1987 Feb;83(2):399–407. doi: 10.1104/pp.83.2.399. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gout E., Bligny R., Douce R. Regulation of intracellular pH values in higher plant cells. Carbon-13 and phosphorus-31 nuclear magnetic resonance studies. J Biol Chem. 1992 Jul 15;267(20):13903–13909. [PubMed] [Google Scholar]
  10. Graham D., Reed M. L., Patterson B. D., Hockley D. G., Dwyer M. R. Chemical properties, distribution, and physiology of plant and algal carbonic anhydrases. Ann N Y Acad Sci. 1984;429:222–237. doi: 10.1111/j.1749-6632.1984.tb12340.x. [DOI] [PubMed] [Google Scholar]
  11. Heldt H. W. Adenine nucleotide translocation in spinach chloroplasts. FEBS Lett. 1969 Sep;5(1):11–14. doi: 10.1016/0014-5793(69)80280-2. [DOI] [PubMed] [Google Scholar]
  12. Heldt W. H., Werdan K., Milovancev M., Geller G. Alkalization of the chloroplast stroma caused by light-dependent proton flux into the thylakoid space. Biochim Biophys Acta. 1973 Aug 31;314(2):224–241. doi: 10.1016/0005-2728(73)90137-0. [DOI] [PubMed] [Google Scholar]
  13. Maury W. J., Huber S. C., Moreland D. E. Effects of Magnesium on Intact Chloroplasts : II. CATION SPECIFICITY AND INVOLVEMENT OF THE ENVELOPE ATPase IN (SODIUM) POTASSIUM/PROTON EXCHANGE ACROSS THE ENVELOPE. Plant Physiol. 1981 Dec;68(6):1257–1263. doi: 10.1104/pp.68.6.1257. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Pfanz H., Heber U. Buffer capacities of leaves, leaf cells, and leaf cell organelles in relation to fluxes of potentially acidic gases. Plant Physiol. 1986 Jun;81(2):597–602. doi: 10.1104/pp.81.2.597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Spanswick R. M., Miller A. G. Measurement of the Cytoplasmic pH in Nitella translucens: Comparison of Values Obtained by Microelectrode and Weak Acid Methods. Plant Physiol. 1977 Apr;59(4):664–666. doi: 10.1104/pp.59.4.664. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Speer M., Kaiser W. M. Ion Relations of Symplastic and Apoplastic Space in Leaves from Spinacia oleracea L. and Pisum sativum L. under Salinity. Plant Physiol. 1991 Nov;97(3):990–997. doi: 10.1104/pp.97.3.990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Wu W., Berkowitz G. A. Lidocaine and ATPase inhibitor interaction with the chloroplast envelope. Plant Physiol. 1991 Dec;97(4):1551–1557. doi: 10.1104/pp.97.4.1551. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Yokota A., Kitaoka S. Correct pK values for dissociation constant of carbonic acid lower the reported Km values of ribulose bisphosphate carboxylase to half. Presentation of a nomograph and an equation for determining the pK values. Biochem Biophys Res Commun. 1985 Sep 30;131(3):1075–1079. doi: 10.1016/0006-291x(85)90200-1. [DOI] [PubMed] [Google Scholar]

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