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. 1991 Oct;97(2):580–587. doi: 10.1104/pp.97.2.580

Surface Charge-Mediated Effects of Mg2+ on K+ Flux across the Chloroplast Envelope Are Associated with Regulation of Stromal pH and Photosynthesis 1

Weihua Wu 1, Jeanne Peters 1, Gerald A Berkowitz 1
PMCID: PMC1081046  PMID: 16668438

Abstract

Studies of Spinacia oleracea L. were undertaken to characterize further how Mg2+ external to the isolated intact chloroplast interacts with stromal K+, pH, and photosynthetic capacity. Data presented in this report were consistent with the previously developed hypothesis that millimolar levels of external, unchelated Mg2+ result in lower stromal K+, which somehow is linked to stromal acidification. Stromal acidification directly results in photosynthetic inhibition. These effects were attributed to Mg2+ interaction (binding) to negative surface charges on the chloroplast envelope. Chloroplast envelope-bound Mg2+ was found to decrease the envelope membrane potential (inside negative) of the illuminated chloroplast by 10 millivolts. It was concluded that Mg2+ effects on photosynthesis were likely not mediated by this effect on membrane potential. Further experiments indicated that envelope-bound Mg2+ caused lower stromal K+ by restricting the rate of K+ influx; Mg2+ did not affect K+ efflux from the stroma. Mg2+ restriction of K+ influx appeared consistent with the typical effects imposed on monovalent cation channels by polyvalent cations that bind to negatively charged sites on a membrane surface near the outer pore of the channel. It was hypothesized that this interaction of Mg2+ with the chloroplast envelope likely mediated external Mg2+ effects on chloroplast metabolism.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. 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]
  2. Douce R., Block M. A., Dorne A. J., Joyard J. The plastid envelope membranes: their structure, composition, and role in chloroplast biogenesis. Subcell Biochem. 1984;10:1–84. doi: 10.1007/978-1-4613-2709-7_1. [DOI] [PubMed] [Google Scholar]
  3. Fermini B., Nathan R. D. Sialic acid and the surface charge associated with hyperpolarization-activated, inward rectifying channels. J Membr Biol. 1990 Mar;114(1):61–69. doi: 10.1007/BF01869385. [DOI] [PubMed] [Google Scholar]
  4. Gilbert D. L., Ehrenstein G. Effect of divalent cations on potassium conductance of squid axons: determination of surface charge. Biophys J. 1969 Mar;9(3):447–463. doi: 10.1016/S0006-3495(69)86396-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Gupta A. S., Berkowitz G. A. Development and use of chlorotetracycline fluorescence as a measurement assay of chloroplast envelope-bound mg. Plant Physiol. 1989 Mar;89(3):753–761. doi: 10.1104/pp.89.3.753. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Heath R. L., Leech R. M. The stimulation of CO2-supported O2 evolution in intact spinach chloroplasts by ammonium ion. Arch Biochem Biophys. 1978 Sep;190(1):221–226. doi: 10.1016/0003-9861(78)90271-0. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. Hille B., Woodhull A. M., Shapiro B. I. Negative surface charge near sodium channels of nerve: divalent ions, monovalent ions, and pH. Philos Trans R Soc Lond B Biol Sci. 1975 Jun 10;270(908):301–318. doi: 10.1098/rstb.1975.0011. [DOI] [PubMed] [Google Scholar]
  9. Huber S. C., Maury W. Effects of Magnesium on Intact Chloroplasts: I. EVIDENCE FOR ACTIVATION OF (SODIUM) POTASSIUM/PROTON EXCHANGE ACROSS THE CHLOROPLAST ENVELOPE. Plant Physiol. 1980 Feb;65(2):350–354. doi: 10.1104/pp.65.2.350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. McLaughlin A., Eng W. K., Vaio G., Wilson T., McLaughlin S. Dimethonium, a divalent cation that exerts only a screening effect on the electrostatic potential adjacent to negatively charged phospholipid bilayer membranes. J Membr Biol. 1983;76(2):183–193. doi: 10.1007/BF02000618. [DOI] [PubMed] [Google Scholar]
  12. Mozhayeva G. N., Naumov A. P. Effect of surface charge on the steady-state potassium conductance of nodal membrane. Nature. 1970 Oct 10;228(5267):164–165. doi: 10.1038/228164a0. [DOI] [PubMed] [Google Scholar]
  13. Peters J. S., Berkowitz G. A. Studies on the System Regulating Proton Movement across the Chloroplast Envelope : Effects of ATPase Inhibitors, Mg, and an Amine Anesthetic on Stromal pH and Photosynthesis. Plant Physiol. 1991 Apr;95(4):1229–1236. doi: 10.1104/pp.95.4.1229. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Portis A. R., Jr, Heldt H. W. Light-dependent changes of the Mg2+ concentration in the stroma in relation to the Mg2+ dependency of CO2 fixation in intact chloroplasts. Biochim Biophys Acta. 1976 Dec 6;449(3):434–436. doi: 10.1016/0005-2728(76)90154-7. [DOI] [PubMed] [Google Scholar]
  15. Prasad R., Höfer M. Tetraphenylphosphonium is an indicator of negative membrane potential in Candida albicans. Biochim Biophys Acta. 1986 Oct 9;861(2):377–380. doi: 10.1016/0005-2736(86)90442-6. [DOI] [PubMed] [Google Scholar]
  16. Stanfield P. R. Intracellular Mg2+ may act as a co-factor in ion channel function. Trends Neurosci. 1988 Nov;11(11):475–477. doi: 10.1016/0166-2236(88)90003-3. [DOI] [PubMed] [Google Scholar]

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