The role of cations in the organization of chloroplast membranes

doi:10.1016/S0003-9861(71)80072-3

Archives of Biochemistry and Biophysics

Volume 146, Issue 1, September 1971, Pages 337-347

https://doi.org/10.1016/S0003-9861(71)80072-3 Get rights and content

The influence of monovalent and divalent cations on the structure of chloroplasts has been investigated. Parameters of structure such as transmission, light scattering, scattering, fluorescence of chlorophyll and 8-anilinonaphthalene-1-sulfonic acid (ANS), were compared with electron microscopy under conditions of varying salt concentration.

Cations are required to stabilize the association of membranes in the grana. A striking correlation exists between the separation of chloroplast grana membranes into individual thylakoids and a marked increase in chlorophyll fluorescence at long wavelength (734 nm) and other parameters of chloroplast membrane structure. The influence of cations on causing a reversible cementing of individual thylakoid membranes together into grana was relatively nonspecific but divalent cations were much more effective than monovalent ions on a concentration basis.

It is concluded that hydrophobic rather than electrostatic interactions predominate in determination of the grana structure. The results are relevant to functional studies of the coupling of electron flow between the two photosystems and of energy conservation in the form of ion gradients and ATP.

References (23)

ShavitN. et al.
Biochim. Biophys. Acta
(1967)
DilleyR.A. et al.
Biochim. Biophys. Acta
(1968)
GrossE. et al.
Arch. Biochem. Biophys.
(1967)
GrossE. et al.
Arch. Biochem. Biophys.
(1969)
AndersonJ.M. et al.
Biochim. Biophys. Acta
(1967)
StryerL.
J. Mol. Biol.
(1965)
CederstrandC.N. et al.
Biochim. Biophys. Acta
(1966)
KokB. et al.
Biochim. biophys. Acta
(1966)
AndersonJ.M. et al.
Biochim. Biophys. Acta
(1968)
MurataN.
Biochim. Biophys. Acta
(1969)

MurataN. et al.

Biochim. Biophys. Acta

(1970)

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This result differs from digitonin solubilisation of whole thylakoids, where maximally approximately half of the PSI complexes had an LHCII antenna attached [15,18,19,47,48], suggesting that with the SMA protocol a specific region of the thylakoid membrane is isolated. Another effect, which should be considered, is the possibility that the negative charge of the SMA drives the association of LHCII with PSI in a manner similar to that observed in the case of cation depletion [49]. To gain insight in the excitation energy transfer and trapping efficiency of the detergent purified PSI and PSI-LHCII complexes and the PSI-LHCII membranes streak camera measurements were performed.
Photosystems I and II (PSI and PSII) work in series to drive oxygenic photosynthesis. The two photosystems have different absorption spectra, therefore changes in light quality can lead to imbalanced excitation of the photosystems and a loss in photosynthetic efficiency. In a short-term adaptation response termed state transitions, excitation energy is directed to the light-limited photosystem. In higher plants a special pool of LHCII antennae, which can be associated with either PSI or PSII, participates in these state transitions. It is known that one LHCII antenna can associate with the PsaH site of PSI. However, membrane fractions were recently isolated in which multiple LHCII antennae appear to transfer energy to PSI. We have used time-resolved fluorescence-streak camera measurements to investigate the energy transfer rates and efficiency in these membrane fractions. Our data show that energy transfer from LHCII to PSI is relatively slow. Nevertheless, the trapping efficiency in supercomplexes of PSI with ~ 2.4 LHCIIs attached is 94%. The absorption cross section of PSI can thus be increased with ~ 65% without having significant loss in quantum efficiency. Comparison of the fluorescence dynamics of PSI-LHCII complexes, isolated in a detergent or located in their native membrane environment, indicates that the environment influences the excitation energy transfer rates in these complexes. This demonstrates the importance of studying membrane protein complexes in their natural environment.
Cationic screening of charged surface groups (carboxylates) affects electron transfer steps in photosystem-II water oxidation and quinone reduction
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Seminal studies pursued in the seventies have resulted in the following picture. Screening of negative surface charges of photosynthetic membrane proteins, in particular located at PSII and associated light-harvesting complexes (LHCs), is a major determinant of the morphology of the thylakoid membrane system, specifically regarding the formation of membrane stacks (thylakoid stacking, e.g., [27,28]; for review, see [29,30]). In 1980, J. Barber summarized these findings and discussed the cationic screening comprehensively on grounds of the Gouy–Chapman theory of electric double-layer formation at charged surfaces [29].
The functional or regulatory role of long-distance interactions between protein surface and interior represents an insufficiently understood aspect of protein function. Cationic screening of surface charges determines the morphology of thylakoid membrane stacks. We show that it also influences directly the light-driven reactions in the interior of photosystem II (PSII). After laser-flash excitation of PSII membrane particles from spinach, time courses of the delayed recombination fluorescence (10 μs–10 ms) and the variable chlorophyll-fluorescence yield (100 μs–1 s) were recorded in the presence of chloride salts. At low salt-concentrations, a stimulating effect was observed for the S-state transition efficiency, the time constant of O₂-formation at the Mn₄Ca-complex of PSII, and the halftime of re-oxidation of the primary quinone acceptor (Q_a) by the secondary quinone acceptor (Q_b). The cation valence determined the half-effect concentrations of the stimulating salt effect, which were around 6 μM, 200 μM and 10 mM for trivalent (LaCl₃), bivalent (MgCl₂, CaCl₂), and monovalent cations (NaCl, KCl), respectively. A depressing high-salt effect also depended strongly on the cation valence (onset concentrations around 2 mM, 50 mM, and 500 mM). These salt effects are proposed to originate from electrostatic screening of negatively charged carboxylate sidechains, which are found in the form of carboxylate clusters at the solvent-exposed protein surface. We conclude that the influence of electrostatic screening by solvent cations manifests a functionally relevant long-distance interaction between protein surface and electron-transfer reactions in the protein interior. A relation to regulation and adaptation in response to environmental changes is conceivable.
The thylakoid membrane in a wide pH range
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The structural organisation of thylakoid systems of pea chloroplasts subjected to osmotic shock after incubation in a wide range of pH values (from 1.0 to 12.0) was studied. It was found that the percentage of thylakoid profiles stacked into granas is 86 % at pH 4.0, 72 % at pH 7.4 and 25 % at pH 10.0. In the pH range from 6.0 to 10.0 under the conditions of osmotic shock, a complete disordering of thylakoid systems, unstacking, and fragmentation of thylakoids are observed. Decreasing medium pH to 5.5-3.5 leads to a shortening of agranal thylakoids, the appearance of numerous lipid drops, and a shrinkage of thylakoid systems, which cease to respond to osmotic shock. Thylakoid systems remain structured, and the stacking in granas is retained. At pH levels from 3.0 to 1.0, thylakoid systems appear as spherical clusters of tightly stacked vesicles, whose structural organisation also does not change under osmotic shock. Increasing the pH of the medium to 11-12 leads to a complete unstacking of thylakoids and a swelling of single thylakoid sheets, which also do not respond to osmotic shock. A correlation between the release of acyl lipids from the thylakoid membrane and the loss of the native response of the membrane to osmotic shock is discussed.
Effect of urea and distilled water on the structure of the thylakoid system
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On the basis of structural data, an attempt is made to substantiate the hypothesis that in a thylakoid membrane, there exists an integral continuous network of intramembrane, lateral protein-protein interactions. It is shown that the forces determining the extent of flattening of the thylakoid system and the forces responsible for the packing of thylakoids in granas act independently. These two discrete groups of bonds, lateral bonds of the external leaflet of the membrane and the bonds of intermembrane stacking, provide a peculiar configuration of the system of internal chloroplast membranes, namely, the granal packing and the extent of flattening of the thylakoid system.
Control of the photosynthetic electron transport by PQ diffusion microdomains in thylakoids of higher plants
2000, Biochimica et Biophysica Acta - Bioenergetics
Citation Excerpt :
The destacking treatment in this study caused only a moderate decrease in Fv (about 60%; Table 2) while F0 remained almost unaffected (not shown). Destacking is further reflected by an increase in transmittance, which is thought to reflect thylakoid swelling [39]. The low Mg2+-treatment caused a light transmittance increase by about 30% (Table 2).
We investigate the role of plastoquinone (PQ) diffusion in the control of the photosynthetic electron transport. A control analysis reveals an unexpected flux control of the whole chain electron transport by photosystem (PS) II. The contribution of PSII to the flux control of whole chain electron transport was high in stacked thylakoids (control coefficient, CJ(PSII)=0.85), but decreased after destacking (CJ(PSII)=0.25). From an ‘electron storage’ experiment, we conclude that in stacked thylakoids only about 50 to 60% of photoreducable PQ is involved in the light-saturated linear electron transport. No redox equilibration throughout the membrane between fixed redox groups at PSII and cytochrome (cyt) bf complexes, and the diffusable carrier PQ is achieved. The data support the PQ diffusion microdomain concept by Lavergne et al. [J. Lavergne, J.-P. Bouchaud, P. Joliot, Biochim. Biophys. Acta 1101 (1992) 13–22], but we come to different conclusions about size, structure and size distribution of domains. From an analysis of cyt b₆ reduction, as a function of PSII inhibition, we conclude that in stacked thylakoids about 70% of PSII is located in small domains, where only 1 to 2 PSII share a local pool of a few PQ molecules. Thirty percent of PSII is located in larger domains. No small domains were found in destacked thylakoids. We present a structural model assuming a hierarchy of specific, strong and weak interactions between PSII core, light harvesting complexes (LHC) II and cyt bf. Peripheral LHCII’s may serve to connect PSII–LHCII supercomplexes to a flexible protein network, by which small closed lipid diffusion compartments are formed. Within each domain, PQ moves rapidly and shuttles electrons between PSII and cyt bf complexes in the close vicinity. At the same time, long range diffusion is slow. We conclude, that in high light, cyt bf complexes located in distant stromal lamellae (20 to 30%) are not involved in the linear electron transport.
Mg<sup>2+</sup>-induced lipid phase transition in thylakoid membranes is reversed by anions
1994, Biochemical and Biophysical Research Communications
Effect of anions on thylakoid membrane fluidity as measured by rotational correlation time, order parameter (by ESR spectroscopy) and fluorescence polarization was studied. The data in the present study offer proof that Mg²⁺-induced rigidity of thylakoid membranes could be reversed by anions like bicarbonate and chloride. Anions were found to play a role in structural reorganization of thylakoid membranes.

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¹: Present address: Department of Biology, College of General Education, University of Tokyo, Tokyo, Japan.

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The role of cations in the organization of chloroplast membranes

Biochim. Biophys. Acta

Biochim. Biophys. Acta

Arch. Biochem. Biophys.

Arch. Biochem. Biophys.

Biochim. Biophys. Acta

J. Mol. Biol.

Biochim. Biophys. Acta

Biochim. biophys. Acta

Biochim. Biophys. Acta

Biochim. Biophys. Acta

Biochim. Biophys. Acta