The transthylakoid membrane potential (ΔΨm) is essential because it can drive the ATP synthesis through the CF0-CF1 type of ATP-synthase in chloroplasts as an energetic equivalent similar to ΔpH. In addition, a high fraction of proton motive force (PMF) stored as the ΔΨm component is physiologically important in the acclimation of photosynthesis to environmental stresses. It has been shown that ΔΨm is the sum of the Donnan potential difference (ΔΨdn) and the diffusion potential difference (ΔΨd). Specifically, ΔΨdn, ΔΨd, and ΔΨm are strongly associated with the ionic activities near the membrane surface, particularly, the extent of ion binding to the charged/neutral sites adjacent to the membrane surface. However, an in-depth analysis of the effect of altered cationic binding to the membrane surface on adjusting the transthylakoid electric potentials (ΔΨdn, ΔΨd, and ΔΨm) is still missing. This lack of a mechanistic understanding is due to the experimental difficulty of closely observing cations binding to the membrane surface in vivo. In this work, a computer model was proposed to investigate the transthylakoid electric phenomena in the chloroplast focusing on the interaction between cations and the negative charges close to the membrane surface. By employing the model, we simulated the membrane potential and consequently, the measured ECS traces, proxing the ΔΨm, were well described by the computing results on continuous illumination followed by a dark-adapted period. Moreover, the computing data clarified the components of transthylakoid membrane potential, unraveled the functional consequences of altered cationic attachment to the membrane surface on adjusting the transthylakoid electric potential, and further revealed the key role played by Donnan potential in regulating the energization of the thylakoid membrane. The current model for calculating electric potentials can function as a preliminary network for the further development into a more detailed theoretical model by which multiple important variables involved in photosynthesis can be explored.

Department of Biophysics Faculty of Science Palacký University Olomouc Czechia

School of Biological Science and Agriculture Qiannan Normal University for Nationalities Duyun China

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Armbruster U., Leonelli L., Correa Galvis V., Strand D., Quinn E. H., Jonikas M. C., et al. (2016). Regulation and Levels of the Thylakoid K+/H+ Antiporter KEA3 Shape the dynamic response of photosynthesis in fluctuating light. PubMed DOI PMC

Barber J. (1980b). Membrane surface charges and potentials in relation to photosynthesis. PubMed

Barber J. (1980a). An explanation for the relationship between salt-induced thylakoid stacking and the chlorophyll fluorescence changes associated with changes in spillover of energy from photosystem II to photosystem I.

Barber J. (1982). Influence of surface charges on thylakoid structure and function.

Barber J., Mills J., Love A. (1977). Electrical diffuse layers and their influence on photosynthetic processes. PubMed

Basso L., Yamori W., Szabo I., Shikanai T. (2020). Collaboration between NDH and KEA3 allows maximally efficient photosynthesis after a long dark adaptation. PubMed DOI PMC

Bulychev A. A. (1984). Different kinetics of membrane potential formation in dark-adapted and preilluminated chloroplasts. PubMed DOI

Bulychev A. A., Vredenberg W. J. (1999). Light-triggered electrical events in the thylakoid membrane of plant chloroplasts.

Correa Galvis V., Strand D. D., Messer M., Thiele W., Bethmann S., Hubner D., et al. (2020). H(+) Transport by K(+) EXCHANGE ANTIPORTER3 Promotes Photosynthesis and Growth in Chloroplast ATP Synthase Mutants. PubMed DOI PMC

Cruz J. A., Kanazawa A., Treff N., Kramer D. M. (2005). Storage of light-driven transthylakoid proton motive force as an electric field (Deltapsi) under steady-state conditions in intact cells of PubMed DOI

Cruz J. A., Sacksteder C. A., Kanazawa A., Kramer D. M. (2001). Contribution of electric field (Delta psi) to steady-state transthylakoid proton motive force (pmf) PubMed DOI

Davis G. A., Kanazawa A., Schottler M. A., Kohzuma K., Froehlich J. E., Rutherford A. W., et al. (2016). Limitations to photosynthesis by proton motive force-induced photosystem II photodamage. PubMed DOI PMC

Davis G. A., Rutherford A. W., Kramer D. M. (2017). Hacking the thylakoid proton motive force for improved photosynthesis: modulating ion flux rates that control proton motive force partitioning into Deltapsi and DeltapH. PubMed DOI PMC

Enz C., Steinkamp T., Wagner R. (1993). Ion channels in the thylakoid membrane (A patch-clamp study). DOI

Gillespie D., Eisenberg R. S. (2001). Modified Donnan potentials for ion transport through biological ion channels. PubMed

Herdean A., Teardo E., Nilsson A. K., Pfeil B. E., Johansson O. N., Unnep R., et al. (2016b). A voltage-dependent chloride channel fine-tunes photosynthesis in plants. PubMed DOI PMC

Herdean A., Nziengui H., Zsiros O., Solymosi K., Garab G., Lundin B., et al. (2016a). The Arabidopsis Thylakoid Chloride Channel AtCLCe functions in chloride homeostasis and regulation of photosynthetic electron transport. PubMed DOI PMC

Johnson M. P., Ruban A. V. (2014). Rethinking the existence of a steady-state Deltapsi component of the proton motive force across plant thylakoid membranes. PubMed DOI

Joliot P., Joliot A. (1989). Characterization of linear and quadratic electrochromic probes in

Kaña R. Govindjee. (2016). Role of ions in the regulation of light-harvesting. PubMed DOI PMC

Kanazawa A., Ostendorf E., Kohzuma K., Hoh D., Strand D. D., Sato-Cruz M., et al. (2017). Chloroplast ATP synthase modulation of the thylakoid proton motive force: implications for Photosystem I and Photosystem II Photoprotection. PubMed DOI PMC

Kinraide T. B., Yermiyahu U., Rytwo G. (1998). Computation of surface electrical potentials of plant cell membranes. Correspondence To published zeta potentials from diverse plant sources. PubMed DOI PMC

Klughammer C., Siebke K., Schreiber U. (2013). Continuous ECS-indicated recording of the proton-motive charge flux in leaves. PubMed DOI PMC

Kramer D. M., Sacksteder C. A. (1998). A diffused-optics flash kinetic spectrophotometer (DOFS) for measurements of absorbance changes in intact plants in the steady-state. PubMed

Kramer D. M., Sacksteder C. A., Cruz J. A. (1999). How acidic is the lumen?

Krause G.H. (1977). Light-induced movement of magnesium ions in intact chloroplasts. Spectroscopic determination with Eriochrome Blue SE. PubMed

Kunz H. H., Gierth M., Herdean A., Satoh-Cruz M., Kramer D. M., Spetea C., et al. (2014). Plastidial transporters KEA1, -2, and -3 are essential for chloroplast osmoregulation, integrity, and pH regulation in Arabidopsis. PubMed DOI PMC

Levine S., Levine M., Sharp K. A., Brooks D. E. (1983). Theory of the electrokinetic behavior of human erythrocytes. PubMed DOI PMC

Li M., Svoboda V., Davis G., Kramer D., Kunz H. H., Kirchhoff H. (2021). Impact of ion fluxes across thylakoid membranes on photosynthetic electron transport and photoprotection. PubMed DOI

Li Z., Wakao S., Fischer B. B., Niyogi K. K. (2009). Sensing and responding to excess light. PubMed

Lyu H., Lazar D. (2017a). Modeling the light-induced electric potential difference (DeltaPsi), the pH difference (DeltapH) and the proton motive force across the thylakoid membrane in C3 leaves. PubMed DOI

Lyu H., Lazar D. (2017b). Modeling the light-induced electric potential difference DeltaPsi across the thylakoid membrane based on the transition state rate theory. PubMed DOI

Mitchell P. (1961). Chemiosmotic coupling in oxidative and photosynthetic phosphorylation. PubMed

Mitchell P. (1966). Chemiosmotic coupling in oxidative and photosynthetic phosphorylation. PubMed

Mitchell P. (2011). Chemiosmotic coupling in oxidative and photosynthetic phosphorylation. 1966. PubMed

Nakatani H. Y., Barber J., Forrester J. A. (1978). Surface charges on chloroplast membranes as studied by particle electrophoresis. PubMed DOI

Ohshima H., Kondo T. (1987). Electrostatic repulsion of ion penetrable charged membranes: role of Donnan potential. PubMed DOI

Ohshima H., Kondo T. (1988b). Membrane potential and Donnan potential. PubMed

Ohshima H., Kondo T. (1988a). Double-layer interaction regulated by the donnan potential. PubMed DOI

Ohshima H., Kondo T. (1990). Relationship among the surface potential, Donnan potential and charge density of ion-penetrable membranes. PubMed DOI

Ohshima H., Ohki S. (1985). Donnan potential and surface potential of a charged membrane. PubMed PMC

Pinnola A., Bassi R. (2018). Molecular mechanisms involved in plant photoprotection. PubMed

Portis A. R. (1981). Evidence of a low stromal Mg2+ concentration in intact chloroplasts in the dark: I. STUDIES WITH THE IONOPHORE A23187. PubMed PMC

Pottosin I., Schönknecht G. (1996). Ion channel permeable for divalent and monovalent cations in native spinach thylakoid membranes. PubMed DOI

Qasem N. A. A., Qureshi B. A., Zubair S. M. (2018). Improvement in design of electrodialysis desalination plants by considering the Donnan potential.

Schönknecht G., Hedrich R., Junge W., Raschke K. (1988). A voltage-dependent chloride channel in the photosynthetic membrane of a higher plant.

Siggel U. (1981a). 414 — Surface and/or Donnan potentials at the thylakoid membrane?

Siggel U. (1981b). 415 - Surface and/or Donnan potentials at the thylakoid membrane?

Siggel U. (1981c). 416 - Surface and/or Donnan potentials at the thylakoid membrane?

Sperelakis N. (ed.) (2012). “Gibbs–Donnan Equilibrium Potentials,” in

Tester M., Blatt M.R. (1989). Direct measurement of k channels in thylakoid membranes by incorporation of vesicles into planar lipid bilayers. PubMed PMC

Van Kooten O., Snel J. F., Vredenberg W. J. (1986). Photosynthetic free energy transduction related to the electric potential changes across the thylakoid membrane. PubMed DOI

Vredenberg W. J. (1981). P515: a monitor of photosynthetic energization in chloroplast membranes.

Vredenberg W. J. (1997). Electrogenesis in the photosynthetic membrane: fields, facts and features.

Vredenberg W. J., Bulychev A. (2003). Photoelectric effects on chlorophyll fluorescence of photosystem II in vivo. Kinetics in the absence and presence of valinomycin. PubMed DOI

Wang C., Shikanai T. (2019). Modification of Activity of the Thylakoid H(+)/K(+) Antiporter KEA3 Disturbs pH-Dependent Regulation of Photosynthesis. PubMed DOI PMC

Wang C., Yamamoto H., Narumiya F., Munekage Y. N., Finazzi G., Szabo I., et al. (2017). Fine-tuned regulation of the K(+) /H(+) antiporter KEA3 is required to optimize photosynthesis during induction. PubMed DOI

Witt H. T. (1979). Energy conversion in the functional membrane of photosynthesis. Analysis by light pulse and electric pulse methods. The central role of the electric field. PubMed DOI

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