Change in H+ Transport across Thylakoid Membrane as Potential Mechanism of 14.3 Hz Magnetic Field Impact on Photosynthetic Light Reactions in Seedlings of Wheat (Triticum aestivum L.).

Ekaterina Sukhova,Nikolay Ilin,Vladimir Vodeneev,Lyubov Yudina,Yana Vetrova,Anastasiia Kior,Ekaterina Gromova,Vladimir Sukhov,Evgeny Mareev

doi:10.3390/plants10102207

Abstract

Natural and artificial extremely low-frequency magnetic fields (ELFMFs) are important factors influencing physiological processes in living organisms including terrestrial plants. Earlier, it was experimentally shown that short-term and long-term treatments by ELFMFs with Schumann resonance frequencies (7.8, 14.3, and 20.8 Hz) influenced parameters of photosynthetic light reactions in wheat leaves. The current work is devoted to an analysis of potential ways of this ELFMF influence on the light reactions. Only a short-term wheat treatment by 14.3 Hz ELFMF was used in the analysis. First, it was experimentally shown that ELFMF-induced changes (an increase in the effective quantum yield of photosystem II, a decrease in the non-photochemical quenching of chlorophyll fluorescence, a decrease in time of changes in these parameters, etc.) were observed under the action of ELFMF with widely ranging magnitudes (from 3 to 180 µT). In contrast, the potential quantum yield of photosystem II and time of relaxation of the energy-dependent component of the non-photochemical quenching were not significantly influenced by ELFMF. Second, it was shown that the ELFMF treatment decreased the proton gradient across the thylakoid membrane. In contrast, the H+ conductivity increased under this treatment. Third, an analysis of the simplest mathematical model of an H+ transport across the thylakoid membrane, which was developed in this work, showed that changes in H+ fluxes related to activities of the photosynthetic electron transport chain and the H+-ATP synthase were not likely a mechanism of the ELFMF influence. In contrast, changes induced by an increase in an additional H+ flux (probably, through the proton leakage and/or through the H+/Ca2+ antiporter activity in the thylakoid membrane) were in good accordance with experimental results. Thus, we hypothesized that this increase is the mechanism of the 14.3 Hz ELFMF influence (and, maybe, influences of other low frequencies) on photosynthetic light reactions in wheat.

Highlights

Photosynthesis is a key process in plant life providing consumption of solar energy and production of biomass
The H+ transport can indirectly influence photosynthetic processes because changes in pH in the lumen and the stroma of chloroplasts regulate photosynthetic processes through the induction of the non-photochemical quenching of the chlorophyll fluorescence (NPQ), including the energy-dependent component of NPQ related to protonation of PsbS proteins in photosystem II (PSII) [4,25,26,27,28,29,30,31,32], activation of enzymes of the Calvin–Benson cycle caused by the high pH optimum of some enzymes [33,34,35], and increasing activity of the ferredoxin–NADP reductase related to pH-dependent changes in its localization in the stroma and thylakoid membrane [36,37]
It is well known that photosynthesis can be affected by numerous environmental factors including physical factors; the potential influence of extremely low-frequency magnetic fields (ELFMFs) on photosynthetic processes is still weakly investigated

Summary

Introduction

Photosynthesis is a key process in plant life providing consumption of solar energy and production of biomass. The H+ transport can indirectly influence photosynthetic processes because changes in pH in the lumen (acidification) and the stroma (alkalization) of chloroplasts regulate photosynthetic processes through the induction of the non-photochemical quenching of the chlorophyll fluorescence (NPQ), including the energy-dependent component of NPQ related to protonation of PsbS proteins in photosystem II (PSII) [4,25,26,27,28,29,30,31,32], activation of enzymes of the Calvin–Benson cycle caused by the high pH optimum of some enzymes [33,34,35], and increasing activity of the ferredoxin–NADP reductase related to pH-dependent changes in its localization in the stroma and thylakoid membrane [36,37] Considering this influence of the stromal and lumenal pH on photosynthetic processes, photosynthesis can depend on an additional H+ flux across the thylakoid membrane in the chloroplast. It is interesting that changes in these processes of H+ transport can participate in photosynthetic damage by action of stressors [16,38,39] (e.g., heating can increase proton permeability of the thylakoid membrane and, thereby, disrupts forming proton gradient across this membrane and synthesis of ATP) and in a photosynthetic adaptation to this action [41,42,43,44] (e.g., increase in proton flux caused by H+/K+ antiporter can accelerate photosynthetic adaptation to the fluctuation of light intensities through the acceleration of changes in NPQ)

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Conclusion