Abstract
Regulation of photosynthetic light harvesting in the thylakoids is one of the major key factors affecting the efficiency of photosynthesis. Thylakoid membrane is negatively charged and influences both the structure and the function of the primarily photosynthetic reactions through its electrical double layer (EDL). Further, there is a heterogeneous organization of soluble ions (K+, Mg2+, Cl−) attached to the thylakoid membrane that, together with fixed charges (negatively charged amino acids, lipids), provides an electrical field. The EDL is affected by the valence of the ions and interferes with the regulation of “state transitions,” protein interactions, and excitation energy “spillover” from Photosystem II to Photosystem I. These effects are reflected in changes in the intensity of chlorophyll a fluorescence, which is also a measure of photoprotective non-photochemical quenching (NPQ) of the excited state of chlorophyll a. A triggering of NPQ proceeds via lumen acidification that is coupled to the export of positive counter-ions (Mg2+, K+) to the stroma or/and negative ions (e.g., Cl−) into the lumen. The effect of protons and anions in the lumen and of the cations (Mg2+, K+) in the stroma are, thus, functionally tightly interconnected. In this review, we discuss the consequences of the model of EDL, proposed by Barber (1980b) Biochim Biophys Acta 594:253–308) in light of light-harvesting regulation. Further, we explain differences between electrostatic screening and neutralization, and we emphasize the opposite effect of monovalent (K+) and divalent (Mg2+) ions on light-harvesting and on “screening” of the negative charges on the thylakoid membrane; this effect needs to be incorporated in all future models of photosynthetic regulation by ion channels and transporters.
Highlights
Thylakoids and other energy transducing membranes produce ATP employing transmembrane electrochemical gradient of protons; see original papers proving this concept (Junge and Witt, 1968; Junge et al, 1968, 1970; Schliephake et al, 1968) as well as selected reviews (Junge, 2004, 2013; Junge and Nelson, 2015)
We describe the role of ELECTRICAL DOUBLE LAYER (EDL), charge neutralization on the membrane on variable Chl a fluorescence and on the regulation of light-harvesting in state transitions and during non-photochemical quenching
Chlorophyll a fluorescence transients, during both fast (∼in seconds) and slow time range, have different characteristics in plants, and in cyanobacteria (Ruban and Johnson, 2009; Papageorgiou and Govindjee, 2011; Kana et al, 2012a; Kirilovsky et al, 2014). These transients are affected by changes in several factors including: (a) the efficiency of PSII photochemistry; (b) state transitions (Ruban and Johnson, 2009); (c) the coupling and uncoupling of antenna from Photosystem I (PS I) and or Photosystem II (PS II) (Kana et al, 2009; Kirilovsky et al, 2014); (d) photoinhibition of PSII in high light (Prášil et al, 1992); (e) lumen acidification during Non-photochemical quenching (NPQ) (e.g., Ruban et al, 2012; Zaks et al, 2013; see Demmig-Adams et al, 2014); (f) the efficiency of carbon cycle reactions; and (g) divalent and monovalent ion concentrations that affect EDL, as well as the electric properties of thylakoid membranes (Barber and Mills, 1976; Barber, 1980b, 1982)
Summary
Thylakoids and other energy transducing membranes produce ATP employing transmembrane electrochemical gradient of protons; see original papers proving this concept (Junge and Witt, 1968; Junge et al, 1968, 1970; Schliephake et al, 1968) as well as selected reviews (Junge, 2004, 2013; Junge and Nelson, 2015). We note that ion screening of membrane charges represents an electrostatic interaction, and it differs from direct neutralization of membrane charges by ions (e.g., H+ binding to amino acid residues, see Barber, 1980a) The extent of this screening affects photosynthesis in various ways; effects have been observed on, e.g., variable chlorophyll (Chl) a fluorescence (Murata, 1969a), through changes in chlorophyll-proteins, in thylakoid membrane (TM) stacking (Barber, 1980a), and in excitation energy redistribution during light—induced state transitions (see e.g., Barber, 1982; Staehelin and Arntzen, 1983; Telfer et al, 1983). We describe the role of EDL (i.e., membrane screening), charge neutralization on the membrane (i.e., direct ions interaction with the membrane) on variable Chl a fluorescence and on the regulation of light-harvesting in state transitions and during non-photochemical quenching
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