Photoinhibition of photosystem II in vivo is preceded by down-regulation through light-induced acidification of the lumen: Consequences for the mechanism of photoinhibition in vivo

Abstract

The mechanism of photoinhibition of photosystem II (PSII) was studied in intact leaf discs of Spinacia oleracea L. and detached leaves of Vigna unguiculata L. The leaf material was exposed to different photon flux densities (PFDs) for 100 min, while non-photochemical (qN) and photochemical quenching (qp) of chlorophyll fluorescence were monitored. The 'energy' and redox state of PSII were manipulated quite independently of the PFD by application of different temperatures (5-20° C), [CO2] and [O2] at different PFDs. A linear or curvilinear relationship between qp and photoinhibition of PSII was observed. When [CO2] and [O2] were both low (30 μl · l(-1) and 2%, respectively), PSII was less susceptible at a given qp than at ambient or higher [CO2] and photoinhibition became only substantial when qp decreased below 0.3. When high levels of energy-dependent quenching (qE) (between 0.6 and 0.8) were reached, a further increase of the PFD or a further decrease of the metabolic demand for ATP and NADPH led to a shift from qE to photoinhibitory quenching (qI). This shift indicated that photoinhibition was preceded by down-regulation through light-induced acidification of the lumen. We propose that photoinhibition took place in the centers down-regulated by qE. The shift from qE to qI occurred concomitant with qP decreasing to zero. The results clearly show that photoinhibition does not primarily depend on the photon density in the antenna, but that photoinhibition depends on the energy state of the membrane in combination with the redox balance of PSII. The results are discussed with regard to the mechanism of photoinhibition of PSII, considering, in particular, effects of light-induced acidification on the donor side of PSII. Interestingly, cold-acclimation of spinach leaves did not significantly affect the relationship between qP, qE and photoinhibition of PSII at low temperature.

The effect of zearalenone on PSII photochemical activity and growth in wheat and soybean under salt (NaCl) stress

“…The data showing that preceding sowing incubation of seeds in ZEN solutions resulted in an increase in the nonphotochemical quenching (qE, qT) during strong illumination for both species (Table 4) are consistent with the opinions of other authors (Fork and Satoh 1986;Horton and Hauge 1988;van Wijk and van Hasselt 1993;Ting and Owens 1994;Ruban and Horton 1995;Owens 1996;Haldrup et al 2001) that such response may be recognized as the action of the first defense line for the photosynthetic apparatus against photoinhibitory injuries and other photooxidative ones. In our experiment it was observed that ZEN prevented photoinhibitory injuries during strong illumination due to the safe dissipation of the excess of absorbed light energy through mechanisms related to the development of pH gradient (qE) in thylakoids and phosphorylation of LHC2 (qT).…”

“…The experimental protocol for the estimation of these components of qN was essentially the same as that described by Walters and Horton (1991). The non-photochemical quench qN is based on three major constituents: the energy quenching qE, qT and qI caused by a photoinhibition of PSII units (Fork and Satoh 1986;Horton and Hauge 1988;van Wijk and van Hasselt 1993;Ting and Owens 1994;Ruban and Horton 1995;Owens 1996;Haldrup et al 2001). qE is thought to occur in PSII antennae and there is evidence that it is regulated by the pH gradient across the thylakoid membrane and by the interconversion of pigments in the xanthophylls cycle (Owens 1996;Ting and Owens 1994;Ruban and Horton 1995).…”

Reversible Photoinhibition in Antarctic Moss during Freezing and Thawing

“…These data suggest that there may be multiple mechanisms leading to fluorescence quenching during freezing. It has been proposed that reversible photoinhibition during colcl temperatures is due to changes within PSII centers that lead to dissipation o1 energy within the reaction center of PSII (Hurry and Huner, 1992;van Wijk and van Hasselt, 1993), a proposal that supports the reaction center quenching model of Weis and Berry (1987). A proposed mechanwn of PSII deactivation is through the loss of calcium ions (Krieger and Weis, 1993).…”

An Investigation of the Sustained Component of Nonphotochemical Quenching of Chlorophyll Fluorescence in Isolated Chloroplasts and Leaves of Spinach

“…It is associated with the presence of zeaxanthin and could therefore represent a more sustained modification of the LHCII system. Alternatively, it is possible that it could arise from a variety of effects on PSII, such as damage to the PSII reaction center or a downregulation of the PSII donor side, perhaps by release of Ca'+ (Krause et al, 1990;Giersch and Krause, 1991;Oquist et al, 1992;van Wijk and van Hasselt, 1993).…”