Cytochrome b6/f Complex as an Indigenous Photodynamic Generator of Singlet Oxygen in Thylakoid Membranes
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Possible association of photodynamic sensitization by cytochrome b6/f complex (cyt b6/f) via singlet oxygen (1O2) mechanism with photoinhibition damage to photosystem II (PS II) was studied using such subthylakoid preparations as photosystem I (PS I) particles, PS II core complex and cyt b6/f from spinach leaves. Upon exposure to bright light, PS II core complex lost photosynthetic electron transport activity to a certain extent, whose-spectral dependence implied that pheophytin a is likely involved in photoinactivation of PS II core complex in itself. The presence of PS I particles exerted virtually no effect on PS II core photoinactivation. However, the inclusion of cyt b6/f in samples resulted in a marked exacerbation of the photoinactivation, particularly in UV-A and blue light. Such effect of cyt b6/f was suppressed by azide and enhanced by the medium deuteration. Photogeneration of 1O2 from cyt b6/f was confirmed by ESR and spectrophotometry, chemically trapping 1O2. Action spectra for both 1O2 photoproduction and PS II core photoinactivation by cyt b6/f bore a close resemblance to each other, seemingly carrying the absorption characteristics of the Rieske Fe-S protein. A complex deficient in the Rieske protein prepared from intact cyt b6/f showed virtually no generation of 1O2 in light, whereas an efficient photoformation of 1O2 was seen in the Rieske protein preparation. The results suggest that cyt b6/f, rather specifically the Rieske center, may play a prominent role in photoinhibition processes through type II photosensitization in thylakoids.Keywords:
Photoinhibition
In vivo measurements of chlorophyll a fluorescence indicate that cold-hardened winter rye (Secale cereale L. cv Musketeer) develops a resistance to low temperature-induced photoinhibition compared with nonhardened rye. After 7.2 hours at 5°C and 1550 micromoles per square meter per second, the ratio of variable fluorescence/maximum fluorescence was depressed by only 23% in cold-hardened rye compared with 46% in nonhardened rye. We have tested the hypothesis that the principal site of this resistance to photoinhibition resides at the level of rye thylakoid membranes. Thylakoids were isolated from cold-hardened and nonhardened rye and exposed to high irradiance (1000-2600 micromoles per square meter per second) at either 5 or 20°C. The photoinhibitory response measured by room temperature fluorescence induction, photosystem II electron transport, photoacoustic spectroscopy, or [14C]atrazine binding indicates that the differential resistance to low temperature-induced photoinhibition in vivo is not observed in isolated thylakoids. Similar results were obtained whether isolated rye thylakoids were photoinhibited or thylakoids were isolated from rye leaves preexposed to a photoinhibitory treatment. Thus, we conclude that increased resistance to low temperature-induced photoinhibition is not a property of thylakoid membranes but is associated with a higher level of cellular organization.
Photoinhibition
Secale
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Photoinhibition
Bicarbonate
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Photoinhibition
Chloroplast stroma
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Selective Photoinhibition of Photosystem I in Isolated Thylakoid Membranes from Cucumber and Spinach
The site of photoinhibition at low temperatures in leaves of a chilling-sensitive plant, cucumber, is photosystem I [Terashima et al. (1994) Planta 193: 300]. As described herein, selective photoinhibition of PSI can also be induced in isolated thylakoid membranes in vitro. Inhibition was observed both at chilling temperatures and at 25°C, and not only in the thylakoid membranes isolated from cucumber, but also in those isolated from a chilling-tolerant plant, spinach. Comparison of these observations in vitro to the earlier results in vivo indicates that (1) photoinhibition of PSI is a universal phenomenon; (2) a mechanism exists to protect PSI in vivo; and (3) the protective mechanism is chilling-sensitive in cucumber. The chilling-sensitive component seems to be lost during the isolation of thylakoid membranes. Very weak light (10–20μmol m-2 s-1) was sufficient to cause the inhibition of PSI. About 80% of the oxygen-evolving activity by PSII was maintained even after the activity of PSI had decreased by more than 70%. This is the first report of the selective photoinhibition of PSI in vitro.
Photoinhibition
Spinacia
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The relationship between thylakoid membrane fluidity and the process of photoinhibition at room and low (4 °C) temperature was investigated. Two different membrane perturbing agents - cholesterol and benzylalcohol were applied to manipulate the fluidity of isolated pea thylakoids. The photochemical activity of photosystem I (PSI) and photosystem II (PSII), polarographically determined, were measured at high light intensity for different time of illumination at both temperatures. The exposure of cholesterol- and benzylalcohol-treated thylakoid membranes to high light intensities resulted in inhibition of both studied photochemical activities, being more pronounced for PSII compared to PSI. Time dependencies of inhibition of PSI and PSII electron transport rates for untreated and membranes with altered fluidity were determined at 20 °C and 4 °C. The effect is more pronounced for PSII activity during low-temperature photoinhibition. The data are discussed in terms of the determining role of physico-chemical properties of thylakoid membranes for the response of photosynthetic apparatus to light stress.
Photoinhibition
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Inhibition of photosynthesis by excess excitation energy is initiated in the reaction center of photosystem II. The primary site of photoinhibition in the reaction center (components of primary charge separation or secondary electron acceptor Q B ) is still disputed. Photoinhibition is characterized by quenching of variable chlorophyll flurescence (F v ), resulting from increased thermal dissipation of excitation energy. Varying responses of initial fluorescence (F 0 ), however, seem to indicate involvement of different mechanisms. As far as photoinhibition is reversible within minutes to hours, it can be viewed as a controlled protective mechanism that serves to dissipate excessive energy, Supposedly, another dissipative mechanism, distinguished by its faster kinetics (response within seconds), is related to the energy‐dependent fluorescence quenching.
Photoinhibition
Heterolysis
Non-photochemical quenching
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We have studied photoinhibition of photosynthesis in the cyanobacterium Synechococcus sp. PCC 7942, which possesses two distinct forms of the photosystem II reaction-center protein D1 (D1:1 and D1:2). We report here that when cells adapted to a growth irradiance of 50 mumol.m-2.s-1 are exposed to an irradiance of 500 mumol.m-2.s-1, the normally predominant D1 form (D1:1) is rapidly replaced with the alternative D1:2. This interchange is not only complete within the first hour of photoinhibition but is also fully reversible once cells are returned to 50 mumol.m-2 x s-1. By using a mutant that synthesizes only D1:1, we show that the failure to replace D1:1 with D1:2 during photoinhibition results in severe loss of photosynthetic activity as well as a diminished capacity to recover after the stress period. We believe that this interchange between D1 forms may constitute an active component in a protection mechanism unique among photosynthetic organisms that enables cyanobacteria to effectively cope with and recover from photoinhibition.
Photoinhibition
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The effect of copper on photoinhibition of photosystem II (PSII) in vitro was studied in bean ( Phaseolus vulgaris L. cv. Dufrix) and pumpkin ( Cucurbita pepo L.) thylakoids. The thylakoids were illuminated at 200–2 000 μmol photons m −2 s −1 in the presence of 70–1 830 added Cu 2+ ions per PSII. Three lines of evidence show that the irreversible damage of PSII caused by illumination of thylakoids in the presence of Cu 2+ was mainly due to donor‐side photoinhibition resulting from inhibition of the PSII donor side by Cu 2+ . First, addition of an artificial electron donor partially restored PSII activity of thylakoids that had been illuminated in the presence of Cu 2+ . Second, already moderate light was enough to cause rapid inhibition of PSII, and the inhibition could be saturated by light. Third, the extrinsic polypeptides of the oxygen‐evolving complex were found to become oxidized by the combined effect of Cu 2+ and light. The presence of oxygen was not necessary for the copper‐induced enhancement of photoinhibition of PSII. When the illumination was prolonged, copper caused a gradual collapse of the thylakoid structure by increasing degradation of thylakoid proteins.
Photoinhibition
Cucurbita pepo
Oxygen evolution
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Photoinhibition
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The effects of the positive charges of amines such as spermine (SPM), putrescine (PUT) and methylamine (MET) on the protection of PSII against excessive illumination were investigated in isolated thylakoid membranes. Under photoinhibition conditions, water oxidation, the kinetics of the Chl fluorescence rise and charge recombination in PSII were affected. A low concentration of SPM (1 mM) added before photoinhibition produced a significant improvement of Fv/F0, the oxygen yield and the amplitude of the B-band of thermoluminescence compared with the other amines. Amongst the amines studied, only SPM could protect the photosynthetic apparatus under photoinhibition conditions. This protection was probably provided by the polycationic nature of SPM (four positive charges at physiological pH), which can stabilize surface-exposed proteins of PSII through electrostatic interaction.
Photoinhibition
DCMU
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