Singlet oxygen production by photosystem II is caused by misses of the oxygen evolving complex

Abstract

Singlet oxygen ( 1 O 2 ) is a harmful species that functions also as a signaling molecule. In chloroplasts, 1 O 2 is produced via charge recombination reactions in photosystem II, but which recombination pathway(s) produce triplet Chl and 1 O 2 remains open. Furthermore, the role of 1 O 2 in photoinhibition is not clear.We compared temperature dependences of 1 O 2 production, photoinhibition, and recombination pathways.1 O 2 production by pumpkin thylakoids increased from −2 to +35°C, ruling out recombination of the primary charge pair as a main contributor. S 2 Q A − or S 2 Q B − recombination pathways, in turn, had too steep temperature dependences. Instead, the temperature dependence of 1 O 2 production matched that of misses (failures of the oxygen (O 2 ) evolving complex to advance an S-state). Photoinhibition in vitro and in vivo (also in Synechocystis), and in the presence or absence of O 2 , had the same temperature dependence, but ultraviolet (UV)radiation-caused photoinhibition showed a weaker temperature response.We suggest that the miss-associated recombination of P 680 + Q A − is the main producer of 1 O 2 . Our results indicate three parallel photoinhibition mechanisms. The manganese mechanism dominates in UV radiation but also functions in white light. Mechanisms that depend on light absorption by Chls, having 1 O 2 or long-lived P 680 + as damaging agents, dominate in red light.

Light‐induced damage to photosystem II at a very low temperature (195 K) depends on singlet oxygen

“…These results lend support to earlier data suggesting that singlet oxygen is involved in photoinhibition (e.g., Davis et al, 2016;Fufezan et al, 2002Fufezan et al, , 2007Rehman et al, 2013;Treves et al, 2016). However, photoinhibition at 20 C proceeded also in the absence of oxygen (Figure 2), indicating that oxidation by singlet oxygen is not the only mechanism of photoinhibition at 20 C. Similar findings have earlier led to the suggestion that photoinhibition at physiological temperatures proceeds via several parallel mechanisms (Mattila et al, 2022;Oguchi et al, 2009;Tyystjärvi, 2013). The observation also shows that different photoinhibition mechanisms dominate at 20 C than at À78.5 C. The conclusion is further supported by the observations that thylakoids isolated from high light-grown Arabidopsis were tolerant against photoinhibition at À78.5 C but not at 20 C (Figure 6), and that the Synechocystis ΔrpoZ strain was not more tolerant against photoinhibition at À78.5 C than the control strain (Figure 5), even though the ΔrpoZ strain produces little singlet oxygen and is tolerant against photoinhibition at 32 C (Hakkila et al, 2013).…”

“…However, the finding that photoinhibition at À78.5 C proceeded more slowly in the presence of a strong external magnetic field (Figure 3C) suggests that singlet oxygen produced via recombination of the primary charge pair is the main contributor to the observed photoinhibition at À78.5 C. The lack of a magnetic field effect on singlet oxygen production at 25 C, on the other hand, does not exclude PSII recombination reactions as the source of the triplet at 25 C, as recombinations involving Q A À (possible at 25 C though not at À78.5 C) start with noncorrelated spins, and their triplet yield would therefore be independent of a magnetic field. In particular, the miss-associated recombination of P 680 + Q A À has been shown to be important at above-zero temperatures (Mattila et al, 2022).…”

Nanodiamond Particles Reduce Oxidative Stress Induced by Methyl Viologen and High Light in the Green Alga Chlamydomonas reinhardtii

“…Exposure of the algal cells to supraoptimal light conditions (high light, HL) is often used to induce photoinhibition in photosynthetic samples [ 42 , 43 ]. Photoinhibition refers to the reduction of PSII activity under strong light, where the mechanisms include damage to PSII and the PSII repair cycle by reactive oxygen species (mainly singlet O 2 ) generated under a high light [ 39 , 42 ].…”

“…Exposure of the algal cells to supraoptimal light conditions (high light, HL) is often used to induce photoinhibition in photosynthetic samples [ 42 , 43 ]. Photoinhibition refers to the reduction of PSII activity under strong light, where the mechanisms include damage to PSII and the PSII repair cycle by reactive oxygen species (mainly singlet O 2 ) generated under a high light [ 39 , 42 ]. Therefore, we tested the ability of Chlamydomonas cells pre-incubated with 40 µg hNDs/mL to withstand HL-induced photoinhibitory and oxidative stress conditions by exposing the cultures to a PPFD of 1000 µmol/m 2 /s for a period of 4 h ( Figure 6 ).…”

Mechanistic Insights on Salicylic Acid Mediated Enhancement of Photosystem II Function in Oregano Seedlings Subjected to Moderate Drought Stress

“…PSII photodamage can appear through photooxidative stress, either at the acceptor side through 3 Chl*, which by exchanging energy and spinning with O 2 in the triplet state (molecular oxygen) results in 1 O 2 formation, or at the donor side through inactivation of the oxygen-evolving complex (OEC) [ 60 , 96 , 97 , 98 ]. Under MoDS, both H 2 O-sprayed and SA-sprayed oregano leaves exhibited a reduced efficiency of the OEC at the donor side ( Figure 5 ).…”