Light-Induced Oxidative Stress, N-Formylkynurenine, and Oxygenic Photosynthesis

Abstract

Light stress in plants results in damage to the water oxidizing reaction center, photosystem II (PSII). Redox signaling, through oxidative modification of amino acid side chains, has been proposed to participate in this process, but the oxidative signals have not yet been identified. Previously, we described an oxidative modification, N-formylkynurenine (NFK), of W365 in the CP43 subunit. The yield of this modification increases under light stress conditions, in parallel with the decrease in oxygen evolving activity. In this work, we show that this modification, NFK365-CP43, is present in thylakoid membranes and may be formed by reactive oxygen species produced at the Mn4CaO5 cluster in the oxygen-evolving complex. NFK accumulation correlates with the extent of photoinhibition in PSII and thylakoid membranes. A modest increase in ionic strength inhibits NFK365-CP43 formation, and leads to accumulation of a new, light-induced NFK modification (NFK317) in the D1 polypeptide. Western analysis shows that D1 degradation and oligomerization occur under both sets of conditions. The NFK modifications in CP43 and D1 are found 17 and 14 Angstrom from the Mn4CaO5 cluster, respectively. Based on these results, we propose that NFK is an oxidative modification that signals for damage and repair in PSII. The data suggest a two pathway model for light stress responses. These pathways involve differential, specific, oxidative modification of the CP43 or D1 polypeptides.

Oxidized Amino Acid Residues in the Vicinity of QA and PheoD1 of the Photosystem II Reaction Center: Putative Generation Sites of Reducing-Side Reactive Oxygen Species

“…Recently, we identified a number of oxidized CP43 residues ( 354 E, 355 T, 356 M and 357 R) which are located in close proximity to the manganese cluster and which may be associated with an oxygen/ROS egress channel on the oxidizing side of the photosystem [20]. Barry and coworkers have also identified oxidatively modified tryptophan residues on both the CP43 ( 365 W) and D1 ( 317 W) proteins which appear to be targets for oxidizing side ROS [21], [22], [23]. Additionally, reductants produced by PS II, such as Q B −2 [24], Pheo D1 − [25], Q A − [26], and, possibly, reduced low potential cytochrome b 559 [27], [28], appear to have redox potentials and lifetimes sufficient to reduce molecular oxygen and have been hypothesized to be sources of ROS.…”

Tripping up Trp: Modification of protein tryptophan residues by reactive oxygen species, modes of detection, and biological consequences

“…In the gathering of light energy, the plant photosynthetic machinery is continuously faced with conditions that generate both radical and non-radical oxidative species [92]. Leakage from the electron transport chains in both photosystems I and II, especially under high light conditions, can result in the production of 1 O 2 , H 2 O 2 and hydroxyl radical.…”

FtsH2-Dependent Proteolysis of EXECUTER1 Is Essential in Mediating Singlet Oxygen-Triggered Retrograde Signaling in Arabidopsis thaliana

“…Because EX1 is associated with PSII and FtsH protease, upon 1 O 2 generation, EX1 possibly undergoes similar oxidative post-translational modification as PSII RC proteins including D1 and CP43 (Dreaden et al, 2012). If the oxidation occurs in EX1, the modified EX1 by 1 O 2 may become a target of FtsH protease, which is shown to be the case of D1 (Kato and Sakamoto, 2009).…”