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Review
. 2020 Jan 10;9(1):91.
doi: 10.3390/plants9010091.

Oxygen and ROS in Photosynthesis

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Free PMC article
Review

Oxygen and ROS in Photosynthesis

Sergey Khorobrykh et al. Plants (Basel). .
Free PMC article

Abstract

Oxygen is a natural acceptor of electrons in the respiratory pathway of aerobic organisms and in many other biochemical reactions. Aerobic metabolism is always associated with the formation of reactive oxygen species (ROS). ROS may damage biomolecules but are also involved in regulatory functions of photosynthetic organisms. This review presents the main properties of ROS, the formation of ROS in the photosynthetic electron transport chain and in the stroma of chloroplasts, and ROS scavenging systems of thylakoid membrane and stroma. Effects of ROS on the photosynthetic apparatus and their roles in redox signaling are discussed.

Keywords: chloroplasts; photodamage; photosynthetic electron transport chain; reactive oxygen species; redox signaling.

Conflict of interest statement

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

Figures

Figure 1
Figure 1
Singlet oxygen (1O2) generation in the antenna complex (A) and in the reaction center of PSII via charge recombination reactions (B). Proposed mechanism for the formation of 1O2 on the donor side of PSII via formation of organic peroxyl radicals (C). (A) In the antenna complex, the absorption of a photon by a molecule of Chl leads to the formation of a singlet excited state, 1Chl*, that can transform to the triplet state 3Chl via intersystem crossing. The formation of 1O2 via intersystem crossing has been demonstrated to occur in isolated LHCII [164,165]. (B) In the reaction centre of PSII, [P680+Pheo] is originally formed via electron transfer from 1P680* to Pheo in a virtual singlet state 1[P680+Pheo] that recombines to 1P680*. Charge recombination of P680+PheoQA] causes the formation of 1[P680+Pheo]. The long lifetime of the state [P680+PheoQA] destroys spin correlation, and therefore the recombination [P680+PheoQA] to 1[P680+PheoQA] often produces a “virtual triplet state” of the primary radical pair, i.e., a radical pair with such a spin configuration that, in its recombination to an excited state of the primary donor, produces a triplet, 3P680 [172,173,174]. (C) On the donor side of PSII, carbon centered radicals (R) can be formed via the oxidation of lipids and proteins by P680+ if electron donation from Mn-cluster to P680+ does not function. R are able to react with O2 to form peroxyl radical (ROO). Two peroxyl radicals react with each other to form linear tetraoxide (ROOOOR) that decomposes to 1O2, carbonyl (R=O) and alcohols (R–OH) via the Russell mechanism [200,201,202].
Figure 2
Figure 2
Formation of reactive oxygen species (ROS) in PSII. (A) Formation of superoxide (O2•−) can occur with the interaction of O2 with a semiquinone anion radicals at the QA and QB sites, when the electron flow from QB to the PQ pool is limited. The low potential form of cyt b559 can reduce O2 to O2•− inside the thylakoid membrane [234,235,236]. (B) Formation of H2O2 and HO. Cyt b559 can catalyze the formation of H2O2 inside the thylakoid membrane by a O2•− dismutation mechanism [72,160]. O2•− can reduce cyt b559 (Fe3+) to cyt b559 (Fe2+). O2•− + cyt b559 (Fe3+) ∆ O2 + cyt b559 (Fe2+). The following interaction of HO2 with Cyt b559 (Fe2+) leads to the formation of a ferric–hydroperoxo intermediate of cyt b559 (Fe3+–OOH) which can spontaneously decompose to cyt b559 (Fe3+) and H2O2. HO2 + cyt b559 (Fe2+) → cyt b559 (Fe3+–OOH) + H+→ cyt b559 (Fe3+) + H2O2. The formation of H2O2 in a cyt b559-dependent way requires the protonation of O2•− to form HO2. The interaction of O2•− with Fe2+ on the acceptor side of PSII can result in the formation of a ferric–peroxo intermediate [Fe3+–OO] that can be protonated to a ferric–hydroperoxo intermediate [Fe3+–OOH]. O2•− + [Fe2+] → [Fe3+–OO] + H+ → [Fe3+–OOH]. [Fe3+–OOH] can be reduced by an electron from QA, which causes its decomposition to a ferric–oxo intermediate [Fe3+–O] and HO. QA + [Fe3+–OOH] → QA + [Fe3+–O] + HO. (C) Formation of organic hydroperoxides on the donor side of PSII. Charge separation when the OEC is inactive leads to the formation of P680•+ and TyrZ which have a long lifetime and are therefore able to interact with surrounding molecules such as Chls, carotenoids and amino acids. The interaction of P680•+ or TyrZ with an organic molecule (RH) can proceed via a radical chain mechanism [200,201,202].
Figure 3
Figure 3
(A) Forward electron transfer chain, lifetimes and midpoint redox potentials of the cofactors of PSI; (B) charge recombination reactions and recombination lifetimes of the cofactors of PSI; the values were taken from [145,268,269,270,271]; (C) possible means of ROS formation in PSI [152,266,272,273,274,275]. PC is plastocyanin; P700 is a dimer of Chl a molecules, the primary electron donor; A0A and A0B are Chl a molecules located in branches A and B, respectively, both act as primary electron acceptors; A1A and A1B are phylloquinone molecules located in branch A and B, respectively, both acting as electron acceptors; FX, a 4Fe-4S cluster, a secondary electron acceptor; FA and FB, 4Fe-4S clusters, terminal electron acceptors.
Figure 4
Figure 4
Autocatalytic oxidation of reduced plastoquinone (PQH2) by O2 in the thylakoid membrane. 1—formation of a plastosemiquinone radical (PQH) by a dismutation reaction of PQH2 with PQ; 2—reduction in O2 by a plastosemiquinone anion radical (PQ•−) with formation of superoxide anion radical (O2•−); 3—oxidation of PQH2 by O2•− with formation of hydrogen peroxide (H2O2) and PQ; 4—diffusion of O2•− from thylakoid membrane to stroma and to lumen. In the autocatalytic oxidation of PQH2, the reaction of O2•− with PQH2 provides excess PQ•− that can be involved in the formation of O2•− and, in turn, accelerates the oxidation of PQH2 [128].
Figure 5
Figure 5
The proposed generation of O2•− in Cyt b6f. (A) In the QO site of Cyt b6f, PQH is generated (Table 2) by the 2Fe-2S cluster of the high-potential Rieske iron−sulfur protein. PQ•− that has a long residence time within the QO pocket, and cytochrome bL can also serve as a reductant for the generation of O2•− in Cyt b6f. In addition, HO2, can be reduced by cytochrome bL to form H2O2 [317]. (B) The proposed generation of O2•− in Cyt b6f in the presence of DNP-INT, an inhibitor of PQH2 oxidation by Cyt b6f. The oxidation of PQH2 does not occur in QO site, formation of PQH and its deprotonation can occur in the Qi site. PQH can be oxidized in subsequent reactions with O2 or with hemes bH or bL. H2O2 can be formed via the reaction of O2•− with PQH2 or via the reaction of HO2 with cytochrome bH or cytochrome bL.

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