Formation of singlet oxygen and protection against its oxidative damage in Photosystem II under abiotic stress
Graphical abstract
Introduction
Photosystem II (PSII) is a protein–pigment complex embedded in the thylakoid membrane of oxygenic photosynthetic organisms (cyanobacteria, algae and higher plants). In higher plant, the PSII antenna complex consists of the major (light harvesting complex, LHCII) and minor (CP29, CP26, and CP24) chlorophyll a/b binding protein complexes and PSII core antenna protein complexes (CP43 and CP47) (Fig. 1) [1], [2]. In the PSII reaction center, redox-active cofactors coordinated to PsbA (D1) and PsbD (D2) proteins in two symmetrical branches comprise weakly-coupled chlorophyll dimer (PD1 and PD2), pheophytins a (PheoD1 and PheoD2), monomeric chlorophylls (ChlD1 and ChlD2), redox-active chlorophylls ChlZD1/ChlZD2, β-carotenes (CarD1 and CarD2), primary and secondary quinone electron acceptors (QA and QB) and redox active tyrosine residues (TyrZ and TyrD) (Fig. 1) [3], [4], [5]. The visible light absorbed by chlorophylls and accessory pigments in the PSII antenna complex is transferred to the PSII reaction center, where the charge separation initiates electron transport. Charge separation forms primary radical pair 1[P680+Pheo−] which transfers electron to the primary QA and the secondary QB quinone electron acceptors on the PSII electron acceptor side [6], [7], [8]. On the PSII electron donor side, highly oxidizing P680+ withdraws an electron from water-splitting manganese complex (Mn4O5Ca) via TyrZ. The latter extracts an electron from the Mn4O5Ca complex known to oxidizes water through catalytic cycle comprising of five oxidation states denoted as Si (i = 0, 1, 2, 3, 4), where i counts the stored oxidation equivalents [9].
When cyanobacteria, algae and higher plants are exposed to abiotic stress, the excitation energy transfer in the PSII antenna complex and the electron transport in the PSII reaction center are inhibited. The limitation in the excitation energy transfer and the electron transport is accompanied with the formation of reactive oxygen species (ROS). Reactive oxygen species such as singlet oxygen (1O2) is formed by the excitation energy transfer, whereas superoxide anion radical (O2−), hydrogen peroxide (H2O2) and hydroxyl radical (HO) are formed by the electron transport [10]. Under high light, 1O2 is formed by the interaction of molecular oxygen and triplet chlorophylls formed either by spin conversion via photosensitization Type II reaction in the PSII antenna complex or by the recombination of 1[P680+Pheo−] radical pair in the PSII reaction center [11], [12], [13], [14], [15]. Apart from high light, several lines of evidence have been provided that 1O2 is formed under heat [16], [17], heavy metal [18] and mechanical injury stress [19], [20]. Whereas 1O2 formation under high light via the photosensitization Type II reaction and the recombination of 1[P680+Pheo−] radical pair is well described, less is known on the mechanistic principles of 1O2 formation under other types of abiotic stresses. Evidence has been provided that 1O2 is produced during lipid peroxidation [16], [21], [22]. It has been proposed that 1O2 is formed by the decomposition of high energy intermediates (dioxetane and tetroxide) formed during lipid peroxidation and protein oxidation [23], [24].
In this review, the focus is given on 1O2 formation either by the triplet–singlet energy transfer from triplet chlorophylls to molecular oxygen or the decomposition of high energy intermediates (dioxetane and tetroxide) formed during lipid peroxidation and protein oxidation under various types of abiotic stresses such as high light, heat, heavy metals and mechanical injury.
Section snippets
Triplet–singlet energy transfer from triplet chlorophylls to molecular oxygen
Under high light, 1O2 is formed by the excitation energy transfer from triplet chlorophylls to molecular oxygen. Triplet chlorophylls are formed by the photosensitization Type II reaction in the PSII antenna complex and by the recombination of 1[P680+Pheo−] radical pair in the PSII reaction center (Fig. 2A). In the photosensitization Type II reaction, the absorption of excitation energy by chlorophylls forms the singlet chlorophylls, which are latter converted to triplet chlorophylls via
Prevention of singlet oxygen formation
To prevent deleterious effect of 1O2 on lipids and proteins, several kinds of protection comprising the prevention of triplet chlorophyll formation, the quenching of triplet chlorophylls, the scavenging of 1O2 and the scavenging of lipid radicals have been evolved in cyanobacteria, algae and higher plants. The prevention of triplet chlorophyll formation is realized by the modulation of redox potential of Pheo/Pheo− and QA/QA− redox couples [27]. The quenching of triplet chlorophylls, the
Acknowledgements
This work was supported by the Ministry of Education, Youth and Sports of the Czech Republic grants no. ED0007/01/01 (Centre of the Region Haná for Biotechnological and Agricultural Research), no. CZ.1.07/2.3.00/20.0057 (Progress and Internationalization of Biophysical Research at the Faculty of Science, Palacký University) and no. CZ.1.07/2.3.00/30.0041 (Support for Building Excellent Research Teams and Intersectoral Mobility at Palacký University). We would like to thank Deepak Kumar Yadav
References (80)
- et al.
Primary photochemistry and energetics leading to the oxidation of the (Mn) 4Ca cluster and to the evolution of molecular oxygen in Photosystem II
Coord. Chem. Rev.
(2008) - et al.
Structural models of the magnese complex of photosystem II and mechanistic implications
Biochim. Biophys. Acta
(2012) Production of reactive oxygen species by photosystem II
Biochim. Biophys. Acta
(2009)- et al.
Singlet oxygen in plants: production, detoxification and signaling
Trends Plant Sci.
(2009) - et al.
Dark production of reactive oxygen species in photosystem II membrane particles at elevated temperature – EPR spin-trapping study
Biochim. Biophys. Acta
(2007) - et al.
Autoluminescence imaging: a non-invasive tool for mapping oxidative stress
Trends Plant Sci.
(2006) - et al.
From free radicals to electronically excited species
Free Rad. Biol. Med.
(1995) - et al.
Janus-faced charge recombinations in photosystem II photoinhibition
Trends Plant Sci.
(2009) - et al.
Direct detection of singlet oxygen from isolated photosystem two reaction centres
Biochim. Biophys. Acta
(1993) - et al.
Isolated photosynthetic reaction center of photosystem two as a sensitizer for the formation of singlet oxygen
J. Biol. Chem.
(1994)
Singlet oxygen production in herbicide-treated photosystem II
FEBS Lett.
Singlet oxygen scavenging activity of plastoquinol in photosystem II of higher plants: electron paramagnetic resonance spin-trapping study
Biochim. Biophys. Acta
Role of singlet oxygen in chloroplast to nucleus retrograde signaling in Chlamydomonas reinhardtii
FEBS let
Singlet oxygen and free radical production during acceptor- and donor-side-induced photoinhibition. Studies with spin trapping EPR spectroscopy
Biochim, Biophys. Acta
Spontaneous and thermoinduced photon emission: new methods to detect and quantify oxidative stress in plants
Trends Plant Sci.
Quality control of photosystem II, reactive oxygen species are responsible for the damage to photosystem II under moderate heat stress
J. Biol. Chem.
Back-reactions, short-circuits, leaks and other energy wasteful reactions in biological electron transfer: redox tuning to survive life in O(2)
FEBS Lett.
Different roles of alpha- and beta-branch xanthophylls in photosystem assembly and photoprotection
J. Biol. Chem.
Tocochromanols, plastoquinol and other biological prenyllipids as singlet oxygen quenchers-determination of singlet oxygen quenching rate constants and oxidation products
Free Rad. Biol. Med.
Plastoquinol as a singlet oxygen scavenger in photosystem II
Biochim. Biophys. Acta
A specific role for tocopherol and of chemical singlet oxygen quenchers in the maintenance of photosystem II structure and function in Chlamydomonas reinhardtii
FEBS Lett.
Tocopherol as singlet oxygen scavenger in photosystem II
J. Plant Physiol.
Addition products of alpha-tocopherol with lipid derived free radicals
Vitam. Horm.
Evolution and functional properties of Photosystem II light harvesting complexes in eukaryotes
Biochim. Biophys. Acta
Light harvesting in photosystem II
Photosynth. Res.
Architecture of the photosynthetic oxygen-evolving center
Science
Cynobacterial photosystem II at 2.9 Å resolution and the role of quinones, lipids, channels and chloride
Nat. Struct. Mol. Biol.
Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å
Nature
AW Rutherford, Charge separation in photosystem II: a comparative and evolutionary overview
Biochim. Biophys. Acta
Light-induced quinone reduction in photosystem II
Biochim. Biophys. Acta
Singlet oxygen and photo-oxidative stress management in plants and algae
Plant Cell Environ.
Singlet oxygen production in photosystem II and related protection mechanism
Photosynth. Res.
Molecular mechanisms of production and scavenging of reactive oxygen species by photosystem II
Biochim. Biophys. Acta
Production, detection, and signaling of singlet oxygen in photosynthetic organisms
Antioxid. Redox. Signaling
The 75 °C thermoluminescence band of green tissues: Chemiluminescence from membrane–chlorophyll interaction
Photochem. Photobiol.
Vitamin E is essential for the tolerance of Arabidopsis thaliana to metal-induced oxidative stress
Plant Cell Environ.
Use of a highly sensitive two-dimensional luminescence imaging system to monitor endogenous bioluminescence in plant leaves
BMC Plant Biol.
Light as both an input and an output of wound-induced reactive oxygen formation in Arabidopsis
Plant Signal. Behav.
Linoleic acid-induced ultra-weak photon emission from Chlamydomonas reinhardtii as a tool for monitoring of lipid peroxidation in the cell membranes
PloS One
Biological hydroperoxides and singlet molecular oxygen generation
IUBMB Life
Cited by (57)
Are tomato plants co-exposed to heat and salinity able to ensure a proper carbon metabolism? – An insight into the photosynthetic hub
2024, Plant Physiology and BiochemistryPhoto-chemical aspects of iron complexes exhibiting photo-activated chemotherapy (PACT)
2023, Journal of Inorganic BiochemistryCitation Excerpt :The relaxation time of phosphorescence is slower than that of fluorescence due to spin forbidden relaxation. The triplet excited state of the transition metal complexes may be deactivated by transferring its energy to molecular oxygen with triplet state, which result in the activation of triplet molecular oxygen into the reactive singlet state [26]. Short-lived or long-lived photo-activated states of the iron complexes are involved in several physico-chemical incidents like the dissociation of ligand, energy transfer, or it can interact with the surrounding molecules including solvent.
Photosystem II photochemical adjustment of tall fescue against heat stress after melatonin priming
2022, Journal of Plant PhysiologyThe high chlorophyll fluorescence 244 (HCF244) Is potentially involved in glutathione peroxidase 7-regulated high light stress in Arabidopsis thaliana
2022, Environmental and Experimental Botany