Formation of singlet oxygen and protection against its oxidative damage in Photosystem II under abiotic stress

https://doi.org/10.1016/j.jphotobiol.2014.04.025Get rights and content

Highlights

Abstract

Photosystem II (PSII) is exposed to various abiotic stresses associated with adverse environmental conditions such as high light, heat, heavy metals or mechanical injury. Distinctive functional response to adverse environmental conditions is formation of singlet oxygen (1O2). In this review, recent progress on mechanistic principles on 1O2 formation under abiotic stresses is summarized. Under high light, 1O2 is formed by excitation energy transfer from triplet chlorophylls to molecular oxygen formed by the spin conversion via photosensitization Type II reaction in the PSII antenna complex or by the recombination of 1[P680radical dot+Pheoradical dot] radical pair in the PSII reaction center. Apart from well-described 1O2 formation by excitation energy transfer, 1O2 formation by decomposition of dioxetane and tetroxide is summarized as a potential source of 1O2 in PSII under heat, heavy metals and mechanical stress. The description of mechanistic principles on 1O2 formation under abiotic stress allows us to understand how plants respond to adverse environmental conditions in vivo.

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[P680radical dot+Pheoradical dot] 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 P680radical dot+ withdraws an electron from water-splitting manganese complex (Mn4O5Ca) via TyrZradical dot. 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 (O2radical dot), hydrogen peroxide (H2O2) and hydroxyl radical (HOradical dot) 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[P680radical dot+Pheoradical dot] 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[P680radical dot+Pheoradical dot] 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[P680radical dot+Pheoradical dot] 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/Pheoradical dot and QA/QAradical dot 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

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