Singlet Oxygen in Plants: Generation, Detection, and Signaling Roles: History
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Subjects: Plant Sciences
Contributor:
Valeriya A. Dmitrieva
,
Elena V. Tyutereva
,
Olga V. Voitsekhovskaja

In a recent review published in Int. J. Mol. Sci. (https://doi.org/10.3390/ijms21093237), we summarize the current understanding of the sites and mechanisms of production of singlet oxygen (1O2) in the plant body, and of emerging physiological roles of 1O2 production in plants. We consider well-characterized mechanisms of 1O2 generation in chloroplast grana cores and novel data on 1O2 formation at grana margins. We discuss signal functions of 1O2 in acclimation to excess light, in chloroplast quality control and in the initiation of programmed cell death (PCD), as well as the less clear roles of stress-related 1O2 production in roots. We argue that infiltration of 1O2-specific membrane-impermeable fluorescent probes in the apoplast provides a useful comparative approach to estimate levels of 1O2 formation in chloroplasts. We present a preliminary overview of cellular mechanisms and signaling pathways leading to 1O2-triggered PCD in plants.

  • singlet oxygen
  • plant acclimation to excess light
  • programmed cell death

During photosynthesis, specifically in the course of water oxidation, molecular oxygen in its ground triplet state (3O2) is generated which is released into the atmosphere. Oxygen can be converted to reactive oxygen species (ROS) either via acquisition of electrons or via acquisition of energy. The latter pathway results in the formation of singlet oxygen (1O2) which represents the first excited electronic state of molecular oxygen. 1O2 is much more reactive than 3O2 and readily oxidizes different biological molecules; therefore, it can be toxic [1].

In plants, the main source of 1O2 is photosystem II (PS II) in chloroplasts [2,3]. PSII reaction centers are the sites of formation of long-lived excited triplet states (3Chl*) of the P680 chlorophyll “special pair”. The triplet states of chlorophylls can transfer their excitation energy to oxygen leading to the formation of 1O2 [4]. 1O2 production essentially increases under high light conditions. Under such conditions, irreversible damage of PS II can occur. It was shown that 1O2 can inhibit the repair of the proteins of the PS II reaction center [5] which leads to down-regulation of photosynthesis, a phenomenon referred as photoinhibition [6,7]. Notably, the main sites of 1O2 generation under high light conditions are the cores of chloroplast grana.

Apart from the P680 “special pair” chlorophyll, other compounds can act as photosensitizers and cause 1O2 generation. In particular, in chloroplasts, the chlorophyll precursors chlorophyllide and protochlorophyllide can function as photosensitizers [3,8,9]. These molecules, however, occur very rarely as free compounds; yet, free chlorophylls, chlorophyllides and protochlorophyllides might occur at grana margins where they participate in the assembly of newly synthesized, as well as in the disassembly of damaged, PSII complexes. Therefore, grana margins are sites of 1O2 generation indicative of accumulation of free chlorophylls or free chlorophyll precursors. Another, recently suggested, source of 1O2 generation at grana margins are incomplete PS II complexes lacking an oxygen evolving complex (OEC) [10]. In such PSII complexes, the long-lived ion-radical pair P680•+TyrZ• (where TyrZ is the tyrosine residue which transfers the electrons from the OEC to P680•+) might form in the light, leading to the generation of lipid and protein hydroperoxides [10]. These tetrahydroperoxides can produce 1O2 while decomposing [11].

Minor sources of 1O2 production in plants can be triplet carbonyls of lipids and proteins which are able to transfer energy to triplet oxygen [10]. Some enzymatic reactions like those mediated by heme proteins and lipoxygenases were shown to lead to 1O2 generation [12]. Important sources of 1O2 production are phytoalexins which function as defense compounds. In particular, phenalenone-like phytoalexins are photosensitizers playing a key role in 1O2 generation during protection against pathogens [13]. Noteworthily, 1O2 can be produced not only in leaves, but also in roots of plants [14,15].

Although the lifetime of 1O2 is very short (ca. 10−6 s), it can diffuse from the site of its generation over a distance of approximately 155 nm [16], and permeate through membranes. Thus, 1O2 readily oxidizes neighboring molecules: its most common targets are proteins [17] but 1O2 also attacks DNA and lipids [4,18,20]. Products of lipid peroxidation can act as signal molecules eventually causing cell death [19]. Plants have evolved a variety of mechanisms of defense from 1O2. On the large scale, the most important 1O2 quenchers are carotenoids [8]. Apart from physical quenching of 1O2 (i.e. energy dissipation as heat), the b-carotene in the reaction centers of PSII can act as a chemical quencher by being oxidized by 1O2. This reaction leads to the formation of volatile signaling molecules such as the endoperoxide of b-carotene, b-cyclocitral, a specific signature of 1O2 production at grana cores in chloroplasts.

1O2 is a prominent signal in chloroplast-to-nucleus signaling pathways. The main signaling roles of 1O2 revealed thus far are part of plants’ acclimation to high light and the induction of PCD, respectively [21]. Two 1O2-mediated signaling pathways have been studied in two Arabidopsis thaliana mutants specifically producing high levels of 1O2 either at grana margins (flu) or at grana cores (ch1) in chloroplasts. It was shown that after transfer from the darkness to light, flu plants accumulate free protochlorophyllide which acts as a strong photosensitizer resulting in 1O2 production at grana margins [19,22,23]. ch1 mutants are unable to synthesize chlorophyll b, which leads to decreased functional activity of PS II and a disturbance of lateral diffusion in thylakoid membrane [24-26], resulting in an essential increase of 1O2 production at grana cores [24]. In flu, nuclear-encoded chloroplast proteins, EXECUTER1 (EX1) and EX2 are specifically activated by 1O2, and lead to activation of PCD [23]. In ch1, a serine-threonine kinase OXIDATIVE SIGNAL INDUCIBLE1 (OXI1) plays the key role in 1O2-dependent PCD, while EX1/2 do not seem to be involved [24]. Recently, a novel signaling pathway mediated by the SAFEGUARD1 (SAFE1) chloroplast protein was proposed, where SAFE1 physically protects grana margins from damage and at the same time might trigger an EX1/2 independent PCD [29].

Phytohormones jasmonic acid (JA) and salicylic acid (SA) play an important role in the transduction of 1O2 signals leading to PCD during both EX1- and OXI1-mediated pathways. JA causes PCD in both flu and ch1 mutants. Moreover, in ch1 mutants, the levels of JA and other jasmonates “define” whether PCD or acclimation to 1O2 will occur [30]. In ch1 mutants, the acclimation response to excess light and to high levels of 1O2 production specifically involves signaling by b-cyclocitral [30]. In summary, two major retrograde-to-nucleus signaling pathways mediated by 1O2 allow plants to distinguish between its production at grana cores and at grana margins, respectively; while the former can result either in acclimation or in induction of PCD, the latter specifically activates PCD. Another recently discovered 1O2 signaling pathway is related to chloroplast quality control [31].

To date, our understanding of mechanisms of 1O2-mediated PCD remains incomplete. In particular, it is known that 1O2 can trigger PCD in roots but the components of signal transduction pathways have not been studied sufficiently. Undoubtedly, chloroplasts play a key role in 1O2-mediated PCD in leaves but PCD involves other cell compartments as well. For instance, photosensitizers such as red-chlorophyll-catabolite can be transported from chloroplasts to mitochondria and thereby induce 1O2-mediated PCD in mutants lacking the ACCELERATED CELL DEATH2 protein [32,33]. A recently revealed important player in 1O2-mediated PCD is the endoplasmic reticulum (ER)-mediated unfolded protein response (UPR) [33]. Furthermore, it was shown that 1O2 produced in the vacuole and at the plasma membrane can be involved in vacuole-mediated PCD [34].

A variety of methods detecting 1O2 has been developed. The most selective is electron paramagnetic resonance (EPR) spectroscopy which enables the identification of 1O2 based on spectral characteristics of “trapping” molecules that form radicals after interaction with 1O2 [35,36]. This technique, however, has a serious limitation in that it cannot be applied to plants in vivo due to its high sensitivity to reductants, especially to those produced in illuminated thylakoids, and to the high water contents in plant tissues. Therefore, specific fluorescent probes changing their properties after reaction with 1O2 have been developed [37,38]. 1O2 generation in chloroplasts can be studied with the use of fluorescing spin probe DanePy; 1O2 quenches its fluorescence in a quantitative manner. Another available, highly selective probe is Singlet Oxygen Sensor Green (SOSG) [39]. The use of this probe is quite convenient, as SOSG solutions can be introduced into leaves by vacuum-infiltration [40,41]. Finally, 1O2 can be detected by in vivo imaging of plants for the detection of autoluminescence which arises due to spontaneous photon emission during decomposition of lipid hydroperoxides and endoperoxides produced by 1O2-caused lipid oxidation [42,43].

Altogether, 1O2 is highly significant for plants. Its detection and signal transduction in plants can lead to opposite strategies such as stress acclimation or induction of PCD. For this reason, elucidation of the mechanisms of its perception and signal transduction is required. Moreover, it is important to extend the knowledge obtained using Arabidopsis to other plant species including crops.[1][2][3][4][5][6][7][8][9][10][11][12][13][14][15][16][17][18][19][20][21][22][23][24][25][26][27][28][29][30][31][32][33][34][35][36][37][38][39][1][2][3][4][5][6][7][8][9][10][11][12][13][14][15][16][17][18][19][20][21][22][23][24][25][26][27][28][29][30][31][32][33][34][35][36][37][38][39][40][41][42][43]

This entry is adapted from the peer-reviewed paper 10.3390/ijms21093237

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