In the present paper, we review the toxicity of sugar- and lipid-derived RCs (reactive carbonyls) and the RC-scavenging systems observed in photosynthetic organisms. Similar to heterotrophs, photosynthetic organisms are exposed to the danger of RCs produced in sugar metabolism during both respiration and photosynthesis. RCs such as methylglyoxal and acrolein have toxic effects on the photosynthetic activity of higher plants and cyanobacteria. These toxic effects are assumed to occur uniquely in photosynthetic organisms, suggesting that RC-scavenging systems are essential for their survival. The aldo–keto reductase and the glyoxalase systems mainly scavenge sugar-derived RCs in higher plants and cyanobacteria. 2-Alkenal reductase and alkenal/alkenone reductase catalyse the reduction of lipid-derived RCs in higher plants. In cyanobacteria, medium-chain dehydrogenases/reductases are the main scavengers of lipid-derived RCs.

Introduction

RCs (reactive carbonyls) are toxic carbonyl compounds that are inevitably produced in sugar metabolism. D-Glucose reacts with proteins non-enzymatically under physiological conditions to form glycated proteins, which yield sugar-derived dicarbonyls such as MG (methylglyoxal), glyoxal and 3-deoxyglucosone via oxidative degradation [1]. In addition, MG is produced during the equilibration between GAP (glyceraldehyde 3-phosphate) and DHAP (dihydroxyacetone phosphate), which is non-enzymatically or enzymatically catalysed by TPI (triosephosphate isomerase) [1]. These sugar-derived dicarbonyls induce modifications of amino acid residues such as lysine, arginine and cysteine in proteins to produce AGEs (advanced glycation end-products). The accumulation of AGEs stimulates the oxidation of cell components and the inactivation of proteins [1]. In addition, the ROS (reactive oxygen species) produced by the autoxidation of D-glucose peroxidize free and membrane-bound unsaturated fatty acids, yields α,β-unsaturated carbonyls such as acrolein and MDA (malondialdehyde) [2,3]. In addition, these lipid-derived α,β-unsaturated carbonyls induce modifications of amino acid residues such as lysine, arginine and cysteine in proteins to inactivate the physiological function of these proteins, resulting in cell dysfunction [4]. In other words, the cell injuries that originate from sugars are causes of diabetes.

Photosynthetic organisms assimilate CO2 using light energy and accumulate sugars at high concentrations in their cells. In addition, photosynthetic organisms contain equilibrium reactions involving TPI, where MG is produced during glycolysis and in the Calvin cycle. Furthermore, the ROS produced by photosynthetic electron transport can react with thylakoid membranes to produce lipid-derived α,β-unsaturated carbonyls. Thus these organisms are exposed to higher levels of toxicity from sugar- and lipid-derived RCs (dicarbonyls and α,β-unsaturated carbonyls) than heterotrophs. The concentration of MG in higher plants, i.e. 35–75 μM [5], is significantly higher than that in the typical cells of heterotrophs, i.e. 2–4 μM [6], although the concentration in higher plants may be overestimated [6]. A recent study using spinach chloroplasts showed directly that MG was produced via 3-phosphoglycerate-dependent photosynthesis in a light- and time-dependent manner (D. Takagi, H. Inoue, M. Odawara, G. Shimakawa and C. Miyake, unpublished work). Furthermore, the levels of protein carbonylation, which is known to be a marker of the accumulation of AGEs, increased in high CO2 conditions that stimulated photosynthesis [7]. We refer to the cell dysfunction caused by sugar toxicity in photosynthetic organisms as plant diabetes. Photosynthetic organisms possess RC scavenging systems to avert the danger of plant diabetes [8,9]. In the present mini-review, we present the mechanisms of RC toxicity and describe the RC-scavenging systems observed in photosynthetic organisms, i.e. higher plants and cyanobacteria.

Toxicity of sugar-derived RCs for photosynthetic organisms

Sugar-derived RCs are dangerous to higher plants. The addition of MG to plant seeds inhibits the germination of seedlings [5,10]. A mutant lacking the plastid isoform of TPI exhibited the accumulation of MG with severely stunted and chlorotic seedlings [10]. On the other hand, MG induced the production of O2 and [Ca2+] oscillations in the leaves of Arabidopsis thaliana, which led to stomatal closure [11].

In a recent study, we elucidated the metabolism of MG in spinach chloroplasts [8], where the addition of MG to illuminated chloroplasts induced the photochemical quenching of chlorophyll fluorescence, i.e. MG-stimulated photosynthetic electron transport. Furthermore, MG enhanced the light-dependent uptake of O2 into chloroplasts. In addition, the accumulation of H2O2 was observed after the illumination of chloroplasts. The MG-dependent uptake of O2 was inhibited by photosynthetic electron transport inhibitors such as 3-(3,4-dichlorophenyl)-1,1-dimethylurea and 2,5-dibromo-3-isopropyl-6-methyl-p-benzoquinone. This quenching was suppressed under anaerobic conditions. These results suggest that MG is metabolized in spinach chloroplasts, where MG is reduced as a Hill oxidant by PSI (Photosystem I) and O2 is reduced to O2 by the reduced MG. Furthermore, O2 is converted into H2O2, which is catalysed by superoxide radical dismutase [12]. This reaction showed a low Km value (100 μM) for MG compared with the NADPH-dependent MG-reducing activity in the stroma from spinach chloroplasts (described below). The concentration of MG in plant cells increases to approximately 200 μM under abiotic stress conditions, indicating that MG is most likely to induce the production of ROS under the stress conditions [8,11].

Toxicity of lipid-derived RCs for photosynthetic organisms

Lipid-derived RCs inhibit the physiological functions of higher plants. Acrolein, one of the most reactive α,β-unsaturated carbonyls, inhibits the CO2-dependent photosynthetic evolution of O2 (photosynthetic activity) in spinach chloroplasts by inactivating its Calvin cycle enzymes [13]. In the higher plant Arabidopsis, the Fv/Fm ratio reflects the quantum yield of PSII (Photosystem II), and it was decreased by approximately half after the infiltration of 10 μM acrolein compared with no treatment [14]. On the other hand, the modification of PSII proteins by MDA, an α,β-unsaturated carbonyl, causes the release of the oxygen-evolving complex 33 kDa protein, which inactivates the photosynthetic O2 evolution activity in PSII. This modification is promoted by light [15].

In a recent study, we investigated how acrolein inhibits the growth of the cyanobacterium Synechocystis sp. PCC 6803 [9]. Cyanobacteria are photosynthetic bacteria and the ancestors of chloroplasts observed in higher plants. Treatment of Synechocystis sp. PCC 6803 with 200 μM acrolein for 3 days significantly and irreversibly inhibited the growth of this bacterium. To elucidate the inhibitory mechanism, we examined the effects of acrolein on photosynthesis. In contrast with dark conditions, the addition of acrolein to Synechocystis sp. PCC 6803 under illuminated conditions reduced the photosynthetic activity. Furthermore, treatment with acrolein lowered the reducing activity of dimethyl benzoquinone, an electron acceptor in PSII, thus indicating that acrolein inhibited the PSII activity in the thylakoid membranes of Synechocystis sp. PCC 6803. The addition of 200 μM acrolein to illuminated Synechocystis sp. PCC 6803 cells gradually increased the steady-state level of chlorophyll fluorescence and decreased the quantum yield of PSII, whereas 200 μM acrolein did not inhibit respiration.

We observed that inactivation of the photosynthetic activity of Synechocystis sp. PCC 6803 by acrolein required light. Acrolein is known to react with hydroxyl radicals (HO) to produce acrolein radicals [16]. During photosynthetic electron transport, superoxide radicals (O2) are formed via the reduction of O2 by reduced quinone under conditions where the oxidation of reduced quinone is suppressed, such as high light conditions. O2 co-ordinates with the non-haem iron in the PSII complex and ferric-hydroperoxide is generated because of the production of HO [17]. Therefore, on the basis of these reactions, we proposed the molecular mechanism of light-dependent PSII inhibition by acrolein in photosynthesis. The acrolein added reacts with the HO produced during photosynthetic electron transport to yield acrolein radicals, which induce the inactivation of PSII electron transport activity. However, even after treatment with 200 μM acrolein, the PSII activity was higher than the photosynthetic activity, which indicates that the molecular mechanism of light-dependent PSII inhibition by acrolein could not be accounted for by our proposed mechanism alone.

RC-scavenging systems in higher plants

Similar to heterotrophs, photosynthetic organisms also possess RC-scavenging systems. AKR (aldo–keto reductase) reduces the aldehyde and ketone groups of RCs, particularly sugar-derived RCs, to the corresponding alcohols using NAD(P)H as electron donors [18]. In higher plants, several AKR enzymes have been reported: AKR4C1 (Hordeum vulgare L.) [19], AKR4C7 (Zea mays) [20], AKR4C12 (Aloë) [21], AKR4C14 (Oryza sativa) [22] and AKR4C8, AKR4C9, AKR4C10 and AKR4C11 (Arabidopsis) [23,24]. All of these belong to the AKR4C subfamily. The expression of AKR4C genes was enhanced under high CO2 concentration, high light and other abiotic conditions [23,24]. Under these conditions, photosynthesis was stimulated and sugar-derived RCs such as MG accumulated in the cells (D. Takagi, H. Inoue, M. Odawara, G. Shimakawa and C. Miyake, unpublished work) [25]. However, the NADPH-dependent MG-reducing activity in the stroma from spinach chloroplasts showed an extremely high Km value (approximately 6.5 mM) compared with that of the AKR4C subfamily [8,24]. This indicates that the AKR4C subfamily members are barely functional in chloroplasts.

Higher plants possess glutathione-dependent scavenging systems for sugar-derived RCs, as well as AKR. The glyoxalase system (GLO1 and GLO2) mainly scavenges MG with reduced glutathione (GSH). During the initial step of the glyoxalase system, GSH non-enzymatically reacts with MG to produce hemithioacetal, which is subsequently converted into S-D-lactoylglutathione by GLO1. GLO2 catalyses the hydrolysis of S-D-lactoylglutathione to D-lactate with the regeneration of GSH [26]. The genome of Arabidopsis contains 11 GLO1 genes and five GLO2 genes [27]. In Arabidopsis, GLO2 activity was detected for a cytoplasmic GLO2, At3g10850 [28], but no GLO1 activity has been reported. In pumpkin leaves, the gene expression of GLO1 was stimulated under abiotic stress conditions [25]. Furthermore, a mutant that overexpressed glyoxalase genes exhibited enhanced salinity tolerance [29]. The concentrations of GSH in the chloroplasts of higher plants are significantly higher (approximately 3.5 mM) compared with those in the other compartments [30]. The high level of GSH in chloroplasts is likely to contribute to the detoxification of MG produced during photosynthesis.

In addition, lipid-derived RCs can be scavenged in higher plants, where 2-alkenal reductase and AOR (alkenal/alkenone reductase) catalyse the reduction of lipid-derived RCs such as acrolein and hexenal using NAD(P)H [31,32]. A mutant of Arabidopsis lacking AOR exhibited more severe damage under conditions of Methyl Viologen-induced oxidative stress compared with the wild-type [33].

RC-scavenging systems in cyanobacteria

The RC-scavenging systems of cyanobacteria differ from those of higher plants in several respects. The NADPH-dependent RC-reducing activities in the soluble fraction of Synechocystis sp. PCC 6803 showed a Km value of 0.3 mM for MG and 0.5 mM for acrolein (G. Shimakawa and C. Miyake, unpublished work) [9], which are significantly lower than those in the stroma from spinach chloroplasts, where the Km value for MG is 6.5 mM and that for acrolein is 7.0 mM [8] (R. Saito, G. Shimakawa and C. Miyake, unpublished work). Respiration and photosynthesis occur in the same compartment in cyanobacteria, i.e. the cytosol. Therefore the danger of RCs is probably even more profound in cyanobacteria than in higher plants. Thus cyanobacteria may enhance the activities of their RC-scavenging systems. To elucidate the scavenging systems in Synechocystis sp. PCC 6803, we selected proteins from the Synechocystis sp. PCC 6803 genome that may have functions in RC scavenging based on their amino acid sequence similarities to proteins with known functions in higher plants. We characterized the enzymatic properties of their GST-fusion proteins, which were expressed in Escherichia coli [34].

First, we characterized an AKR in Synechocystis sp. PCC 6803, Slr0942, which shared 41.6% homology with AKR4C9. Several amino acid residues related to the catalytic reaction are conserved in the AKR4C subfamily and are present in Slr0942: Asp52, Tyr57, Lys86 and His119. Furthermore, the amino acid residues that function during NADPH binding to the catalytic sites of AKR are conserved in Slr0942, except for Gln279 [18]. Slr0942 mainly scavenges sugar-derived RCs. The Km value of MG was lower compared with that of the AKR4C subfamily in Arabidopsis. Furthermore, we observed that Slr0942 reduced acrolein. Three AKRs are present in the Synechocystis sp. PCC 6803 genome, i.e. Slr0942, Slr1503 and Slr0545; however, the latter two enzymes lack RC-reducing activities [24,34].

We first identified the glyoxalase system in cyanobacteria [34]. Synechocystis sp. PCC 6803 possesses a GLO1, Slr0381, and a GLO2, Sll1019. The amino acid sequence of Slr0381 shared 49.6% homology with that of At1g11840, one of the GLO1 proteins in Arabidopsis; it contains three GLO motifs. The amino acid sequence of Sll1019 shared 36.6% homology with At3g10850. These two enzymes exhibited the activities of GLO1 and GLO2 respectively. The concentration of GSH is high in Synechocystis sp. PCC 6803 cells (3 mM) [35], which is probably because it protects these cells from MG toxicity.

Synechocystis sp. PCC 6803 does not possess 2-alkenal reductase or AOR, whereas the NADPH-dependent reducing activity of acrolein shows an extremely low Km value in the soluble fraction [9]. We observed that an MDR (medium-chain dehydrogenase/reductase), Slr1192, functions during the reduction of lipid-derived RCs in Synechocystis sp. PCC 6803 [34]. Slr1192 carries an alcohol dehydrogenase motif and a CAD (cynnamyl alcohol dehydrogenase) motif, which are also observed in the CAD family [36]. In higher plants, CAD functions in the biosynthesis of lignin and not in the detoxification of RCs [37], but Slr1192 has high activity against RCs, particularly lipid-derived RCs.

Slr0315, an SDR (short-chain dehydrogenase/reductase) was characterized in Synechocystis sp. PCC 6803 [34]. Slr0315 only reduced MG, but its activity was higher than that of SDR in higher plants [32]. Thus MDR and SDR are assumed to have evolved in functionally different directions compared with AKR.

Conclusions

In the present mini-review, we proposed mechanisms for the production and detoxification of RCs (Figure 1). Photosynthetic organisms convert CO2 into sugars in the Calvin cycle during photosynthesis, where sugar- and lipid-derived RCs are produced. Sugars are metabolized in glycolysis during respiration, which also produces RCs. Photosynthetic organisms such as higher plants and cyanobacteria scavenge these RCs via scavenging systems, including AKR, AOR, MDR, SDR and glyoxalase with NAD(P)H and GSH. However, the accumulation of RCs at high levels inevitably causes undesirable reactions such as protein carbonylation, ROS production and PSII photoinhibition, resulting in cell dysfunction. Thus photosynthetic organisms have plant diabetes. Photosynthetic activity will be enhanced by the increased concentration of atmospheric CO2 in the future, which is most likely to promote the production of RCs in plants. Therefore the elucidation and characterization of the physiological functions of RC-scavenging systems in photosynthetic organisms are required to ensure the future success of agriculture.

RC production and detoxification mechanisms in photosynthetic organisms

Figure 1
RC production and detoxification mechanisms in photosynthetic organisms

Production and detoxification mechanisms for RCs, such as methylglyoxal and acrolein, in higher plants (a) and in cyanobacteria (b). PET, photosynthetic electron transport.

Figure 1
RC production and detoxification mechanisms in photosynthetic organisms

Production and detoxification mechanisms for RCs, such as methylglyoxal and acrolein, in higher plants (a) and in cyanobacteria (b). PET, photosynthetic electron transport.

Glyoxalase Centennial: 100 Years of Glyoxalase Research and Emergence of Dicarbonyl Stress: A Biochemical Society Focused Meeting held at the University of Warwick, U.K., 27–29 November 2013. Organized and Edited by Naila Rabbani and Paul Thornalley (University of Warwick, U.K.).

Abbreviations

     
  • AGE

    advanced glycation end-product

  •  
  • AKR

    aldo–keto reductase

  •  
  • AOR

    alkenal/alkenone reductase

  •  
  • CAD

    cynnamyl alcohol dehydrogenase

  •  
  • GLO

    glyoxalase

  •  
  • MDA

    malondialdehyde

  •  
  • MDR

    medium-chain dehydrogenase/reductase

  •  
  • MG

    methylglyoxal

  •  
  • PS

    Photosystem

  •  
  • RC

    reactive carbonyl

  •  
  • ROS

    reactive oxygen species

  •  
  • SDR

    short-chain dehydrogenase/reductase

  •  
  • TPI

    triosephosphate isomerase

Funding

This work was supported by the Japan Society for the Promotion of Science [Scientific Research Grant number 21570041 (to C.M.)] and the Ministry of Education, Culture, Sports, Science, and Technology in Japan [Scientific Research on Innovative Area number 22114512 (to C.M. and A.M.)].

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