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Methylglyoxal and glyoxalase system in plants: old players, new concepts.

Introduction

Methylglyoxal (MG; CH3COCHO) which is a typical oxygenated short aldehyde is a by-product of several metabolic pathways, including glycolysis, photosynthesis, lipid peroxidation and oxidative degradation of glucose and glycated proteins, its production is spontaneous and unavoidable, overaccumulation of MG is a common phenomenon under abiotic and biotic stresses in plants (Kaur et al., 2014a, b; Hossain et al, 2011, 2016; Singh & Dhaka, 2016). MG has dual role, that is, it can function as both a cytotoxin at high concentration and signal molecule at low concentration in plants. MG at cytotoxic levels inhibits cell proliferation and results in a number of adverse effects, including increasing the degradation of proteins through the formation of advanced glycation end products (AGEs); inactivating the antioxidant defense system such as superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX), glutathione reductase (GR), glutathione S-transferase (GST) and glutathione peroxidase (GPX); increasing sister chromatic exchange and endoreduplication; inducing DNA strand breaks and increases point mutations. Finally, MG causes disruption of cellular functions, and even cell death (Martins et al., 2001; Wang et al., 2003; Hoque et al., 2012a; Kaur et al., 2014a, b; Hossain et al., 2016; Singh & Dhaka, 2016).

To combat with above-mentioned potential threats, during evolution, plants have developed a unique detoxification system of MG, including glyoxalase system and other dehydrogenase system (non-glyoxalase system). Plant glyoxalase system mainly includes glyoxalase I (Gly I; lactoylglutathione lyase; EC 4.4.1.5) and glyoxalase II (Gly II; hydroxyacylglutathione hydrolase; EC 3.1.2.6), both of which are considered to be important for maintaining a robust stress tolerance response in plants by MG detoxification and maintaining glutathione (GSH) homeostasis (Devanathan et al., 2014; Kaur et al., 2014a, b; Hossain et al., 2016; Singh & Dhaka, 2016). Under abiotic and biotic stresses, glyoxalases are differentially regulated and their overexpression confers tolerance of plants to various abiotic stressors (Yadav et al., 2005a, b, 2005c; Viveros et al., 2013). In addition, endogenous MG can increase 2 ~ 6-fold in many plant species under abiotic stress such as salinity, drought, cold, heavy metal and high light stresses and its accumulation appears to be closely associated with basic stress responses (Hossain & Fujita, 2009; Yadav et al., 2005a, b), indicating that MG may be a second messenger in the response of plants to stressful environments. Thus, further study of MG metabolism and the regulation of MG by the glyoxalase system will be of great importance in plants especially crop plants under abiotic stress conditions (Hossain et al., 2011, 2014). Meanwhile, the regulatory roles of the glyoxalase system have recently attracted much attention in abiotic stress tolerance research in plants. On the basis of current advances on MG and its detoxification system glyoxalase, in this review, MG biosynthesis and degradation; determination of MG; MG as signal initiator crosstalk with [Ca.sup.2+], reactive oxygen species (ROS) and abscisic acid (ABA); abiotic stress tolerance involved in MG and glyoxalase; stomatal movement; seed germination; as well as cell division and organ differentiation, were summarized, the aim is to better understand MG and its detoxification system function in plants especially in abiotic stress conditions.

MG Metabolism

MG, a reactive [alpha], [beta]-dicarbonyl ketoaldehyde, is synthesized endogenously via several enzymatic and non-enzymatic pathways (Chakraborty et al., 2014; Kaur et al., 2014a, b; Hossain et al., 2016; Singh & Dhaka, 2016). The production of endogenous MG originates from carbohydrates, proteins and lipid metabolism in the mitochondria, chloroplasts and the cytosol of plant cells (Chakraborty et al., 2014; Kaur et al., 2014a, b; Hossain et al., 2016; Singh & Dhaka, 2016; Fig. 1). The glyoxalase system (mainly Gly I and Gly II) is an integral component and the major pathway for detoxification of MG in living organisms including plants (Cheng et al., 2012; Mustafiz et al., 2014; Kaur et al., 2014a, b; Hossain et al., 2016; Singh & Dhaka, 2016). Commonly, MG metabolic pathway is present in the cytosol of plant cells and cellular organelles, particularly mitochondria (Yadav et al., 2008; Rabbani & Thornalley, 2012), which was presented as follows respectively.

MG Biosynthesis

Enzymatic Pathways

The enzymatic synthesis of MG at least includes four potential pathways in plants: (1) glyceraldehyde-3-phosphate (G3P) pathway: Triosephosphate (TP) isomerase (TPI) hydrolyzes G3P or DHAP to yield MG and phosphate (Pi), this is the major source of MG formation; (2) acetol pathway: acetone monooxygenase catalyzes acetone (a metabolite of fatty acids) to acetol, the latter is converted to MG by acetol monooxygenase (AMO); (3) aminoacetone pathway: in this pathway, semicarbazide-sensitive amine oxidase (SSAO) is able to convert aminoacetone (a metabolite of protein) into MG; (4) dihydroxyacetone phosphate (DHAP) pathway: MG can be produced from DHAP via MG synthase (MGS) (Kaur et al., 2014a, b; Hossain et al., 2016; Singh & Dhaka, 2016; Fig. 1). In addition, in animal systems, the degradation of lipid peroxidation also generates products like MG and 4-hydroxynon-2-enal (Kaur et al., 2014a, b; Hossain et al., 2016; Singh & Dhaka, 2016). However, whether these mechanisms of MG formation are contributing to total MG in plants still needs to be established.

Non-enzymatic Pathways

In addition to enzymatic pathways, MG also can be formed spontaneously in plants by non-enzymatic mechanisms from glycolysis and from photosynthesis intermediates like G3P and DHAP underphysiological conditions (Kaur et al., 2014a, b; Hossain et al., 2016; Singh & Dhaka, 2016; Fig. 1). Under stress conditions, the rate of glycolysis increases, leading to an imbalance (in the initial and latter five reactions) in the pathway. TPs are very unstable metabolites, and removal of the phosphoryl group by [beta]-elimination from 1, 2-enediolate of these TPs leads to the formation of MG (Kaur et al., 2014a, b; Hossain et al., 2016; Singh & Dhaka, 2016). Therefore, spontaneous production of MG is an unavoidable consequence of the glycolysis pathway under stress conditions.

MG Degradation

Because MG is both a mutagen and a genotoxic agent at high concentration, it is very important to maintain MG homeostasis in plant cells during various abiotic and biotic stress conditions, which is one of the most important adaptive strategies of plant stress tolerance. MG homeostasis in plant cells is mainly regulated by glyoxalase system and non-glyoxalase system presented as follows.

Glyoxalase System of MG Detoxification

As mentioned above, the glyoxalase system is the major pathway of degradation of MG present in the cytosol of cells and cellular organelles, particularly mitochondria, in living systems including plants (Kaur et al., 2014a, b; Flossain et al., 2016; Singh & Dhaka, 2016). In animal system, the function of the glyoxalase pathway has been studied extensively, but less in plants. Glyoxalase system consists mainly of two enzymes: Gly I and Gly II. The spontaneous reaction between GSH and MG forms hemithioacetal (HTA), which is then converted to S-D-lactoylglutahione (SLG) by Gly 1. In addition, Gly II catalyzes the hydrolysis of SLG to form D-lactate and GSH, and the latter is recycled back into the system (Kaur et al., 2014a, b; Hossain et al., 2016; Singh & Dhaka, 2016; Fig. 1). Therefore, MG detoxification is strongly dependent on the availability of cellular GSH. Deficiency of GSH limits the production of HTA, leading to the accumulation of MG and cell damage (Kaur et al., 2014a, b; Hossain et al., 2016; Singh & Dhaka, 2016). In addition, in Arabidopsis thaliana, Kwon et al. (2013) and Ghosh et al. (2016) also found a novel glyoxalase known as glyoxalase III (Gly III), which directly catalyzes the conversion of MG into D-lactate without involvement of GSH. Recent years, many investigations have brought new developments in the involvement of the glyoxalase system in stress tolerance and its involvement with oxidative defense systems in plants, and the pioneering work provides a potential framework for interpreting the physiological roles of MG and the glyoxalase system in higher plants against various abiotic stresses (Veena et al., 1999; Singla-Pareek et al., 2003; Saxena et al., 2005; Yadav et al., 2005a, b).

Non-glyoxalase Metabolism of MG

Except for glyoxalase system, MG can be degraded by non-glyoxalase system in living systems including plants. Because MG contains two functional groups (aldo- and keto-), it can be either oxidized or reduced by aldose/aldehyde reductase (ALR) or aldo-keto reductase (AKR) using NADH or NADPH to form acetol, lactaldehyde and pyruvate (Kaur et al, 2014a, b; Hossain et al., 2016; Singh & Dhaka, 2016). MG dehydrogenase (MDDH), MG reductase (MDR) and aldehyde dehydrogenase (ADH), respectively, catalyzes the conversion of MG into pyruvate, L-lactaldehyde and D-lactaldehyde, and L-/D-lactaldehyde is then converted to pymvate by L-/D-lactate dehydrogenase (L-/D-LDH), the pyruvate finally enters into tricarboxylic acid cycle (TCA) (Kaur et al., 2014a, b; Hossain et al., 2016; Singh & Dhaka, 2016). Among the reductase family, ALR and AKR are currently attracting much interest since it converts MG to acetol and lactaldehyde. Overexpression of the ALR or AKR gene in tobacco increases tolerance against oxidative stress, extreme temperature, Cd and drought stress, and the transgenic plants also exhibited higher AKR activity and less MG accumulation under heat stress conditions (Oberschall et al., 2000; Hegedus et al., 2004; Turoczy et al., 2011).

Determination of MG

Because MG is a cytotoxin at high concentration, its homeostasis is of great importance in plant growth, development and the acquisition of stress tolerance. In addition, in order to further understand the functions of MG, it is necessary to precisely determine the concentration of MG in biological sample. Measurement method for MG is mainly spectrophotometry, which commonly include Gly I, 2,4-dinitrophenylhydrazine (DNP) and N-acetyl-L-cysteine (NAC) methods (Racker, 1951; Gilbert & Brandt, 1975; Wild et al., 2012).

Gly I method is an enzyme-catalyzed endpoint assay based on the glyoxalase I catalyzed formation of SLG from MG. SLG has the maximum absorbance at 240 nm, and the concentration of SLG was calculated using a molecular absorption coefficient of 3430 [M.sup.-1] [cm.sup.-1] (determination limitation of MG is 50 ~ 500 uM) at pH 6.6 (Racker, 1951; Wild et al., 2012). This method is a "gold standard" method for the determination of MG concentration in the millimolar range. However, as this assay used purified Gly I, which is quite expensive and easy to loss activity (Wild et al., 2012).

In DNP method, MG reacts with DNP and forms MG-bis-2,4-DNP-hydrozone, which has the maximum absorbance at 432 nm and its molecular absorption coefficient is 33,600 [M.sup.-1] [cm.sup.-1] (determination limitation of MG is 6 ~ 30 uM) (Gilbert & Brandt, 1975; Wild et al., 2012). In DNP method, because DNP is explosive, it needs special handling and storage. In addition, precipitation of the product MG-bis-2,4-DNP-hydrozone during the reaction limits the reliability of this method, and this method requires more time (45 min) than Gly I method (10 min) (Gilbert & Brandt, 1975; Wild et al., 2012). To overcome these shortcomings, Mustafiz et al. (2010) replaced 1,2-diaminobenzene replace with DNP, and read absorbance at 336 nm after reaction at room temperature for 30 min, which showed better reliability and repeatibility.

NAC method is based on the fast reaction between MG and NAC at room temperature, and yields an easily detectable condensation product, N-[alpha]-acetyl-S-(1-hydroxy-2-oxo-prop-1-yl)cysteine, which shows the maximum absorbance at 288 nm and its molecular absorption coefficient is 249 [M.sup.-1] [cm.sup.-1] (determination limitation of MG is 0.1 ~ 10 mM) (Wild et al., 2012). The NAC method provides an economical and robust assay without the need for the use of hazardous or expensive reagents, it is the most favorable.

Emerging Physiological Functions of MG and Glyoxalase System

MG as Signal Initiator Crosstalk with [Ca.sup.2+], ROS and ABA

As mentioned above, many abiotic stress, including salinity, heavy metal, drought, heat, cold, and high light stresses can induce an increase in endogenous MG in many plant species (Hossain & Fujita, 2009; Yadav et al., 2005a), and this increase appears to be closely associated with stress responses (Yadav et al., 2005a, b). Therefore, MG may act as a signal molecule in plants under stress conditions (Hossain & Fujita, 2009; Kaur et al., 2014a, b; Hoque et al., 2016). Although MG was found to activate several signal transduction pathways in yeasts, information regarding the signalling roles of MG in higher plants is less. In Saccharomyces cerevisiae, MG activates a high osmolarity glycerol-mitogen-activated protein kinase cascade and enhances the influx of extracellular [Ca.sup.2+] into cells through [Ca.sup.2+] channels, stimulating the calcineurin/Crz1-mediated [Ca.sup.2+] signalling pathway and thereby functioning as a signal initiator (Maeta et al., 2005; Hoque et al., 2016). Similarly, in prokaryote E. coli, Campbell and co-workers also identified that MG can directly induce an increase in cytosolic free [Ca.sup.2+] ([[[Ca.sup.2+]].sub.cyt]) in a concentration dependent fashion, and this increase is blocked by lanthanum, a plasma membrane [Ca.sup.2+] channel blocker (Campbell et al., 2007; Hoque et al., 2016), suggesting that [Ca.sup.2+] transient requires the entry of extracellular [Ca.sup.2+] into cells across the plasma membrane.

In addition, in Brassica oleracea, the activity of Gly I in leaf discs was inhibited in the presence of calmodulin inhibitors such as trifluoperazine (TFP), chlorpromazine (CPZ) and compound 48/80 in the cultures, which in turn significantly inhibited callus induction (Bagga et al., 1987; Hoque et al., 2016), indicating that calmodulin may activate Gly I activitiy. Similarly, Gly I, a heterodimeric protein with 56 kDa, from Brassica juncea, is activated by calcium/calmodulin ([Ca.sup.2+]/CaM). In the presence of [Ca.sup.2+] in reaction system Gly I activity significantly increased by 2.6-fold. It showed a [Ca.sup.2+] dependent mobility shift on denaturing gels. Its [Ca.sup.2+] binding was also confirmed by Chelex-100 assay and gel overlays using [sup.45]Ca[Cl.sub.2] (Deswal & Sopory, 1999; Hoque et al., 2016). In addition, Gly I was activated by over 7-fold in the presence of [Ca.sup.2+] (25 uM) and CaM (145 nM) in reaction system and this stimulation was blocked by the CaM antibodies and a CaM inhibitor, TFP (150 uM) (Deswal & Sopory, 1999; Hoque et al., 2016). Also, Gly I binds to a CaM-Sepharose column and was eluted by EGTA, and the eluted protein fractions also showed stimulation by CaM. The stimulation of Gly I activity by CaM was the maximum in the presence of [Mg.sup.2+] and [Ca.sup.2+], and [Mg.sup.2+] alone also showed Gly I activation by CaM (Deswal & Sopory, 1999; Hoque et al., 2016). These results indicate that MG can induce increase in [[[Ca.sup.2+]].sub.cyt] via the entry of extracellular [Ca.sup.2+] into cells across the plasma membrane, which in turn activates the activity of Gly I, ultimately maintains MG homeostasis in cells.

In guard cells, to unravel the roles of MG in cell signalling, Hoque et al. (2012c, d) investigated the regulation of stomatal conductance by exposing plants to various concentrations of MG in the model plant Arabidopsis, the results showed that MG can act as a signalling molecule by inducing stomatal closure without reducing the viability of guard cells at low concentration ([less than or equal to] 1 mM), but high MG concentrations ([greater than or equal to] 1 mM) were cytotoxic. MG at different physiological concentrations (0.01-1 mM) reversibly induced stomatal closure in a concentration-dependent manner, which involved an extracellular oxidative burst and an elevation of [[[Ca.sup.2+]].sub.cyt]. This study clearly demonstrated that MG can induce extracellular ROS production, mediated by salicylhydroxamic acid (SHAM)-sensitive peroxidases (POD), followed by inducing intracellular ROS accumulation and [[[Ca.sup.2+]].sub.cyt] oscillations in guard cells, which in turn lead to stomatal closure in Arabidopsis. In addition, Hoque et al. (2012c) also found that MG can inhibit light-induced stomatal opening in a concentration-dependent manner by inhibiting inward-rectifying potassium channels, MG-induced stomatal closure can be considered a unique signalling role for MG associated with guard cell signal transduction in higher plants. Therefore, induction of stomatal closure is likely to be one of the physiological functions of MG in the stressed plants.

Reactive oxygen species (ROS), mainly [H.sub.2][O.sub.2] and [MATHEMATICAL EXPRESSION NOT REPRODUCIBLE IN ASCII], are second messengers, which play a very important role in plant grow, development and the acquisition of stress tolerance. Many studies found that MG can induce a increase in [H.suib.2][O.sub.2] and [MATHEMATICAL EXPRESSION NOT REPRODUCIBLE IN ASCII] by inhibiting mitochondrial electron transfer chain, complex III and antioxidant enzymes, formating advanced glycation endproducts (AGEs), catalysing the photoreduction of [O.sub.2] at photosystem I (PS I), activating salicylhydroxamic acid-sensitive peroxidases (Chang et al., 2005; Wang et al., 2009; Desai et al., 2010; Hoque et al., 2016), which in turn induced [[[Ca.sup.2+]].sub.cyt], further triggering downstream physiological, biochemical and molecular events involved in stress tolerance (Fig. 2).

Also, as the phytohormone ABA serves as an endogenous messenger in biotic and abiotic stress responses of plants and as a major factor in regulating developmental and physiological processes (Zhu, 2002; Yamaguchi-Shinozaki & Shinozaki, 2006; Fujii et al., 2007; Golldack et al., 2014; Hoque et al., 2016), the involvement of ABA in the response following MG accumulation can be anticipated. To unravel the coordinated role of MG and ABA in MG signalling during stress, Hoque et al. (2012b) investigated the effect of MG on the expression of various stress-responsive genes, including RESPONSIVE TO DEHYDRATION 29A (RD29A), RD29B and RESPONSIVE TO ABA (RABI8), in Arabidopsis wild type plants and in ABA-deficient aba2-2 mutant plants. The study revealed that MG had no effect on transcription of RD29A in either plant type, but significantly increased the transcription of RD29B and RAB18, in a concentration-dependent manner. These findings confirmed that MG can affect the transcription of stress genes in Arabidopsis through an ABA-dependent pathway. However, further investigation is required to clarify the involvement of endogenous ABA in MG signalling. The finding that MG induces gene expression in plants under stress is in agreement with previous research findings establishing a signalling role for MG, through activation of stress genes in yeasts. In Saccharomyces cerevisiae and Schizosaccharomyces pombe, MG functions as a signal initiator for the activation of a stress-activated protein kinase, a mitogen-activated protein kinase and abasic-domain leucine-zipper transcription factor (Aguilera et al., 2005; Zuin et al., 2005; Takatsume et al., 2006; Hoque et al., 2016).

The above studies clearly demonstrate that MG can trigger an increase in other second messengers like [Ca.sup.2+], ROS and ABA, which in turn modulates stress responses in plants. Afterwards, increased [Ca.sup.2+] can activate glyoxalase system which controls MG at low physiological level in plant cells. These studies provide a potential framework for interpreting the physiological roles of MG in biological systems.

Salt Tolerance

Salt stress commonly leads to osmotic stress, ion stress, oxidative stress and membrane damage. To combat with these deleterious effects, plants have evolved a series of complex physiological, biochemical and molecular mechanisms (Zhu, 2002; Ceccoli et al., 2015; Singh & Dhaka, 2016). These strategies include osmotic adjustment (synthesis of osmolytes and compatible solutes); ion homeostasis and compartmentalization; control of ion uptake by roots and transport into leaves; alteration in membrane structure; induction of antioxidative enzymes and antioxidant compounds (Ceccoli et al., 2015; Hoque et al., 2016; Singh & Dhaka, 2016; Tables 1 and 2).

Many investigations show that MG can increase 2- to 6-fold in response to salinity stress. In tobacco BY-2 cells, MG content increased by twofold under 200 mM NaCl stress (Banu et al., 2010). Similarly, in tobacco plants exposed to salt and drought stress, MG level was also found to be increased (Kumar et al., 2013; Ghosh et al., 2014). In mung bean (Vigna radiata L.) seedlings, the salt stress significantly increased the MG, malondialdehyde (MDA), [H.suib.2][O.sub.2] and proline (Pro) content, [MATHEMATICAL EXPRESSION NOT REPRODUCIBLE IN ASCII] generation rate, and GSH and oxidized glutathione (GSSG) content, as well as reduced the ascorbate (AsA) content and the GSH/GSSG ratio. In addition, the salt stress decreased the activities of Gly I, Gly II, mono-dehydroascorbate reductase (MDHAR), dehydroascorbate reductase (DHAR), CAT; but increased the activities of APX, GR,

SOD, GST and GPX. Adversely, Mung bean seedlings treated with NaCl in combination with GSH showed an improved AsA and GSH content, GSH/GSSG ratio, higher activities of Gly I, Gly II, APX, MDHAR, DHAR, GR, SOD, CAT, GPX and GST compared with those treated with NaCl alone. Afterwards, the improved glyoxalase and antioxidant systems by GSH application decreased the MG, MDA and [H.sub.2][O.sub.2] content as well as [MATHEMATICAL EXPRESSION NOT REPRODUCIBLE IN ASCII] generation rate, which in turn improved the tolerance of the mung bean seedlings to the salt stress (Nahar et al., 2015a). Similarly, in mung bean seedlings, application of Pro or glycinebetaine resulted in an increase in GSH content, followed by maintenance of a high GSH redox state and higher activities of Gly I, Gly II GPX, GST and GR involved in the MG and ROS detoxification system. These results suggest that GSH, Pro and glycinebetaine provide a protective action against salt-induced oxidative damage by enhancing MG detoxification and antioxidant defense systems (Hossain & Fujita, 2010).

In tobacco seedlings, the plants overexpressing Gly II improved the resistance to higher level of MG under salinity stress. Adversely, transgenic tobacco underexpressing Gly I showed enhanced accumulation of MG, which in turn resulted in the inhibition of seed germination. Similarly, overexpression of rice Gly II showed higher tolerance to toxic concentrations of MG and NaCl in tobacco seedlings. Compared with non-transgenics, transgenic tobacco seedlings exhibited sustained growth and more favorable ion balance under salt stress conditions (Singla-Pareek et al., 2008).

Interestingly, in rice (Oryza sativa L.) seedlings, salt-tolerant cultivar showed considerably lower level of [H.sub.2][O.sub.2] and higher activity of Gly I and Gly II as compared to sensitive cultivar, indicating the former posses a more efficient antioxidant defense and MG detoxification systems to cope up with salt-induced oxidative stress. As GSH is involved in the AsA-GSH pathway and in the MG detoxification pathway, it may be a point of interaction between antioxidant defense system and MG detoxification system. The results suggest that both AsA and GSH homeostasis, modulated also via glyoxalases, can be considered as biomarkers for salt tolerance in rice (El-Shabrawi et al., 2010).

Similarly, NaCl stress decreased the Gly I, Glyll and GR activities in wheat seedlings, especially at 300 mM, with a concomitant increase in the [H.sub.2][O.sub.2] and MDA levels. Adversely, NO pre-treatment had a synergistic effect; that is, the NO pre-treatment increased the AsA and GSH content and the GSH/GSSG ratio, as well as the activities of Gly I, Gly II, MDHAR, DHAR, GR, GST and GPX in most of the seedlings subjected to salt stress, suggesting that the exogenous application of NO rendered the plants more tolerant to salinity-induced oxidative damage by enhancing their MG detoxification and antioxidant defense systems (Hasanuzzaman et al., 2011).

All of the above investigations show that MG can be rapidly increased in plants under salt stress, which is a general stress response and MG might act as a signal molecule for plants to respond and adapt to salt stress by enhancing MG detoxification and antioxidant defense systems.

Heavy Metal Tolerance

Heavy metal (HM) toxicity is one of the major abiotic stresses leading to hazardous effects in plants. A common consequence of HM toxicity is the excessive accumulation of MG and ROS, both of which can cause lipid peroxidation, protein oxidation, enzymes inactivation and DNA damage. Higher plants have evolved a sophisticated glyoxalase and antioxidant defense systems to scavenge MG and ROS. Due to a central molecule of both the glyoxalase and antioxidant defense systems, GSH is involved in both direct and indirect control of MG and ROS, and their reaction products in plant cells, ultimately improved the resistant ability of plant to HM stress. Recent studies have shown that GSH by itself and its metabolizing enzymes, including Gly I, Gly II, GST, GPX, DHAR and GR, act additively and coordinately for efficient protection against MG- and ROS-induced damage in addition to reducing uptake, detoxification, complexation, chelation and compartmentation of HM (Hossain et al., 2012).

In rice seedlings, cadmium (Cd) treatment increased the MG and ROS levels, while treatment with calcium in combination with Cd reduced Cd uptake and significantly increased the AsA content, the activities of Gly I, Gly II, SOD, CAT, GST, MDHAR and DHAR, followed by reversing overproduced MG and ROS, which in turn reduced Cd toxicity (Rahman et al., 2016). Similarly, under arsenic (As) stress, exogenous application of [Ca.sup.2+] (10 mM) significantly decreased As accumulation, reduced ROS production, increased AsA content, the activities of Gly I, Gly II, MDHAR, DHAR, CAT, GPX and SOD, which in turn restored water loss and plant growth, compared with seedlings exposed to As only (Rahman et al., 2015). These results suggest that [Ca.sup.2+] supplementation improves rice seedlings tolerance to HM by reducing HM uptake, enhancing glyoxalase and antioxidant defense systems.

In transgenic tobacco seedlings with overexpressing Gly I and II, Singla-Pareek et al. (2006) found that the phytochelatins (PC) production was dependent on the presence of HMs. Zinc stress resulted in 280 % increase in PC levels in double transgenic plants (Gly I and II), and about 155 % increase in either of the single-gene transformant (Gly I or II). In addition, the increase in the endogenous levels of GSH also showed a positive correlation with zinc tolerance (Singla-Pareek et al., 2006). These data suggest that an increase in PC induced by HM and maintenance of GSH homeostasis regulated by glyoxalase system, similar to salinity tolerance mechanism, as the possible mechanism for HMs tolerance.

Drought Tolerance

Drought is considered one of the most acute environmental stresses presently affecting agriculture production. As mentioned above, drought stress induced the increase in MG and ROS levels. Thus, detoxification of MG and ROS is one of the major mechanisms underlining drought tolerance in plants. In mung bean (Vigna radiate L. cv. Binamoog1) seedlings, Nahar et al. (2015b) studied the role of exogenous GSH in conferring drought stress tolerance by examining the MG detoxification and antioxidant defence systems and physiological features. The results showed that the activities of Gly I and Gly II increased during drought stress. In contrast to drought stress alone, exogenous GSH enhanced the components of the glyoxalase and antioxidant systems in drought-affected mung bean seedlings, but GSH did not significantly affect AsA, Pro, water content (RWC), leaf succulence and the activities of Gly I and DHAR. Thus, exogenous GSH supplementation significantly enhanced the antioxidant components and successively reduced oxidative damage, up-regulated the glyoxalase system and reduced MG toxicity, which played a significant role in improving the physiological features and drought tolerance.

In Brassicaspecies seedlings, drought stress significantly increased the lipoxygenase activity, the levels of MDA and [H.sub.2][O.sub.2], reduced seedling biomass, chi content and RWC. In contrast, Drought stress increased Pro, oxidized ascorbate (DHA) and GSSG levels. Spraying drought-stressed seedlings with JA increased Gly I, Gly II, DHAR, GR and GPX activities (Alam et al., 2014), indicating that the JA could improve drought tolerance of Brassicaspecies seedlings by enhancing activity of glyoxalase systm and antioxidant defense system.

As discussed above, Gly I is the first enzyme of the glyoxalase system, Mg rapidly increased under stress conditions including drought stress. The transgenic tobacco plants overexpressing Gly I showed significant tolerance to MG and hypertonic solution by assaying detached leaf disc senescence. A comparison of tobacco plants expressing high and low levels of Gly I showed that the tolerance to different osmotic stress was correlated with the degree of Gly I expression (Veena et al., 1999). In addition, transgenic tobacco plants constitutively expressing BvM14-glyoxalase 1 showed significant tolerance to MG and mannitol stresses (Wu et al., 2013). These results suggested that Gly I plays an important role in conferring the tolerance of plants to abiotic stress including drought stress.

It is well known the acquisition of drought tolerance is closely related with the accumulation of osmolytes such as Pro, soluble sugar and betaine, whether MG can induce osmolyte accumulation and its relation to drought tolerance need to be further investigated in the future.

Heat Tolerance

Heat stress is the deleterious effect of high temperature (HT) on seed germination, seedling establishment, plant growth and development and even survival, while heat tolerance is the resistant ability of plants to HT stress by repair and reestablishment of biomembrane, synthesis of heat shock protein, enhancement of MG detoxification and antioxidant defense systems, and the accumulation of osmolytes (Li et al., 2013).

Nahar et al. (2015c) investigated that the 6-day-old mung bean seedlings treated with 0.5 mM GHS for 24 h were exposed to HT stress for 24 and 48 h, and found that heat stress markedly decreased the activities of Gly I, MDHAR, DHAR, GPX and CAT at 24 and 48 h; but increased the activity of Gly II at 48 h. In addition, under HT stress, mung bean seedlings pretreated with exogenous GSH increased Gly I, Gly II, APX, MDHAR, DHAR, GR, GPX, GST and CAT activities; which in turn improved endogenous GSH content and the GSH/GSSG ratio; and lowered GSSG content. Similarly, pretreatment with GSH resulted in better physiological performance, improved glyoxalase and antioxidant systems, and reduced MG and oxidative stress under 24 h of HT stress, compared with that of 48 h. The results suggest that exogenous GSH enhances mung bean seedling tolerance of short-term HT stress by modulating the glyoxalase and antioxidant systems, and by improving physiological adaptation.

In rice seedlings, HT significantly increased lipoxygenase activity, MDA, [H.sub.2][O.sub.2] and Pro contents; decreased fresh weight (FW) and Chl content; significantly increased the activities of Gly I and Gly II. In contrast, foliar spray with spermidine lowered the levels of MDA and [H.sub.2][O.sub.2], and Pro content; but increased the levels of AsA, GSH, FW, Chl, and AsA and GSH redox status (Mostofa et al., 2014). These results show that enhancement of the glyoxalase and antioxidative systems by Spd rendered rice seedlings more tolerant to heat stress, and coinduction of the glyoxalase and antioxidative systems was closely associated with Spd mediated enhanced level of GSH.

As mentioned above, AKR is the major component of MG detoxification in plants, its transcription level was greatly induced by ABA and various stress treatments. The AKR recombinant protein exhibited a high NADPH-dependent catalytic activity to reduce toxic aldehydes including MG and MDA (Turoczy et al., 2011). The transgenic tobacco plants improved resistance to HT stress, and also exhibited higher AKR activity and accumulated less MG in their leaves than the wild type plants under normal and heat stress conditions (Turoczy et al., 2011). These results support the positive role of AKR in heat stress-related reactive aldehyde detoxification pathways and its use for improvement of stress tolerance in plants.

Selenium (Se) plays very important role in minimizing HT-induced damages in plants. The 10-day-old rapeseed seedlings supplemented with Se (25 [micro]M [Na.sub.2] Se[O.sub.4]) enhanced the activities of Gly I, Gly II, MDHAR, DHAR, GR, GPX and CAT, the contents of Pro, AsA and GSH, as well as the GSH/GSSG ratio; which in turn significantly decreased the MDA, [H.sub.2][O.sub.2] and MG content as compared to heat-treated seedlings without Se supplementation (Hasanuzzaman et al., 2014)), indicating that exogenous Se application confers heat stress tolerance in rapeseed seedlings by upregulating the MG detoxification and antioxidant defense systems.

Cold Tolerance

Similar to other abiotic stresses, cold stress also lead to excessive accumulation of MG and ROS (Li et al., 2014). In Camellia sinensis (L.) O. Kuntze, Kumar and Yadav (2009) found that cold stress enhanced MG and lipid peroxidation levels in tea bud (youngest topmost leaf), while exogenously applied Pro and betaine to tea bud can alleviate the decrease in Gly I and Gly II and the increase in MG level under cold stress. In addition, Pro exposure enhanced GST and GR activities, while betaine increased only GR activity during cold stress. This investigation, therefore, suggest that Pro and betaine might provide protection to cold stress in tea by regulating MG and lipid peroxidation formation as well as by activating or protecting some of glyoxalase and antioxidant pathway enzymes. Interestingly, proteomics protocol also identified that Gly I and Gly II participated in cold tolerance in arabidopsis (Goulas et al., 2006), rice (Lee et al., 2009) and onion (Chen et al., 2013).

Stomatal Movement

As mentioned above, MG may act as a signaling molecule in plants during stresses. Hoque et al. (2012c) found that MG can induce production of ROS and [[[Ca.sup.2+]].sub.cyt] oscillations, leading to stomatal closure. The MG-induced stomatal closure and ROS production were completely inhibited by a peroxidase inhibitor SHAM. Furthermore, the MG-elicited [[[Ca.sup.2+]].sub.cyt] oscillations were significantly suppressed by SHAM, but not by the atrbohD atrbohF mutation. In addition, further experiments found that MG also can inhibit light-induced stomatal opening in a concentration-dependent manner by inhibiting inward-rectifying potassium channels (Hoque et al., 2012d). These results suggest that intrinsic metabolite MG can induce stomatal closure in Arabidopsis by triggering [[[Ca.sup.2+]].sub.cyt] oscillations induced by ROS originated from SHAM-sensitive peroxidases, and by inhibiting inward-rectifying potassium channels. In addition, Mg can induce stomatal closure, which indicated that MG might be involved in the acquisition of drought tolerance in plants, but this hypothesis needs to be uncovered in the future.

Seed Germination

Successful seed germination and seedling establishment are of great importance for agriculture and forest production due to their sensitive to adverse environments (Li et al., 2012). In Arabidopsis, Hoque et al. (2012b) examined the effect of MG on seed germination, root elongation, chlorosis and stress-responsive gene expression using an ABA-deficient mutant aba2-2. The results showed that, in the wild type, 0.1 mM MG did not affect germination, but delayed root elongation, whereas 1.0 mM MG inhibited germination and root elongation, and induced chlorosis. In addition, MG increased transcription levels of RD29B and RABI8 in a dose-dependent manner, but did not affect RD29A transcription level. Adversely, in the aba2-2 mutant, MG- inhibited seed germination at 1.0 mm and 10.0 mm and MG-delayed root elongation at 0.1 mm MG were mitigated, although there was no significant difference in chlorosis between the wild type and mutant. Moreover, the aba2-2 mutation impaired MG-induced RD29B and RAB18 gene expression. These observations suggest that MG not only directly inhibits germination and root elongation, but also indirectly modulates these processes via endogenous ABA in Arabidopsis.

Cell Division and Organ Differentiation

In addition to abiotic stress tolerance, Gly I has long been considered as an enzyme generally associated with cell proliferation in animal, microbial and plant systems. Paulus et al. (1993), using a strictly auxin-dependent soybean (Glycine max L. Merr.) cell suspension, studied the correlation of auxin-dependent cell proliferation and Gly I activity, the results showed that Gly I activity can be modulated during the proliferation cycle, with a maximal activity between day 2 and day 4 of culture growth. After starving the culture of auxins for three subsequent periods, Gly I activity and cell growth could be re-initiated with auxin, and Gly I activity reached its maximum 1 day before cell number was at a maximum. In addition, in Solanum nigrum and Daucus carota, Roy et al. (2004) also found that MG could completely replace kinetin to initiate differentiation of plantlets from calluses. Moreover, the effect of MG was more pronounced compared to that of kinetin and the optimum concentration for MG had been determined to be 0.5 mM. Parallel with the differentiation of calluses to plantlets, the Chl contents increased, whereas the endogenous level of MG remained unchanged. In addition, this remarkable effect of MG in plant differentiation had been found out to be specific, because some related compounds such as pyruvate and D-lactate could not replace the requirement for MG in the differentiation process. Also, the activity of Gly I decreased with differentiation, the endogenous level of GSH showed an initial decrease followed by an increase. These results appear that the effect of kinetin and MG are similar in nature. Similarly, Ray et al. (2013) evaluated the influence of MG on organogenesis and regeneration of tobacco (Nicotiana tabacum L.) plants from callus in media containing glycine or succinate. The best improvement in shoot proliferation and shoot length was obtained in the medium supplemented with 0.1 mM MG and 0.5 mM glycine or 0.25 mM succinate. The histological also studies showed vigorous development of corm like structures and shoot organogenesis from callus tissues cultured in MG supplemented media (Ray et al., 2013).

Conclusions and Future Prospects

Similar to other signal molecules like [Ca.sup.2+], ROS, NO and hydrogen sulfide ([H.sub.2] S), MG shows dual role, that is, as cytotoxin at high concentration and signal molecule at low concentration in plants. Recent years, signal molecule function of MG has gained much attention in plant biology, accumulating evidence uncovered that MG participated in many phyiological processes, including signal crosstalk with other second messengers like [Ca.sup.2+], ROS and ABA; stress tolerance like salt, HM, drought, heat and cold tolerance; stomatal movement; seed germination; as well as cell division and organ differentiation. In additon, the omics approaches have illustrated that detoxification system of MG, Gly I and Gly II, as stress markers involved in the acquisition of salt (Sun et al., 2010), drought (Le et al., 2012), heat (Zhang et al., 2013) and cold (Goulas et al., 2006; Lee et al., 2009; Chen et al., 2013) tolerance in tomato, soybean, radish, arabidopsis, rice and onion plants. Although research on MG and glyoxalase system has greatly made progress in plants especially in abiotic stress conditions, the following opening questions need to be further answered in the future: (1) using proteomics and metabolomics protocols to understand MG metabolism and elucidate signalling roles of MG in various plant species, which would be worthwhile research to help improve multiple abiotic stress tolerance; (2) using sensitive intracellular imaging to precisely quantify MG in plant cell, tissue, organ and other subcellular compartments; (3) a thorough investigation of the interaction between MG and [Ca.sup.2+], ROS, NO, [H.sub.2] S, plant hormones, osmolyte, heat shock protein and transcription factors, as well as components of the glyoxalase system in different subcellular compartments could reveal more significant regulatory roles of the glyoxalase system in plants; (4) potential target molecules of MG as a potential signal molecule.

Abbreviations

ABA        Abscisic acid
ADH        Aldehyde dehydrogenase
AGEs       Advanced glycation end products
AKR        Aldo-keto reductase
ALR        Aldose/aldehyde reductase
AMO        Acetol monooxygenase
APX        Ascorbate peroxidase
AsA        Ascorbic acid
CaM        Calmodulin
CAT        Catalase
CPZ        Chlorpromazine
DHA        Dehydroascorbic acid
DHAP       Dihydroxyacetone phosphate
DHAR       Dehydroascorbate reductase
DNP        2,4-dinitrophenylhydrazine
Gly        I/II Glyoxalase I/II
GPX        Glutathione peroxidase
G3P        Glyceraldehyde-3 -phosphate
GR         Glutathione reductase
GSH        Glutathione
GSSG       Oxidized glutathione
GST        Glutathione S-transferase
HM         Heavy metal
HTA        Hemithioacetal
L-/D-LDH   L-/D-lactate dehydrogenase
MDA        Malondialdehyde
MDHAR      Mono-dehydroascorbate reductase
MG         Methylglyoxal
MGDH       Methylglyoxal dehydrogenase
MGR        Methylglyoxal reductase
MGS        Methylglyoxal synthase
Mit        Mitochondia
NAC        N-acetyl-L-cysteine
NO         Nitric oxide
PC         Phytochaletins
POD        Peroxidase
Pro        Proline
ROS        Reactive oxygen species
SHAM       Salicylhydroxamic acid
SLG        S-D-lactoylglutahione
SOD        Superoxide dismutase
SSAO       Semicarbazide-sensitive amine oxidase
TCA        Tricarboxylic acid cycle
TFP        Trifluoperazine
TP         Triosephosphate
TPI        Triosephosphate isomerase


DOI 10.1007/s12229-016-9167-9

Acknowledgments This research is supported by National Natural Science Foundation of China (31360057) and Doctor Startup Foundation of Yunnan Normal University China (01200205020503099). We appreciate the reviewers and editors for their exceptionally helpful comments about the manuscript.

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Zhong-Guang Li (1,2,3,4)

(1) School of Life Sciences, Yunnan Normal University, Kunming (650500), People's Republic of China

(2) Engineering Research Center of Sustainable Development and Utilization of Biomass Energy, Ministry of Education, Kunming (650500), People's Republic of China

(3) Key Laboratory of Biomass Energy and Environmental Biotechnology, Yunnan Province, Yunnan Normal University, Kunming (650500), People's Republic of China

(4) Author for Correspondence; e-mail: zhongguang_li@163.com

Published online: 2 May 2016

Table 1 Reaction catalyzed by major ROS-scavenging antioxidant enzymes

Enzymatic antioxidants       Reactions catalyzed

Superoxide dismutase (SOD)   [O.sub.2] x - +[O.sub.2] x - +2H+
EC 1.15.1.1                  [right arrow] 2[H.sub.2][O.sub.2]
                             + [O.sub.2]

Catalase (CAT) EC 1.11.1.6   [H.sub.2][O.sub.2] [right arrow]
                             [H.sub.2]O+ 1/2 [O.sub.2]

Ascorbate peroxidase (APX)   [H.sub.2][O.sub.2] + AA
EC 1.11.1.11                 [right arrow] 2[H.sub.2]O + DHA

Guaicol peroxidase (GPX)     [H.sub.2][O.sub.2] + GSH
EC 1.11.1.7                  [right arrow] [H.sub.2]O + GSSG

Monodehydroascorbate         MDHA + NAD(P)H [right arrow] AA +
reductase (MDHAR) EC         [NAD(PP).sup.+]
1.6.5.4

Dehydroascorbate             DHA + 2GSH [right arrow] AA + GSSG
reductase (DHAR) 1.8.5.1

Glutathione reductase (GR)   GSSG + NAD(P)H [right arrow]
                             2GSH + [NAD(P).sup.+]

Source: Gill & Tuteja, 2010

Table 2 Plant genetic transformation for salinity tolerance
and specific expressed trait conferring salt tolerance

Gene                Gene source       Transgenic
                                      plant

TPS1-TPS2           Yeast             Alfalfa

BADH                E. coli           Tobacco

IMT1                M. crystalinum    Tobacco

P5CS                V aconitifolia    Tobacco

Apo-Inv             S. cereviseae     Tobacco

TSP1                S. cereviseae     Tobacco

Ni107               N. tabacum        Tobacco

GS                  O. sativa         Rice

MnSOD               S. cereviseae     Rice

APX                 Arabidopsis       Tobacco

GST                 Tomato            Rice

HAL1                S. cereviseae     Arabidopsis

AtNHX1              A. thaliana       Arabidopsis

CaN                 S. cereviseae     Rice

Na+/H+              Arabidopsis       Arabidopsis
antiporter (SOS1)

Na+/H+              Salicornia        Rice
antiporter (SOD2)   brachiata

Na+/H+              Arabidopsis       Buckwheat
antiporter (NHX)

mtID                E. coli           Rice

Myo-inositol O-     M. crystallinum   Wheat
methyltransferase

P5CS                Moth bean         Wheat

DREB1A              A. thaliana       Arabidopsis

C1PK                Arabidopsis       Barley

MAPK                Chickpea          Tobacco

AP2/ERF             Cotton            Wheat

MYB                 Soybean           Tomato

NAC                 Tomato            Rice

Gene                Functions/Response          Reference
                    of transgenic plant

TPS1-TPS2           Increased compatible        Suarez et al.
                    solute accumulation         (2009)

BADH                Betaine synthesis           Holmstrom et al.
                                                (2000)

IMT1                D-ononitol synthesis        She vele va et al.
                                                (1997)

P5CS                Proline synthesis           Kishor et al.
                                                (1995)

Apo-Inv             Sucrose synthesis           Fukushima et al.
                                                (2001)

TSP1                Trehalose synthase          Serrano et al.
                                                (1999)

Ni107               GSSG synthesis              Roxas et al. (1997)

GS                  Glutamine synthesis         Hoshida et al.
                                                (2000)

MnSOD               Reduction of O-2            Tanaka et al.
                    content                     (1999)

APX                 Maintenance of              Roy et al. (2014)
                    photosynthetic efficiency

GST                 Maintenance of growth       Roy et al. (2014)

HAL1                K/Na homeostasis            Gisbert et al.
                                                (2000)

AtNHX1              Na vacuolar sequestration   Zhang et al. (2001)

CaN                 Improve Ca+2 signaling      Pardo et al. (1998)

Na+/H+              Altered shoot and root      Roy et al. (2014)
antiporter (SOS1)   accumulation of Na+ and
                    K

Na+/H+              Improved biomass            Roy et al. (2014)
antiporter (SOD2)   production

Na+/H+              Improved shoot and root     Roy et al. (2014)
antiporter (NHX)    biomass production

mtID                Increased growth            Roy et al. (2014)

Myo-inositol O-     Maintenance of              Roy et al. (2014)
methyltransferase   photosynthetic efficiency

P5CS                Maintenance of              Roy et al. (2014)
                    photosynthetic efficiency

DREB1A              Transcription factor        Kasuga et al.
                                                (1999)

C1PK                Altered Na+, K+ and         Roy et al. (2014)
                    C1_accumulation

MAPK                Improved biomass            Roy et al. (2014)
                    production

AP2/ERF             Improved biomass            Roy et al. (2014)

MYB                 Improved chlorophyll        Roy et al. (2014)
                    retention

NAC                 Altered Na+accumulation     Roy et al. (2014)
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