Glyoxalase Centennial: 100 Years of Glyoxalase Research and Emergence of Dicarbonyl Stress

Glyoxalases and stress tolerance in plants Charanpreet Kaur*, Ajit Ghosh*, Ashwani Pareek†, Sudhir K. Sopory* and Sneh L. Singla-Pareek*1 *International Centre for Genetic Engineering and Biotechnology, Aruna Asaf Ali Marg, New Delhi 110067, India †School of Life Sciences, Jawaharlal Nehru University, New Delhi, India

Biochemical Society Transactions

Abstract The glyoxalase pathway is required for detoxification of cytotoxic metabolite MG (methylglyoxal) that would otherwise increase to lethal concentrations under adverse environmental conditions. Since its discovery 100 years ago, several roles have been assigned to glyoxalases, but, in plants, their involvement in stress response and tolerance is the most widely accepted role. The plant glyoxalases have emerged as multigene family and this expansion is considered to be important from the perspective of maintaining a robust defence machinery in these sessile species. Glyoxalases are known to be differentially regulated under stress conditions and their overexpression in plants confers tolerance to multiple abiotic stresses. In the present article, we review the importance of glyoxalases in plants, discussing possible roles with emphasis on involvement of the glyoxalase pathway in plant stress tolerance.

Methylglyoxal and glyoxalase system The cytotoxic nature of MG (methylglyoxal) in living systems is well known where it is associated with several pathological conditions in animals [1] and inhibition of growth and development in plants [2]. MG induces oxidative stress in cells either directly through increased generation of ROS (reactive oxygen species) or indirectly by forming AGEs (advanced glycation end-products) with protein and nucleotide moieties [3]. Since it accumulates at higher concentrations under adverse conditions, living systems, including both plants and animals, have evolved several detoxification mechanisms to combat the so-called ‘MG stress’ developed under such conditions. The major pathway for detoxification of MG is through a two-step enzymecatalysed glyoxalase system, comprising GlyI (glyoxalase I, also abbreviated Glo1) and GlyII (glyoxalase II, also abbreviated Glo2) enzymes that uses hemithioacetal formed from the spontaneous combination of MG and glutathione (GSH) as a substrate to yield D-lactate, thereby regenerating GSH in the process. Other enzymes for MG detoxification include aldo–keto/aldehyde reductases and dehydrogenases. Glyoxalases were discovered in 1913, but their presence in the plant kingdom was reported in the late 20th Century. The detection of glyoxalase activity in Douglas fir needles by Smits and Johnson probably marks the beginning of plant glyoxalase research [4]. Thereafter, glyoxalase activity has been reported in various plant species, suggesting their ubiquitous presence. These enzymes are believed to be key players in the plant stress response, and their overexpression confers significant tolerance to multiple stresses such as salinity and heavy metal stress [5,6]. The glyoxalase pathway

Key words: abiotic stress, glyoxalase pathway, methylglyoxal (MG), multigene family, plant, stress tolerance. Abbreviations: AGE, advanced glycation end-product; Gly, glyoxalase; MG, methylglyoxal; ROS, reactive oxygen species; TcGLX1, Thlaspi caerulescens GlyI. 1 To whom correspondence should be addressed (email [email protected]).

Biochem. Soc. Trans. (2014) 42, 485–490; doi:10.1042/BST20130242

in plants operates in both cytosol and mitochondria, with GlyI enzymes being cytosolic since their substrate MG is produced majorly as a by-product of the cytosol-based glycolytic pathway. However, peroxisomal localization of GlyI has also been reported in Arabidopsis [7]. On the other hand, GlyII proteins are present in both cytosol and mitochondria. Earlier immunolocalization studies in tomato have determined the distribution of GlyI proteins in all cell types with preferential accumulation in phloem sieve elements [8]. In Brassica, it is present in seeds, roots, hypocotyl, cotyledon and different flower parts [9]. Biochemically, glyoxalases have been well characterized in animal and microbial systems, but little is known at present about the biochemistry of plant glyoxalases where they have been studied more from a physiological perspective. In general, glyoxalases are metalloenzymes, requiring divalent metals for activation [10]. On the basis of the metal ion requirement, GlyI proteins have been grouped as Zn(II)dependent or non-Zn(II)-dependent enzymes, with the latter needing Ni(II) or Co(II) for activation. The first category was believed earlier to contain enzymes of mainly eukaryotic origin and the second class consisted of GlyI proteins from prokaryotes, but, with the discovery of newer GlyI candidates, several exceptions to the above classification have emerged. For example, Pseudomonas aeruginosa contains enzymes from both the activation classes [11]. Similarly, GlyII is also a metalloenzyme, belonging to the superfamily of metallo-β-lactamases, with a conserved motif that is able to bind up to two metal ions in their active sites, generally zinc and iron [12].

Proposed biological roles of glyoxalases in plants Although detoxification of MG constitutes in particular a very important role for the glyoxalase enzymes, its  C The

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evolutionarily conserved nature and ubiquitous presence certainly suggests a profound significance of glyoxalases in biological systems, besides MG metabolism. Since their discovery, glyoxalases have been assigned various roles, from being linked as mainstream players in glycolysis to being associated with cell division and microtubule assembly [13,14]. Glyoxalase research has seen many twists regarding the physiological significance of these proteins, which is still an open question as none of the proposed theories could completely justify the fundamental importance of these proteins. However, the regulatory role of glyoxalases in cell division had been studied by various groups which over the course of time has been overshadowed in view of the emerging role of glyoxalases in plant stress tolerance.

Role of glyoxalases in cell division The promine/retine theory initially proposed by Szent¨ Gyorgyi with MG as retine and GlyI as promine, suggested a crucial regulatory function of glyoxalases in cell division [13]. Similarly, in plants, the role of glyoxalases in cell division had been established where rapidly proliferating cell lines have been repeatedly shown to exhibit increased GlyI activity. For instance, GlyI activity was found to be in good correlation with mitotic index in Pisum sativum roots [15] and also in Datura callus culture, where addition of mitotic inhibitors such as vinblastine to the growth medium was found to inhibit GlyI activity, but spermidine, an inducer of cell growth, enhanced GlyI activity [16]. Additionally, calmodulin inhibitors and LiCl that inhibit cell proliferation, reduced GlyI activity in Brassica oleracea [17], whereas phytohormone and blue light treatments that stimulate cell proliferation in callus cultures of Amaranthus increased GlyI activity [18,19]. Similar findings were reported in coconut palm [20], jute [21] and soya bean [22]. Although increased GlyI activity has been firmly linked to cell division, no functional role can be assigned to glyoxalases owing to a lack of experimental evidence on the causal relationship between enzyme activity and cell division.

Role of glyoxalases in plant stress response A firm link between glyoxalases and stress tolerance has been established in plants as a result of extensive work carried out by various research groups (Figure 1). Initial studies in tomato opened vistas for a prospective role of glyoxalases in stress physiology where 2–3-fold up-regulation in GlyI transcripts was observed in roots, stems and leaves of tomato plants treated with NaCl, mannitol and ABA (abscisic acid) treatment [8]. Thereafter, transgenic tobacco plants overexpressing Brassica GlyI revealed the potential of these genes in conferring enhanced tolerance to MG and high salt conditions [23]. Increased GlyI expression on exposure to salinity stress correlated well with levels of stress tolerance. Similar results were obtained by overexpressing the same GLYI gene in Vigna mungo, imparting salinity tolerance to transgenic plants [24]. Overexpression of rice GLYII gene in tobacco and even rice had also been shown to impart improved tolerance to high MG and NaCl concentrations  C The

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[5,25]. The transgenic tobacco plants were able to grow, flower and set normal viable seeds under continuous salinity stress conditions. Furthermore, transgenic rice plants sustained growth and maintained a more favourable ion balance compared with untransformed plants contributing to salinity tolerance. Consistent with these observations, expression of the same GLYII gene in Brassica juncea conferred improved salinity stress tolerance by delaying senescence [26]. Transgenic plants overexpressing the entire glyoxalase pathway (Brassica GLYI + rice GLYII) had also been raised and show a better response than either of the singlegene-transformed lines and also the untransformed plants under salinity and heavy metal stress conditions [5,6]. Keeping MG levels in check together with maintaining higher levels of reduced GSH and antioxidant enzymes sustains the redox balance in the system, thereby conferring tolerance under stress [27]. Likewise, overexpression of a similar construct harbouring glyoxalase pathway genes in tomato has led to salt-tolerant transgenic tomato plants which exhibit reduced oxidative stress and thus better stress tolerance [28]. In addition, increased phytochelatin production observed in transgenic plants after zinc treatment promotes efficient heavy metal detoxification and thereby contributes to observed tolerance of transgenic plants in zinc-spiked soil [6]. However, in hyperaccumulator plant Thlaspi caerulescens, no correlation between TcGLX1 (T. caerulescens GlyI) expression and the degrees of zinc tolerance could be observed. Neither was any phenotype visible in Arabidopsis thaliana T-DNA (transferred DNA) insertion line for the closest A. thaliana homologue of TcGLX1 [29]. It is likely that overexpression of both GlyI and GlyII together contribute to the zinc tolerance observed. However, expression of wheat GlyI in tobacco plants imparted zinc tolerance to transgenic tobacco plants [30]. Thus the genetic manipulation of plants via overexpression of glyoxalases can successfully contribute to improving stress tolerance (summarized in Table 1). In addition to the genetic engineering approach, transcriptome and proteome studies have also evaluated the role of glyoxalases in stress. For instance, GLYI had been identified as a dehydration-induced gene in foliage grass Sporobolus stapfianus [31]. GLYI transcripts are also induced by white light, salinity, MG and heavy metal treatment in pumpkin seedlings [32]. In wheat, GlyI levels are up-regulated in response to Fusarium graminearium infection in addition to NaCl and ZnCl2 treatments [30]. Also, transcriptome studies for investigation of plant responses to xenobiotics, senescence and chalkiness formation in grain-filling caryopses have led to the identification of GLYI and GLYII genes being induced under such conditions. Several comparative transcriptome studies have also shed light on significance of glyoxalases in stress response. Analysis of salt-tolerance traits in sensitive and tolerant rice and tomato varieties have revealed stressinduced higher expression of GLYI genes in tolerant varieties [33,34]. Assessment of stress proteomes of various species has also advanced our understanding of the role of glyoxalases in stress

Glyoxalase Centennial: 100 Years of Glyoxalase Research and Emergence of Dicarbonyl Stress

Figure 1 Timeline depicting important developments in plant glyoxalase research

tolerance. In response to diverse stimuli such as osmotic, dehydration, extreme temperature and heavy metal stresses and hormones such as methyl jasmonate and salicylic acid treatments, glyoxalase proteins are accumulated. Moreover, glyoxalase activity is also induced under these conditions as reported in various species such as onion bulbs and pumpkin seedlings, providing further evidence of the role of glyoxalases [32,35]. Various studies undertaken to determine the regulatory role of different stimuli such as selenium, nitric oxide, salicylic acid, osmolytes such as proline and betaine, and extreme

temperature treatments before or together with different stress conditions have also shown an increase in glyoxalase activity probably as a marker for stress tolerance in plants (reviewed in [36]). Also through phosphoproteomics, GlyI proteins have been identified as targets of SnRK2 (sucrose non-fermenting-1-related protein kinase 2) kinases that are known to be activated by abiotic stress [37]. Apart from environmental cues, glyoxalases can impart tolerance in response to infection by various pathogens. The proteomic comparison of maize kernel embryo of aflatoxin-resistant and -susceptible genotypes has led to the  C The

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Table 1 Genetic engineering of glyoxalase genes for enhancing stress tolerance Gene

Host plant


Brassica GLYI


Salinity stress tolerance


Brassica GLYI Brassica GLYI

Vigna mungo Arabidopsis

Alleviation of salt stress Provides salt tolerance

[24] [49]

Brassica GLYI Wheat GLYI Sugar beet GLYI

Rice Tobacco Tobacco

Confers salinity tolerance Imparts zinc tolerance to transgenic plants Shows significant tolerance to MG, salt, mannitol and H2 O2

[50] [30] [48]


Tobacco Rice Brassica

Enhances salinity tolerance Tolerance against MG and salt Enhances salinity tolerance

[5] [25] [26]

Brassica GLYI + rice GLYII Brassica GLYI + Pennisetum GLYII

Tobacco Tomato

Enhances salinity tolerance and set viable seeds under zinc-spiked soil Confers salt-tolerance

[5,6,27] [28]

identification of GlyI protein being up-regulated in resistant embryos, consistent with the observed constitutive high GlyI activity in resistant lines [38]. GlyI is believed to play an important role in controlling MG levels inside kernels which otherwise induces aflatoxin production. Similarly, GlyI expression is induced in rice in response to brown planthopper infestation [39] and in Brassica upon infection with Sclerotinia sclerotiorum [40]. Thus these findings convincingly suggest the vital importance of the glyoxalase detoxification pathway in abiotic and biotic stress responses.

Glyoxalases in glycation stress MG is a potent and highly reactive glycation agent, modifying amino groups of proteins or DNA molecules forming protein and nucleotide AGEs. AGEs are dysfunctional molecular modifications that distort protein structure and biological activity and also disrupt genomic integrity leading to genotoxicity. However, MG-derived AGEs need to be cleared from the system, for which no enzymatic deglycation process has been yet detected. Hence it is justified to assign anti-glycation defence functions to glyoxalases which keep causal MG levels in check. In humans, increased accumulation of AGE-modified proteins has implications in disease development and progression, as observed in diabetes and its associated vascular complications, renal failure, cirrhosis and aging [1]. However, in plants, assessment of anti-glycation defence by glyoxalases is largely incomplete. But stress tolerance in glyoxalase-overexpressing transgenic plants has been scored mainly on their ability to delay senescence when compared with untransformed plants [5,23]. This probably works by keeping elevated MG levels in check which would increase to toxic concentrations under different stresses [41] and can form AGEs, contributing to stress-mediated senescence mechanisms in plants. Transcriptome studies in Arabidopsis have also led to identification of the GLYII gene being up-regulated 8-fold during leaf senescence. It is likely that glyoxalases have a protective role towards the proteome against glycation damage in plants as well.  C The

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Evolution of plant glyoxalases as a multigene family and emergence of novel forms Glyoxalases are known to be ubiquitously present in living organisms from prokaryotes to eukaryotes. They are present as single-copy genes in microbial and animal systems except for the bacterial species P. aeruginosa, which encodes three GlyI proteins [11]. Investigation of domain architecture of bacterial and human GlyI enzymes reveals their presence as single-domain proteins that form homodimers in native form. In contrast, two-domain GlyI proteins have been reported in plants such as wheat [30], Brassica oleracea, Sporobolus stapfianus [42] and rice (A. Mustafiz, A. Ghosh, A.K. Tripathi, C. Kaur, A. Pareek, S.K. Sopory, S.L. SinglaPareek, unpublished work), similarly to yeast GlyI. Analysis of rice and Arabidopsis genomes has revealed the presence of glyoxalases as a multigene family in these species [43], which has been extended further to other plants, revealing a universal expansion of glyoxalase genes as a multimember family in plants (C. Kaur, A. Vishnoi, T. Ariyadasa, A. Bhattacharya, S.L. Singla-Pareek and S.K. Sopory, unpublished work). In rice, a total of 19 GlyI proteins encoded by 11 genes and four GlyII proteins encoded by three genes have been reported. In Arabidopsis, 22 GlyI proteins are encoded by 11 genes and nine GlyII proteins by five genes. The presence of multiple forms of these genes suggests a role of fundamental importance in plant systems. Expression profile of the members of the rice and Arabidopsis glyoxalase families using publicly available databases (massively parallel signature sequencing and microarray) suggests differential response of this gene family in response to various stresses [43]. The expression pattern of these genes also varies in different tissues and during various stages of vegetative and reproductive development. It is quite probable that, in order to overcome the limitations imposed by the sessile nature of plants, more robust defence mechanisms have evolved and the emergence of multiple forms of these glyoxalases is a strategy adopted for better stress adaptation in plants. Assessment of catalytic activity of plant glyoxalases has revealed functional divergence in this multigene family where

Glyoxalase Centennial: 100 Years of Glyoxalase Research and Emergence of Dicarbonyl Stress

Figure 2 Scheme depicting the involvement of the glyoxalase pathway in plant stress response During stress, an increase in ROS impairs the redox balance of the cell. MG levels also rise, further inducing ROS generation through the formation of AGEs, resulting in ROS-mediated cellular injury and death. Increase in glyoxalase activity either through overexpression or otherwise naturally under stress conditions restores redox homoeostasis by lowering MG levels and regenerating GSH back into the system, thereby decreasing ROS production which leads to improved stress tolerance. HTA, hemithioacetal; SLG, S-d-lactoylglutathione.

few members have evolved structurally to adopt different roles. For instance, two Arabidopsis GLYII genes, AtGlx21 and AtGlx2-3 lack GlyII activity, but instead possess β-lactamase and sulfur dioxygenase activities respectively [44,45]. GlyI activity is also absent from some GlyI proteins in rice where their true functions remain unknown. Additionally, recent findings have suggested the presence of novel glyoxalases in Arabidopsis which constitute single enzymes capable of converting MG into D-lactate directly [46], such as bacterial GlyIII and human DJ-1 proteins. In humans, these proteins have implications in the onset of Parkinson’s disease [47]. Taken together, the glyoxalase pathway in plants plays an important role in stress response, either directly through MG detoxification or indirectly by reducing oxidative stress, thereby imparting stress tolerance (illustrated in Figure 2). Moreover, the emergence of multiple forms of these genes in plants indicates a role much more important than that currently known. We believe that detailed studies are needed to decipher the exact functional significance of these genes in plants.

Acknowledgements We apologize to colleagues whose primary work was not cited owing to space limitations.

Funding S.L.S.-P. acknowledges the grants received from the International Centre for Genetic Engineering and Biotechnology (ICGEB) and the Department of Biotechnology, Government of India.

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Glyoxalases and stress tolerance in plants.

The glyoxalase pathway is required for detoxification of cytotoxic metabolite MG (methylglyoxal) that would otherwise increase to lethal concentration...
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