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Methylglyoxal: An Emerging Signaling Molecule in Plant Abiotic Stress Responses and Tolerance

Identifieur interne : 001383 ( Pmc/Corpus ); précédent : 001382; suivant : 001384

Methylglyoxal: An Emerging Signaling Molecule in Plant Abiotic Stress Responses and Tolerance

Auteurs : Tahsina S. Hoque ; Mohammad A. Hossain ; Mohammad G. Mostofa ; David J. Burritt ; Masayuki Fujita ; Lam-Son P. Tran

Source :

RBID : PMC:5020096

Abstract

The oxygenated short aldehyde methylglyoxal (MG) is produced in plants as a by-product of a number of metabolic reactions, including elimination of phosphate groups from glycolysis intermediates dihydroxyacetone phosphate and glyceraldehyde 3-phosphate. MG is mostly detoxified by the combined actions of the enzymes glyoxalase I and glyoxalase II that together with glutathione make up the glyoxalase system. Under normal growth conditions, basal levels of MG remain low in plants; however, when plants are exposed to abiotic stress, MG can accumulate to much higher levels. Stress-induced MG functions as a toxic molecule, inhibiting different developmental processes, including seed germination, photosynthesis and root growth, whereas MG, at low levels, acts as an important signaling molecule, involved in regulating diverse events, such as cell proliferation and survival, control of the redox status of cells, and many other aspects of general metabolism and cellular homeostases. MG can modulate plant stress responses by regulating stomatal opening and closure, the production of reactive oxygen species, cytosolic calcium ion concentrations, the activation of inward rectifying potassium channels and the expression of many stress-responsive genes. MG appears to play important roles in signal transduction by transmitting and amplifying cellular signals and functions that promote adaptation of plants growing under adverse environmental conditions. Thus, MG is now considered as a potential biochemical marker for plant abiotic stress tolerance, and is receiving considerable attention by the scientific community. In this review, we will summarize recent findings regarding MG metabolism in plants under abiotic stress, and evaluate the concept of MG signaling. In addition, we will demonstrate the importance of giving consideration to MG metabolism and the glyoxalase system, when investigating plant adaptation and responses to various environmental stresses.


Url:
DOI: 10.3389/fpls.2016.01341
PubMed: 27679640
PubMed Central: 5020096

Links to Exploration step

PMC:5020096

Le document en format XML

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</TEI>
<pmc article-type="review-article">
<pmc-dir>properties open_access</pmc-dir>
<front>
<journal-meta>
<journal-id journal-id-type="nlm-ta">Front Plant Sci</journal-id>
<journal-id journal-id-type="iso-abbrev">Front Plant Sci</journal-id>
<journal-id journal-id-type="publisher-id">Front. Plant Sci.</journal-id>
<journal-title-group>
<journal-title>Frontiers in Plant Science</journal-title>
</journal-title-group>
<issn pub-type="epub">1664-462X</issn>
<publisher>
<publisher-name>Frontiers Media S.A.</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">27679640</article-id>
<article-id pub-id-type="pmc">5020096</article-id>
<article-id pub-id-type="doi">10.3389/fpls.2016.01341</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Plant Science</subject>
<subj-group>
<subject>Review</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>Methylglyoxal: An Emerging Signaling Molecule in Plant Abiotic Stress Responses and Tolerance</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Hoque</surname>
<given-names>Tahsina S.</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/373573/overview"></uri>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Hossain</surname>
<given-names>Mohammad A.</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/191808/overview"></uri>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Mostofa</surname>
<given-names>Mohammad G.</given-names>
</name>
<xref ref-type="aff" rid="aff3">
<sup>3</sup>
</xref>
<xref ref-type="author-notes" rid="fn001">
<sup>*</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/241745/overview"></uri>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Burritt</surname>
<given-names>David J.</given-names>
</name>
<xref ref-type="aff" rid="aff4">
<sup>4</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/220674/overview"></uri>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Fujita</surname>
<given-names>Masayuki</given-names>
</name>
<xref ref-type="aff" rid="aff5">
<sup>5</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/191807/overview"></uri>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Tran</surname>
<given-names>Lam-Son P.</given-names>
</name>
<xref ref-type="aff" rid="aff6">
<sup>6</sup>
</xref>
<xref ref-type="aff" rid="aff7">
<sup>7</sup>
</xref>
<xref ref-type="author-notes" rid="fn001">
<sup>*</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/64534/overview"></uri>
</contrib>
</contrib-group>
<aff id="aff1">
<sup>1</sup>
<institution>Department of Soil Science, Bangladesh Agricultural University</institution>
<country>Mymensingh, Bangladesh</country>
</aff>
<aff id="aff2">
<sup>2</sup>
<institution>Department of Genetics and Plant Breeding, Bangladesh Agricultural University</institution>
<country>Mymensingh, Bangladesh</country>
</aff>
<aff id="aff3">
<sup>3</sup>
<institution>Department of Biochemistry and Molecular Biology, Bangabandhu Sheikh Mujibur Rahman Agricultural University</institution>
<country>Gazipur, Bangladesh</country>
</aff>
<aff id="aff4">
<sup>4</sup>
<institution>Department of Botany, University of Otago</institution>
<country>Dunedin, New Zealand</country>
</aff>
<aff id="aff5">
<sup>5</sup>
<institution>Laboratory of Plant Stress Responses, Department of Applied Biological Science, Faculty of Agriculture, Kagawa University</institution>
<country>Kagawa, Japan</country>
</aff>
<aff id="aff6">
<sup>6</sup>
<institution>Plant Abiotic Stress Research Group & Faculty of Applied Sciences, Ton Duc Thang University</institution>
<country>Ho Chi Minh City, Vietnam</country>
</aff>
<aff id="aff7">
<sup>7</sup>
<institution>Signaling Pathway Research Unit, RIKEN Center for Sustainable Resource Science</institution>
<country>Yokohama, Japan</country>
</aff>
<author-notes>
<fn fn-type="edited-by">
<p>Edited by:
<italic>Susana Araújo, Universidade Nova de Lisboa, Portugal</italic>
</p>
</fn>
<fn fn-type="edited-by">
<p>Reviewed by:
<italic>Veronica Graciela Maurino, Heinrich Heine University Düsseldorf, Germany; Abu Hena Mostafa Kamal, University of Texas at Arlington, USA</italic>
</p>
</fn>
<corresp id="fn001">*Correspondence:
<italic>Mohammad G. Mostofa,
<email xlink:type="simple">mostofa@bsmrau.edu.bd</email>
Lam-Son P. Tran,
<email xlink:type="simple">sontran@tdt.edu.vn</email>
;
<email xlink:type="simple">son.tran@riken.jp</email>
</italic>
</corresp>
<fn fn-type="other" id="fn002">
<p>This article was submitted to Crop Science and Horticulture, a section of the journal Frontiers in Plant Science</p>
</fn>
</author-notes>
<pub-date pub-type="epub">
<day>13</day>
<month>9</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="collection">
<year>2016</year>
</pub-date>
<volume>7</volume>
<elocation-id>1341</elocation-id>
<history>
<date date-type="received">
<day>14</day>
<month>6</month>
<year>2016</year>
</date>
<date date-type="accepted">
<day>19</day>
<month>8</month>
<year>2016</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright © 2016 Hoque, Hossain, Mostofa, Burritt, Fujita and Tran.</copyright-statement>
<copyright-year>2016</copyright-year>
<copyright-holder>Hoque, Hossain, Mostofa, Burritt, Fujita and Tran</copyright-holder>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/">
<license-p>This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.</license-p>
</license>
</permissions>
<abstract>
<p>The oxygenated short aldehyde methylglyoxal (MG) is produced in plants as a by-product of a number of metabolic reactions, including elimination of phosphate groups from glycolysis intermediates dihydroxyacetone phosphate and glyceraldehyde 3-phosphate. MG is mostly detoxified by the combined actions of the enzymes glyoxalase I and glyoxalase II that together with glutathione make up the glyoxalase system. Under normal growth conditions, basal levels of MG remain low in plants; however, when plants are exposed to abiotic stress, MG can accumulate to much higher levels. Stress-induced MG functions as a toxic molecule, inhibiting different developmental processes, including seed germination, photosynthesis and root growth, whereas MG, at low levels, acts as an important signaling molecule, involved in regulating diverse events, such as cell proliferation and survival, control of the redox status of cells, and many other aspects of general metabolism and cellular homeostases. MG can modulate plant stress responses by regulating stomatal opening and closure, the production of reactive oxygen species, cytosolic calcium ion concentrations, the activation of inward rectifying potassium channels and the expression of many stress-responsive genes. MG appears to play important roles in signal transduction by transmitting and amplifying cellular signals and functions that promote adaptation of plants growing under adverse environmental conditions. Thus, MG is now considered as a potential biochemical marker for plant abiotic stress tolerance, and is receiving considerable attention by the scientific community. In this review, we will summarize recent findings regarding MG metabolism in plants under abiotic stress, and evaluate the concept of MG signaling. In addition, we will demonstrate the importance of giving consideration to MG metabolism and the glyoxalase system, when investigating plant adaptation and responses to various environmental stresses.</p>
</abstract>
<kwd-group>
<kwd>abiotic stress</kwd>
<kwd>glyoxalases</kwd>
<kwd>methylglyoxal</kwd>
<kwd>reactive oxygen species</kwd>
<kwd>signaling crosstalk</kwd>
<kwd>stress tolerance mechanism</kwd>
</kwd-group>
<counts>
<fig-count count="2"></fig-count>
<table-count count="2"></table-count>
<equation-count count="0"></equation-count>
<ref-count count="120"></ref-count>
<page-count count="11"></page-count>
<word-count count="0"></word-count>
</counts>
</article-meta>
</front>
<body>
<sec>
<title>Introduction</title>
<p>Most plants live in environments where they are constantly exposed to one or combinations of various abiotic stressors, such as extreme temperatures, salinity, drought, and excessive light, which can severely limit plant growth and development. For many important crop plants, exposure to stress(es) ultimately results in a considerable reduction in potential yields (
<xref rid="B5" ref-type="bibr">Atkinson and Urwin, 2012</xref>
). The interaction between abiotic stressors and plants is complex, eliciting multiple morphological, physiological, biochemical and molecular changes that can ultimately result in varying degrees of stress adaptation, enabling some plants to grow and develop under environmentally induced stress. Because of the number of metabolic pathways involved, and the compexity of their regulation, it is often difficult for researchers to identify the major regulatory components involved in the abiotic stress responses of plants (
<xref rid="B96" ref-type="bibr">Sharma et al., 2013</xref>
). Plants subjected to stress often produce toxic aldehydes (
<xref rid="B30" ref-type="bibr">Hoque et al., 2012a</xref>
,
<xref rid="B31" ref-type="bibr">b</xref>
,
<xref rid="B32" ref-type="bibr">c</xref>
;
<xref rid="B28" ref-type="bibr">Hoque M.A. et al., 2012</xref>
;
<xref rid="B59" ref-type="bibr">Mano, 2012</xref>
), of which methylglyoxal (CH
<sub>3</sub>
COCHO; MG) is the most ubiquitous. The reactive alpha-ketoaldehyde MG is cytotoxic to plant cells at high cellular concentrations, but it may act as an important signaling molecule at low concentrations (
<xref rid="B115" ref-type="bibr">Yadav et al., 2005a</xref>
,
<xref rid="B116" ref-type="bibr">b</xref>
;
<xref rid="B99" ref-type="bibr">Singla-Pareek et al., 2006</xref>
;
<xref rid="B35" ref-type="bibr">Hossain et al., 2009</xref>
;
<xref rid="B44" ref-type="bibr">Kaur et al., 2015a</xref>
,
<xref rid="B46" ref-type="bibr">b</xref>
). MG is produced in plant cells as a result of glycolysis, and its celluar concentrations are maintained at very low levels in the absence of any environmental stress (
<xref rid="B46" ref-type="bibr">Kaur et al., 2015b</xref>
). However, in response to abiotic stressors celluar concentrations of MG rapidly increase (
<xref rid="B115" ref-type="bibr">Yadav et al., 2005a</xref>
,
<xref rid="B116" ref-type="bibr">b</xref>
). Accumulation of MG can disrupt the normal functioning of cells, leading to alterations in metabolic behavior and, in some instances, the death of plants (
<xref rid="B37" ref-type="bibr">Hossain et al., 2011</xref>
). The glyoxalase pathway has evolved to enable plants, and other organisms, to withstand the detrimental effects of MG overproduction, by limiting the accumulation of MG in the cells under stress (
<xref rid="B99" ref-type="bibr">Singla-Pareek et al., 2006</xref>
,
<xref rid="B100" ref-type="bibr">2008</xref>
;
<xref rid="B4" ref-type="bibr">Alvarez Viveros et al., 2013</xref>
). MG and the glyoxalases are now considered as potential markers for evaluating plant abiotic stress tolerance (
<xref rid="B35" ref-type="bibr">Hossain et al., 2009</xref>
;
<xref rid="B43" ref-type="bibr">Kaur et al., 2014a</xref>
,
<xref rid="B45" ref-type="bibr">b</xref>
,
<xref rid="B47" ref-type="bibr">c</xref>
;
<xref rid="B71" ref-type="bibr">Nahar et al., 2015a</xref>
). Although significant progress has been made in investigating MG metabolism and toxicity in plants, the role of MG as a signaling molecule in stress responses and the acquisition of stress tolerance in plants still remain unclear. In this review, we will summarize recent findings regarding MG metabolism and the glyoxalase system in plants under abiotic stress, evaluate the concept of MG signaling, and discuss the importance of MG metabolism in modulating plant abiotic stress responses and tolerance.</p>
</sec>
<sec>
<title>MG Synthesis in Plants</title>
<p>In plant cells, the cytosol, chloroplasts and mitochondria are all considered to be potential sites of MG production. However, the specific rate and sites of MG production vary depending upon the cell or tissue type, the plant organ (e.g. leaves or roots), and the physiological state of the whole plant (
<xref rid="B44" ref-type="bibr">Kaur et al., 2015a</xref>
,
<xref rid="B46" ref-type="bibr">b</xref>
). Spontaneous production of MG occurs as a consequence of glycolysis, in metabolically active plant cells, from the reaction of the triose sugar phosphates glyceraldehyde-3-phosphate (G3P) and dihydroxyacetone phosphate (DHAP), both of which are photosynthetic intermediates (
<xref rid="B115" ref-type="bibr">Yadav et al., 2005a</xref>
;
<xref rid="B101" ref-type="bibr">Takagi et al., 2014</xref>
;
<xref rid="B44" ref-type="bibr">Kaur et al., 2015a</xref>
,
<xref rid="B46" ref-type="bibr">b</xref>
). This reaction is considered to be the principal route for MG formation under normal physiological conditions (
<bold>Figure
<xref ref-type="fig" rid="F1">1</xref>
</bold>
). Triose phosphates are unstable metabolites and show a high tendency to release an α-carbonyl proton, producing an enediolate phosphate intermediate that has a relatively low energy barrier for the elimination of phosphate groups (
<xref rid="B86" ref-type="bibr">Richard, 1984</xref>
). Thus, MG is formed by the deprotonation followed by the spontaneous β-elimination of the phosphate groups of triose phosphates (
<xref rid="B87" ref-type="bibr">Richard, 1993</xref>
). The enzymatic formation of MG occurs through the triose phosphate isomerase (TPI) that hydrolyzes G3P and DHAP, and removes phosphate to yield MG (
<xref rid="B80" ref-type="bibr">Phillips and Thornalley, 1993</xref>
). MG may also be formed by Amadori rearrangement during production of a Schiff base, which involves the reaction of the aldehyde groups of sugars with free amino acids or the amino acids of proteins (
<xref rid="B110" ref-type="bibr">Vistoli et al., 2013</xref>
). Other possible sources for MG formation include the auto-oxidation of surgars, as well as the metabolism of acetone and aminoacetone (
<xref rid="B41" ref-type="bibr">Kalapos, 1999</xref>
), although there is little evidence that these routes occur in plants.</p>
<fig id="F1" position="float">
<label>FIGURE 1</label>
<caption>
<p>
<bold>A diagrammatic representation of methylglyoxal (MG) synthesis and detoxification in plants (modified from
<xref rid="B50" ref-type="bibr">Ko et al., 2005</xref>
;
<xref rid="B37" ref-type="bibr">Hossain et al., 2011</xref>
).</bold>
MG is primarily produced as a by-product of carbohydrate metabolism, with small amount produced during protein and lipid metabolism. Cytotoxic MG is efficiently degraded to form
<sc>D</sc>
-lactate by the action of the enzymes Gly I and Gly II, with the help of GSH. In addition, GSH-independent Gly III is able to convert MG to
<sc>D</sc>
-lactate.
<sc>D</sc>
-lactate dehydrogenase finally converts
<sc>D</sc>
-lactate into pyruvate, which enters TCA cycle via acetyl CoA. The broken line separates the synthesis and detoxification pathways of MG. For further discussion, see the text. Abbreviations are defined in the text.</p>
</caption>
<graphic xlink:href="fpls-07-01341-g001"></graphic>
</fig>
</sec>
<sec>
<title>MG Detoxification in Plants via Glyoxalase and Other Metabolic Pathways</title>
<p>Methylglyoxal detoxification involves the conversion of MG to less toxic molecules, thus limiting its detrimental effects. The major route for MG detoxification in plants is the glyoxalase pathway, whose prescence was demonstrated in plants over 20 years ago (
<xref rid="B76" ref-type="bibr">Norton et al., 1990</xref>
;
<xref rid="B58" ref-type="bibr">Maiti et al., 1997</xref>
). In plant cells, the glyoxalase pathway is present in the cytosol and organelles, with high levels of glyoxalase enzyme activity found in chloroplasts and mitochondria (
<xref rid="B117" ref-type="bibr">Yadav et al., 2008</xref>
;
<xref rid="B82" ref-type="bibr">Rabbani and Thornalley, 2012</xref>
). There are two main enzymes associated with the glyoxalase pathway; glyoxalase I (Gly I; lactoylglutathione lyase; EC 4.4.1.5) and glyoxalase II (Gly II; hydroxyacylglutathione hydrolase; EC 3.1.2.6). These enzymes function in tandem to transform MG, and other 2-oxoaldehydes, to 2-hydroxyacids with the release of glutathione (GSH) (
<xref rid="B103" ref-type="bibr">Thornalley, 1990</xref>
). The detoxification of MG involves two irreversible reactions catalyzed by glyoxalases. The first step involves the reaction of MG with GSH, resulting in the formation of hemithioacetal that is then converted to
<italic>S</italic>
-D-lactoylglutathione (SLG) in a reaction catalyzed by Gly I. In the second step, which is catalyzed by Gly II, GSH is regenerated and D-lactate is formed by the hydrolysis of SLG (
<bold>Figure
<xref ref-type="fig" rid="F1">1</xref>
</bold>
).
<sc>D</sc>
-lactate, which is also considered a toxic compound if overaccumulated, is converted into pyruvate by
<sc>D</sc>
-lactate dehydrogenase (
<xref rid="B13" ref-type="bibr">Engqvist et al., 2009</xref>
;
<xref rid="B113" ref-type="bibr">Wienstroer et al., 2012</xref>
). Pyruvate, the major catabolic product of MG, can enter the tricarboxylic acid (TCA) cycle via acetyl CoA (
<bold>Figure
<xref ref-type="fig" rid="F1">1</xref>
</bold>
). The availability of cellular GSH is an important factor for MG detoxification via the glyoxalase system as the lack of GSH restricts hemithioacetal formation, resulting in MG accumulation (
<xref rid="B37" ref-type="bibr">Hossain et al., 2011</xref>
). Recently, a novel glyoxalase enzyme, named glyoxalase III (Gly III), was detected in plants, providing a shorter route for MG detoxification (
<xref rid="B16" ref-type="bibr">Ghosh et al., 2016</xref>
). Gly III contains a DJ-1/PfpI domain, and the presence of this domain has been used to confirm the existence of Gly III-like proteins in various plant species. Conventional glyoxalases (Gly I and Gly II) detoxify MG by converting it to D-lactate, with the help of GSH, but Gly III is able to irreversibly convert MG to
<sc>D</sc>
-lactate in a single step, without the need for GSH (
<bold>Figure
<xref ref-type="fig" rid="F1">1</xref>
</bold>
).</p>
<p>In addition to the glyoxalase system, several other pathways contribute to the detoxification of MG in plants. Other enzymes, including NADPH-dependent reductases, such as the aldo-keto reductases and aldehyde/aldose reductases, involved in detoxifying reactive carbonyls (
<xref rid="B118" ref-type="bibr">Yamauchi et al., 2010</xref>
), can reduce MG to the corresponding alcohol (
<xref rid="B97" ref-type="bibr">Simpson et al., 2009</xref>
;
<xref rid="B74" ref-type="bibr">Narawongsanont et al., 2012</xref>
). Another pathway is the irreversible oxidation of reactive aldehydes, including MG, to their corresponding carboxylic acids, which is catalyzed by aldehyde dehydrogenases (
<xref rid="B49" ref-type="bibr">Kirch et al., 2005</xref>
). However, the glyoxalase system is the most efficient MG detoxification system in plants under normal physiological conditions (
<xref rid="B16" ref-type="bibr">Ghosh et al., 2016</xref>
), and this pathway is very important for plants under stress (
<xref rid="B99" ref-type="bibr">Singla-Pareek et al., 2006</xref>
;
<xref rid="B4" ref-type="bibr">Alvarez Viveros et al., 2013</xref>
).</p>
</sec>
<sec>
<title>MG Levels in Plants Under Stressful Conditions</title>
<p>Under normal metabolic conditions, plants usually maintain a lower level (30-75 μM) of MG (
<xref rid="B115" ref-type="bibr">Yadav et al., 2005a</xref>
;
<xref rid="B35" ref-type="bibr">Hossain et al., 2009</xref>
); however, an abrupt increase was observed in respone to abiotic stresses (
<xref rid="B115" ref-type="bibr">Yadav et al., 2005a</xref>
;
<xref rid="B35" ref-type="bibr">Hossain et al., 2009</xref>
;
<xref rid="B63" ref-type="bibr">Mostofa et al., 2015a</xref>
,
<xref rid="B64" ref-type="bibr">b</xref>
). Salt stress-induced inceases in MG levels were found in various plant species, including pumpkin (
<italic>Cucurbita maxima</italic>
L.) by 77%, tobacco (
<italic>Nicotiana tabacum</italic>
L., cv. BY-2) by 67% and potato (
<italic>Solanum tuberosum</italic>
L. cv. Taedong Valley) by 50%, compared with the respective controls (
<xref rid="B35" ref-type="bibr">Hossain et al., 2009</xref>
;
<xref rid="B6" ref-type="bibr">Banu et al., 2010</xref>
;
<xref rid="B107" ref-type="bibr">Upadhyaya et al., 2011</xref>
;
<xref rid="B17" ref-type="bibr">Ghosh et al., 2014</xref>
). Increased MG levels were also found in mung bean (
<italic>Vigna radiata</italic>
L.),
<italic>Lepidium sativum</italic>
and rice plants in response to drought (90–107%), and excessive Cd (60–260%) and Cu (106–156%) stresses, respectively, when compared with control counterparts (
<xref rid="B72" ref-type="bibr">Nahar et al., 2015b</xref>
;
<xref rid="B64" ref-type="bibr">Mostofa et al., 2015b</xref>
,
<xref rid="B65" ref-type="bibr">c</xref>
). These findings indicate that the increase in MG levels is a common response of plants to a variety of abiotic stressors, and that stress-induced MG could act as a generic signal molecule for plants under adverse environmental conditions.</p>
</sec>
<sec>
<title>MG Toxicity in Plant Cells During Plant Growth and Development</title>
<p>In plant cells, MG accumulation has been shown to correlate with increased levels of intracellular oxidative stress, due to the enhanced reactive oxygen species (ROS) production (
<xref rid="B57" ref-type="bibr">Maeta et al., 2005</xref>
;
<xref rid="B42" ref-type="bibr">Kalapos, 2008</xref>
). MG accumulation may indirectly result in increased ROS production by decreasing available GSH levels and by impairing the function of antioxidant enzymes in plants under oxidative stress. In addition, MG can function as a Hill oxidant and catalyze the photoreduction of O
<sub>2</sub>
to superoxide (
<inline-graphic xlink:href="fpls-07-01341-i001.jpg"></inline-graphic>
) in photosystem I (PSI) (
<xref rid="B89" ref-type="bibr">Saito et al., 2011</xref>
). The production of
<inline-graphic xlink:href="fpls-07-01341-i001.jpg"></inline-graphic>
is deleterious as it can cause oxidative damage to cellular components.</p>
<p>Methylglyoxal is an α,β-dicarbonyl compound that can act both as a genotoxic and a glycation agent (
<xref rid="B83" ref-type="bibr">Rabbani and Thornalley, 2014</xref>
). MG has two functional groups; a ketone group and an aldehyde group, the latter being more reactive than the former (
<xref rid="B53" ref-type="bibr">Leoncini, 1979</xref>
). The dicarbonyl group within MG can readily react with the amine groups of proteins and nucleic acids, including DNA and RNA. The accumulation of MG is often called dicarbonyl stress, which has been implicated as a cause of tissue damage and aging (
<xref rid="B83" ref-type="bibr">Rabbani and Thornalley, 2014</xref>
). MG reacts with the amino acids lysine, cysteine and arginine producing glycated proteins, often referred to as advanced glycation end products (AGEs) (
<xref rid="B2" ref-type="bibr">Ahmed and Thornalley, 2007</xref>
), which can cause inactivation of proteins and oxidative damage to key cellular components (
<xref rid="B104" ref-type="bibr">Thornalley, 2006</xref>
). AGEs and dicarbonyl compounds, including MG, often accumulate in plant leaves upon exposure to high light or elevated CO
<sub>2</sub>
concentrations (
<xref rid="B81" ref-type="bibr">Qiu et al., 2008</xref>
;
<xref rid="B7" ref-type="bibr">Bechtold et al., 2009</xref>
). Thus, it appears that the increase in sugar accumulation and changes in the metabolic flux of sugars, which occur at high CO
<sub>2</sub>
concentrations, promote the production of MG and other reactive carbonyls, resulting in the accumulation of AGEs. In summary, excessive MG accumulation in plant cells under stress can inhibit cell proliferations, and cause the inactivation and/or degradation of proteins, inactivation of antioxidant defenses, leading to disruption of many cellular functions (
<xref rid="B27" ref-type="bibr">Hoque et al., 2010</xref>
;
<xref rid="B28" ref-type="bibr">Hoque M.A. et al., 2012</xref>
).</p>
<fig id="F2" position="float">
<label>FIGURE 2</label>
<caption>
<p>
<bold>A schematic model depicting the signaling roles of MG in plant during abiotic stresses (modified from
<xref rid="B29" ref-type="bibr">Hoque et al., 2015</xref>
;
<xref rid="B44" ref-type="bibr">Kaur et al., 2015a</xref>
).</bold>
Stress-induced MG participates in signal transduction by altering the expression of a number of genes, such as those encoding protein kinases and transcription factors (TFs), triggering various responses, including changes in general metabolism and ion/metabolite transport, stress and defense responses, as well as protein degradation. For further discussion, see the text. Abbreviations are defined in the text.</p>
</caption>
<graphic xlink:href="fpls-07-01341-g002"></graphic>
</fig>
<p>Indeed, MG showed toxicity to photosynthesis in the chloroplasts of spinach (
<italic>Spinacia oleracea</italic>
L.) (
<xref rid="B60" ref-type="bibr">Mano et al., 2009</xref>
), and the accumulation of MG in the
<italic>pdtpi</italic>
mutant, which lacks the plastid isoform of TPI, exhibited greatly reduced growth and increased chlorosis (
<xref rid="B9" ref-type="bibr">Chen and Thelen, 2010</xref>
).
<xref rid="B115" ref-type="bibr">Yadav et al. (2005a)</xref>
reported that accumulation of MG, as a result of salt stress, directly and adversely influenced plant developmental processes, such as seed germination and seedling growth, in tobacco plants. Similarly,
<xref rid="B13" ref-type="bibr">Engqvist et al. (2009)</xref>
found that
<italic>Arabidopsi</italic>
s plants grown on MS medium supplemented with MG (0.1 or 1 mM MG) exhibited a significant reduction in shoot and root growth. Later, the same group reported a dose-dependent decrease in root and shoot growth of
<italic>Arabidopsi</italic>
s, tomato and tobacco plants grown on MS medium containing 1 mM MG (
<xref rid="B113" ref-type="bibr">Wienstroer et al., 2012</xref>
). Furthermore,
<xref rid="B31" ref-type="bibr">Hoque et al. (2012b)</xref>
examined the inhibitory effects of MG on growth and development in
<italic>Arabidopsis</italic>
and suggested that 1 mM MG is toxic enough to significantly inhibit seed germination and root elongation in seedlings. However, concentrations lower than 0.1 mM MG had no influence on seed germination, but did reduced the rate of root elongation. In addition, concentrations of 1 mM MG or higher resulted in seedling chlorosis within 4 days of treatment. Recently,
<xref rid="B44" ref-type="bibr">Kaur et al. (2015a)</xref>
also reported that MG exposure caused a significant growth reduction in rice seedlings (
<italic>Oryza sativa</italic>
cv. IR4), with acute effects on root elongation in a concentration-dependent manner. The above findings highlight the growth inhibitory effects of MG on plants, and indicate that the MG levels causing toxic effects to plants vary depending on plant species, exposure time and perhaps age of plants.</p>
</sec>
<sec>
<title>MG As A Signaling Molecule in Plants Under Stress</title>
<sec>
<title>MG-Induced ROS Regulation</title>
<p>In plants, ROS are primarily formed at low levels as metabolic by-products of photosynthesis and respiration in organelles through enzymatic reactions that take place in plant cell walls and the apoplastic space in response to pathogens (
<xref rid="B1" ref-type="bibr">Ahmad et al., 2010</xref>
;
<xref rid="B95" ref-type="bibr">Sharma et al., 2012</xref>
). In plants, the rates of ROS production dramatically increase under abiotic or biotic stress (
<xref rid="B95" ref-type="bibr">Sharma et al., 2012</xref>
), leading to the onset of oxidative stress. The enzymes involved directly in ROS production include plasmamembrane NAD(P)H oxidases, cell-wall peroxidases (
<xref rid="B18" ref-type="bibr">Grant et al., 2000</xref>
;
<xref rid="B106" ref-type="bibr">Torres et al., 2002</xref>
), apoplastic amine oxidases, oxalate oxidases and heme-containing peroxidases (
<xref rid="B94" ref-type="bibr">Sewelam et al., 2016</xref>
). Recently,
<xref rid="B43" ref-type="bibr">Kaur et al. (2014a)</xref>
reported that when MG levels in plant cells increased due to stress, ROS generation increased directly due to the presence of MG or indirectly due to the formation of AGEs. It has been reported that application of exogenous MG to tobacco plants, at concentrations between 0.5 and 10 mM, reduced the activities of antioxidant enzymes, such as glutathione
<italic>S</italic>
-transferase (GST) and ascorbate peroxidase (APX), leading to oxidative stress (
<xref rid="B27" ref-type="bibr">Hoque et al., 2010</xref>
;
<xref rid="B28" ref-type="bibr">Hoque M.A. et al., 2012</xref>
). In addition,
<xref rid="B89" ref-type="bibr">Saito et al. (2011)</xref>
also demonstrated that MG induced
<inline-graphic xlink:href="fpls-07-01341-i001.jpg"></inline-graphic>
production in chloroplasts during photosynthesis. MG, at concentrations to 1 mM, has also been shown to cause a reversible induction of
<inline-graphic xlink:href="fpls-07-01341-i001.jpg"></inline-graphic>
production in leaves of both wild-type
<italic>Arabidopsis</italic>
and NAD(P)H oxidase knock-out
<italic>atrbohD atrbohF</italic>
mutant plants, suggesting that salicylhydroxamic acid (SHAM)-sensitive peroxidases could be involved in this oxidative burst.</p>
</sec>
<sec>
<title>Regulation of Stomatal Conductance Involving Cytosolic Ca
<sup>2+</sup>
Oscillation and Inward K
<sub>in</sub>
Channel Activation</title>
<p>Plants appear to have well-developed systems to sense and react to diverse environmental stimuli (
<xref rid="B39" ref-type="bibr">Jia and Zhang, 2008</xref>
). Stomata, which control CO
<sub>2</sub>
uptake and minimize transpirational water loss, are capable of responding to various environmental stimuli, e.g., light levels, CO
<sub>2</sub>
levels, temperature and humidity, and are often used as a model system to investigate cell-to-cell signaling in plants (
<xref rid="B93" ref-type="bibr">Schroeder et al., 2001</xref>
;
<xref rid="B48" ref-type="bibr">Kim et al., 2010</xref>
). Stomatal closure is an adaptive mechanism in plants, enabling them to survive in adverse environments (
<xref rid="B77" ref-type="bibr">Osakabe et al., 2014</xref>
). Stomatal closure is associated with increased concentrations of cytosolic calcium, [Ca
<sup>2+</sup>
]
<sub>cyt</sub>
, with oscillations in [Ca
<sup>2+</sup>
]
<sub>cyt</sub>
occuring in guard cells in response to a diverse range of environmental stimuli (
<xref rid="B78" ref-type="bibr">Pei et al., 2000</xref>
;
<xref rid="B61" ref-type="bibr">Mori et al., 2006</xref>
;
<xref rid="B120" ref-type="bibr">Young et al., 2006</xref>
).</p>
<p>To investigate the mode of action of MG in stomatal guard cell signal transduction,
<xref rid="B30" ref-type="bibr">Hoque et al. (2012a</xref>
,
<xref rid="B32" ref-type="bibr">c</xref>
) investigated stomatal movement in
<italic>Arabidopsis</italic>
treated with different concentrations of MG. They found that at concentrations of MG up to 1 mM, MG behaved like a signal molecule as it induced stomatal closure, in a dose-dependant and reversible manner, without reducing the viability of guard cells. The induction of stomatal closure by MG involved an extracellular peroxidase-mediated oxidative burst and [Ca
<sup>2+</sup>
]
<sub>cyt</sub>
oscillations (
<bold>Figure
<xref ref-type="fig" rid="F2">2</xref>
</bold>
). However, this MG-controlled induction did not require endogenous abscisic acid (ABA) nor endogenous methyl jasmonate (MeJA), and was not affected by deficiency in NAD(P)H oxidases. Thus, the studies of
<xref rid="B30" ref-type="bibr">Hoque et al. (2012a</xref>
,
<xref rid="B32" ref-type="bibr">c</xref>
) provided evidence that MG can induce stomatal closure, which is an important adaptive response of plants to environmentally induced stress.</p>
<p>Regulation of stomatal opening can greatly influence plant productivity and stress management (
<xref rid="B11" ref-type="bibr">Dietrich et al., 2001</xref>
), with inhibition of light-induced stomatal opening likely being occurred in plants under stress. The uptake of K
<sup>+</sup>
into the guard cells accompanies light-induced stomatal opening, and inward-rectifying potassium (K
<sub>in</sub>
) channels play important roles in regulating K
<sup>+</sup>
uptake (
<xref rid="B93" ref-type="bibr">Schroeder et al., 2001</xref>
). The K
<sup>+</sup>
transporter of
<italic>Arabidopsis thaliana KAT1</italic>
gene is expressed in stomatal guard cells, and plants with a dominant negative mutation in this gene have reduction of K
<sub>in</sub>
channel currents, which results in a reduced ability in regulating K
<sup>+</sup>
ion flow and suppression of light-induced stomatal opening (
<xref rid="B52" ref-type="bibr">Kwak et al., 2001</xref>
). It has also been demonstrated that MG, in a concentration-dependent manner, can interfere with light-induced stomatal opening in
<italic>Arabidopsis</italic>
, and that this interference involves inhibition of K
<sub>in</sub>
channel currents in guard cells, partially due to suppression of KAT1 channel activity (
<xref rid="B30" ref-type="bibr">Hoque et al., 2012a</xref>
,
<xref rid="B32" ref-type="bibr">c</xref>
) (
<bold>Figure
<xref ref-type="fig" rid="F2">2</xref>
</bold>
). According to
<xref rid="B91" ref-type="bibr">Sato et al. (2009</xref>
,
<xref rid="B90" ref-type="bibr">2010</xref>
), protein kinase C (PKC) and stress-activated protein kinase SnRK2.6 (Snf1-related protein kinase 2.6) phosphorylate the C-terminal regions of KAT1, which modulates the activity of KAT1 channel. It is possible that MG can restrain the K
<sub>in</sub>
channel activity by modifying C-terminal regions of KAT1, as well as other components, which inhibits stomatal opening.</p>
</sec>
<sec>
<title>Expression of Stress-Responsive Genes in Co-ordination with ABA</title>
<p>Abiotic stresses, including drought, salinity and extreme temperatures, can induce the expression of many defense-related genes in plants. Stress-induced genes are important for plant survival as they encode proteins with both direct and indirect protective functions, and proteins that play important roles in signal transduction and gene regulation, both of which are important for coordinated stress responses (
<xref rid="B56" ref-type="bibr">Ma et al., 2012</xref>
;
<xref rid="B102" ref-type="bibr">Thao and Tran, 2012</xref>
;
<xref rid="B119" ref-type="bibr">Yoshida et al., 2015</xref>
). The plant hormone ABA is an important signal molecule for plant growth and development, as well as various physiological processes, including abiotic stress responses (
<xref rid="B14" ref-type="bibr">Fujita et al., 2011</xref>
,
<xref rid="B15" ref-type="bibr">2013</xref>
;
<xref rid="B77" ref-type="bibr">Osakabe et al., 2014</xref>
). Many stress-inducible genes exhibit ABA-dependent gene expression patterns (
<xref rid="B20" ref-type="bibr">Hadiarto and Tran, 2011</xref>
;
<xref rid="B105" ref-type="bibr">Todaka et al., 2015</xref>
).</p>
<p>As ABA plays an important role in the integration of stress signals and downstream regulation of stress responses in plants (
<xref rid="B38" ref-type="bibr">Hubbard et al., 2010</xref>
;
<xref rid="B112" ref-type="bibr">Weiner et al., 2010</xref>
), it is possible that ABA could be involved in the responses that occur following MG accumulation.
<xref rid="B31" ref-type="bibr">Hoque et al. (2012b)</xref>
investigated the expression of the stress- and ABA-responsive genes
<italic>RD29B</italic>
and
<italic>RAB18</italic>
in
<italic>Arabidopsis</italic>
wild-type and ABA-deficient (
<italic>aba2-2</italic>
) mutant plants in response to MG treatment. They reported that MG significantly enhanced transcriptional levels of
<italic>RD29B</italic>
and
<italic>RAB18</italic>
in WT seedlings in a dose-dependent manner. In contrast, the transcription of neither
<italic>RD29B</italic>
nor
<italic>RAB18</italic>
was affected by MG in
<italic>aba2-2</italic>
mutant plants, indicating that ABA is involved in MG-induced up-regulation of
<italic>RD29B</italic>
and
<italic>RAB18</italic>
genes. This finding suggests that stress-induced MG may regulate stress-responsive genes in ABA-dependent pathway for plant adaptation to stress.</p>
</sec>
<sec>
<title>MG-Responsive Signal Transduction Pathways</title>
<p>Plants have developed effective detection mechanisms and efficient signal transduction pathways to enable them to respond to various environmental stresses (
<xref rid="B79" ref-type="bibr">Petrov et al., 2015</xref>
). These pathways often involve multiple genes/proteins, operating in a coordinated manner, to regulate the expression patterns of the key genes, enabling plants to respond to a diverse range of external stimuli (
<xref rid="B20" ref-type="bibr">Hadiarto and Tran, 2011</xref>
;
<xref rid="B19" ref-type="bibr">Gururani et al., 2015</xref>
;
<xref rid="B54" ref-type="bibr">Li and Tran, 2015</xref>
).
<xref rid="B44" ref-type="bibr">Kaur et al. (2015a)</xref>
used microarray analysis to investigate gene expression profiles in rice exposed to exogenous MG, and study the molecular basis of MG responses. MG affected genes involved in hormone signaling, cell-to-cell communications, and chromatin remodeling. A number of genes encoding bZIP, MYB, NAC, WRKY, AP2/EREBP, and zinc finger transcription factors (TFs) were also found to be MG-responsive. In addition, various genes encoding protein kinases, including mitogen-activated protein kinases (MAP kinases), calcium/calmodulin-dependent protein kinases (CDPKs), Ser/Thr protein kinases, histidine kinases and receptor-like kinases, and OsRR2 type-A response regulator showed changes in their expression patterns. Since cellular MG levels increase in plants in response to stressful conditions, altered expression patterns of stress-inducible genes encoding TFs and protein kinases are expected to be observed following MG application (
<bold>Figure
<xref ref-type="fig" rid="F2">2</xref>
</bold>
). Using
<italic>in silico</italic>
analysis,
<xref rid="B44" ref-type="bibr">Kaur et al. (2015a)</xref>
identified conserved motifs as MG-responsive elements (MGREs) in the upstream regions of MG-responsive genes and provided the putative MGRE sequences (CTXXCTC and GGCGGCGX). The ability of MG to influence the stress-responsive signaling network highlights the importance of MG in plant stress responses.</p>
</sec>
</sec>
<sec>
<title>Glyoxalases in Plant Abiotic Stress Responses and Adaptation to Environmental Stressors</title>
<p>The glyoxalase system is involved in various cellular functions, but the involvement of this system in plant stress responses and tolerance is regarded as its most significant role (
<xref rid="B43" ref-type="bibr">Kaur et al., 2014a</xref>
). The glyoxalase system regulates MG levels in plants under stress and regenerates GSH. GSH and a high GSH/GSSG ratio are required to help protect plants against oxidative stress (
<xref rid="B115" ref-type="bibr">Yadav et al., 2005a</xref>
,
<xref rid="B116" ref-type="bibr">b</xref>
;
<xref rid="B75" ref-type="bibr">Noctor et al., 2012</xref>
), and GSH is directly or indirectly required for the functioning of various antioxidant enzymes, including GST, glutathione peroxidase (GPX), and APX (
<xref rid="B117" ref-type="bibr">Yadav et al., 2008</xref>
). Several studies have shown close links between the antioxidant and glyoxalase systems in plants, suggesting a direct influence of the glyoxalase system on ROS detoxification (
<xref rid="B115" ref-type="bibr">Yadav et al., 2005a</xref>
;
<xref rid="B12" ref-type="bibr">El-Shabrawi et al., 2010</xref>
;
<xref rid="B107" ref-type="bibr">Upadhyaya et al., 2011</xref>
;
<xref rid="B67" ref-type="bibr">Mostofa et al., 2014a</xref>
,
<xref rid="B63" ref-type="bibr">2015a</xref>
).</p>
<p>An increase in glyoxalase enzyme activities occurs in plants in response to many different stressors, including osmotic stress, extremes of temperature, heavy metals and exposure to stress-related hormones, including MeJA, ABA and salicylic acid (SA) (
<xref rid="B33" ref-type="bibr">Hossain and Fujita, 2009</xref>
;
<xref rid="B35" ref-type="bibr">Hossain et al., 2009</xref>
). Transcriptomic and proteomic analyses of various plant species have improved our knowledge and understanding of the roles of glyoxalases in plant stress responses and tolerance (
<xref rid="B98" ref-type="bibr">Singla-Pareek et al., 2003</xref>
,
<xref rid="B99" ref-type="bibr">2006</xref>
;
<xref rid="B35" ref-type="bibr">Hossain et al., 2009</xref>
;
<xref rid="B55" ref-type="bibr">Lin et al., 2010</xref>
;
<xref rid="B70" ref-type="bibr">Mustafiz et al., 2011</xref>
). Plant glyoxalase genes (
<italic>Gly I and Gly II</italic>
) have been cloned from various plant species and characterized in detail. The expression of
<italic>Gly I</italic>
and
<italic>Gly II</italic>
genes has been shown to be up-regulated in many plant species by a diverse range of environmental cues, and plants overexpressing either
<italic>Gly I</italic>
or
<italic>Gly II</italic>
showed enhanced plant abiotic stress tolerance (
<xref rid="B98" ref-type="bibr">Singla-Pareek et al., 2003</xref>
,
<xref rid="B99" ref-type="bibr">2006</xref>
,
<xref rid="B100" ref-type="bibr">2008</xref>
;
<xref rid="B55" ref-type="bibr">Lin et al., 2010</xref>
;
<xref rid="B4" ref-type="bibr">Alvarez Viveros et al., 2013</xref>
;
<xref rid="B114" ref-type="bibr">Wu et al., 2013</xref>
;
<xref rid="B43" ref-type="bibr">Kaur et al., 2014a</xref>
,
<xref rid="B47" ref-type="bibr">c</xref>
). The genetic manipulation of the glyoxalase system in plants has successfully contributed to improved tolerance to multiple abiotic stresses, such as salinity, heavy metals and MG treatments (
<bold>Table
<xref ref-type="table" rid="T1">1</xref>
</bold>
). Transgenic plants overexpressing glyoxalase pathway genes have lower MG and ROS levels when exposed to stress, because they have better GSH homeostasis and retain better antioxidant enzyme functionality. Thus, glyoxalase enzyme levels can be used as phenomic biomarkers to indicate degrees of stress tolerance, and plants with high glyoxalase enzyme levels are potentially tolerant to a wide range of abiotic stresses (
<xref rid="B47" ref-type="bibr">Kaur et al., 2014c</xref>
). In
<bold>Table
<xref ref-type="table" rid="T1">1</xref>
</bold>
, we summarized most of the successful transgenic studies that showed that transgenic plants, including important crop plants, overexpressing individually or together
<italic>Gly I</italic>
and
<italic>Gly II</italic>
have increased stress tolerance.</p>
<table-wrap id="T1" position="float">
<label>Table 1</label>
<caption>
<p>Glyoxalase genes overexpressed in transgenic plants exhibiting enhanced abiotic stress tolerance.</p>
</caption>
<table frame="hsides" rules="groups" cellspacing="5" cellpadding="5">
<thead>
<tr>
<th valign="top" align="left" rowspan="1" colspan="1">Gene</th>
<th valign="top" align="left" rowspan="1" colspan="1">Plant species</th>
<th valign="top" align="left" rowspan="1" colspan="1">Response phenotype</th>
<th valign="top" align="left" rowspan="1" colspan="1">Reference</th>
</tr>
</thead>
<tbody>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1">
<italic>Gly I</italic>
</td>
<td valign="top" align="left" rowspan="1" colspan="1">Tobacco (
<italic>Nicotiana tabacum)</italic>
</td>
<td valign="top" align="left" rowspan="1" colspan="1">Improved salt stress tolerance</td>
<td valign="top" align="left" rowspan="1" colspan="1">
<xref rid="B108" ref-type="bibr">Veena et al., 1999</xref>
</td>
</tr>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1">
<italic>Gly I</italic>
</td>
<td valign="top" align="left" rowspan="1" colspan="1">Black gram (
<italic>Vigna mungo)</italic>
</td>
<td valign="top" align="left" rowspan="1" colspan="1">Improved salt stress tolerance</td>
<td valign="top" align="left" rowspan="1" colspan="1">
<xref rid="B8" ref-type="bibr">Bhomkar et al., 2008</xref>
</td>
</tr>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1">
<italic>Gly I</italic>
</td>
<td valign="top" align="left" rowspan="1" colspan="1">
<italic>Arabidopsis thaliana</italic>
</td>
<td valign="top" align="left" rowspan="1" colspan="1">Improved salt stress tolerance</td>
<td valign="top" align="left" rowspan="1" colspan="1">
<xref rid="B88" ref-type="bibr">Roy et al., 2008</xref>
</td>
</tr>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1">
<italic>Gly I</italic>
</td>
<td valign="top" align="left" rowspan="1" colspan="1">Rice (
<italic>Oryza sativa)</italic>
</td>
<td valign="top" align="left" rowspan="1" colspan="1">Improved salt stress tolerance</td>
<td valign="top" align="left" rowspan="1" colspan="1">
<xref rid="B109" ref-type="bibr">Verma et al., 2005</xref>
</td>
</tr>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1">
<italic>Gly I</italic>
</td>
<td valign="top" align="left" rowspan="1" colspan="1">Tobacco (
<italic>Nicotiana tabacum)</italic>
</td>
<td valign="top" align="left" rowspan="1" colspan="1">Improved salt stress tolerance</td>
<td valign="top" align="left" rowspan="1" colspan="1">
<xref rid="B115" ref-type="bibr">Yadav et al., 2005a</xref>
</td>
</tr>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1">
<italic>Gly I</italic>
</td>
<td valign="top" align="left" rowspan="1" colspan="1">Tobacco (
<italic>Nicotiana tabacum)</italic>
</td>
<td valign="top" align="left" rowspan="1" colspan="1">Improved zinc tolerance</td>
<td valign="top" align="left" rowspan="1" colspan="1">
<xref rid="B55" ref-type="bibr">Lin et al., 2010</xref>
</td>
</tr>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1">
<italic>Gly I</italic>
</td>
<td valign="top" align="left" rowspan="1" colspan="1">Tobacco (
<italic>Nicotiana tabacum</italic>
</td>
<td valign="top" align="left" rowspan="1" colspan="1">Improved tolerance to MG, salt stress, excessive mannitol and H
<sub>2</sub>
O
<sub>2</sub>
</td>
<td valign="top" align="left" rowspan="1" colspan="1">
<xref rid="B114" ref-type="bibr">Wu et al., 2013</xref>
</td>
</tr>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1">
<italic>Gly I</italic>
</td>
<td valign="top" align="left" rowspan="1" colspan="1">Tobacco (
<italic>Nicotiana tabacum)</italic>
</td>
<td valign="top" align="left" rowspan="1" colspan="1">Improved tolerance to MG and salt stress</td>
<td valign="top" align="left" rowspan="1" colspan="1">
<xref rid="B69" ref-type="bibr">Mustafiz et al., 2014</xref>
</td>
</tr>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1">
<italic>Gly II</italic>
</td>
<td valign="top" align="left" rowspan="1" colspan="1">Rice (
<italic>Oryza sativa)</italic>
</td>
<td valign="top" align="left" rowspan="1" colspan="1">Improved salinity tolerance</td>
<td valign="top" align="left" rowspan="1" colspan="1">
<xref rid="B100" ref-type="bibr">Singla-Pareek et al., 2008</xref>
</td>
</tr>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1">
<italic>Gly II</italic>
</td>
<td valign="top" align="left" rowspan="1" colspan="1">Mustard
<italic>(Brassica juncea)</italic>
</td>
<td valign="top" align="left" rowspan="1" colspan="1">Improved salinity tolerance</td>
<td valign="top" align="left" rowspan="1" colspan="1">
<xref rid="B92" ref-type="bibr">Saxena et al., 2011</xref>
</td>
</tr>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1">
<italic>Gly II</italic>
</td>
<td valign="top" align="left" rowspan="1" colspan="1">Rice (
<italic>Oryza sativa)</italic>
</td>
<td valign="top" align="left" rowspan="1" colspan="1">Improved salinity tolerance</td>
<td valign="top" align="left" rowspan="1" colspan="1">
<xref rid="B111" ref-type="bibr">Wani and Gosal, 2011</xref>
</td>
</tr>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1">
<italic>Gly II</italic>
</td>
<td valign="top" align="left" rowspan="1" colspan="1">
<italic>Arabidopsis thaliana</italic>
</td>
<td valign="top" align="left" rowspan="1" colspan="1">Improved salt and anoxic stress tolerance</td>
<td valign="top" align="left" rowspan="1" colspan="1">
<xref rid="B10" ref-type="bibr">Devanathan et al., 2014</xref>
</td>
</tr>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1">
<italic>Gly II</italic>
</td>
<td valign="top" align="left" rowspan="1" colspan="1">Tobacco (
<italic>Nicotiana tabacum)</italic>
</td>
<td valign="top" align="left" rowspan="1" colspan="1">Improved salinity tolerance</td>
<td valign="top" align="left" rowspan="1" colspan="1">
<xref rid="B17" ref-type="bibr">Ghosh et al., 2014</xref>
</td>
</tr>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1">
<italic>Gly I</italic>
+
<italic>Gly II</italic>
</td>
<td valign="top" align="left" rowspan="1" colspan="1">Tobacco (
<italic>Nicotiana tabacum)</italic>
</td>
<td valign="top" align="left" rowspan="1" colspan="1">Improved salinity tolerance and set viable seeds under zinc-spiked soils</td>
<td valign="top" align="left" rowspan="1" colspan="1">
<xref rid="B98" ref-type="bibr">Singla-Pareek et al., 2003</xref>
,
<xref rid="B99" ref-type="bibr">2006</xref>
;
<xref rid="B116" ref-type="bibr">Yadav et al., 2005b</xref>
</td>
</tr>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1">
<italic>Gly I</italic>
+
<italic>Gly II</italic>
</td>
<td valign="top" align="left" rowspan="1" colspan="1">Tomato (
<italic>Solanum lycopersicum)</italic>
</td>
<td valign="top" align="left" rowspan="1" colspan="1">Improved salt stress tolerance</td>
<td valign="top" align="left" rowspan="1" colspan="1">
<xref rid="B4" ref-type="bibr">Alvarez Viveros et al., 2013</xref>
</td>
</tr>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1">
<italic>Gly I</italic>
+
<italic>Gly II</italic>
</td>
<td valign="top" align="left" rowspan="1" colspan="1">Carrizo citrange (
<italic>Citrus sinensis</italic>
×
<italic>Poncirus trifoliata)</italic>
</td>
<td valign="top" align="left" rowspan="1" colspan="1">Improved salinity tolerance</td>
<td valign="top" align="left" rowspan="1" colspan="1">
<xref rid="B3" ref-type="bibr">Alvarez-Gerding et al., 2015</xref>
</td>
</tr>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1"></td>
</tr>
</tbody>
</table>
<table-wrap-foot>
<attrib>
<italic>
<italic>Gly</italic>
, glyoxalase.</italic>
</attrib>
</table-wrap-foot>
</table-wrap>
<p>In addition to the transgenic approach, alternative methods, such as treatments of seeds prior to sowing and/or plants with exogenous chemicals, e.g., plant growth regulators, osmoprotectants, signaling molecules etc., can also alter the glyoxalase system in plants, thereby improving stress tolerance (
<bold>Table
<xref ref-type="table" rid="T2">2</xref>
</bold>
). For instance, treatment of rice seedlings with Ca has been shown to increase the activities of Gly I and Gly II, contributing to the reduction in As- and Cd- induced growth inhibition (
<xref rid="B84" ref-type="bibr">Rahman et al., 2015a</xref>
,
<xref rid="B85" ref-type="bibr">b</xref>
).
<xref rid="B62" ref-type="bibr">Mostofa and Fujita (2013)</xref>
reported that a SA pre-treatment of rice seedlings under Cu stress alleviated Cu-toxicity by increasing the capacity of both antioxidant and glyoxalase systems.
<bold>Table
<xref ref-type="table" rid="T2">2</xref>
</bold>
lists most of the important studies in which chemical treatments were used to influence the glyoxalase system, leading to enhanced stress tolerance.</p>
<table-wrap id="T2" position="float">
<label>Table 2</label>
<caption>
<p>Effects of exogenous chemicals on glyoxalase systems and abiotic stress tolerance.</p>
</caption>
<table frame="hsides" rules="groups" cellspacing="5" cellpadding="5">
<thead>
<tr>
<th valign="top" align="left" rowspan="1" colspan="1">Plant species</th>
<th valign="top" align="left" rowspan="1" colspan="1">Types of stresses</th>
<th valign="top" align="center" rowspan="1" colspan="1">Exogenous chemicals</th>
<th valign="top" align="left" rowspan="1" colspan="1">Responses of glyoxalases (Gly I and II)</th>
<th valign="top" align="center" rowspan="1" colspan="1">Concentration of MG</th>
<th valign="top" align="left" rowspan="1" colspan="1">Reference</th>
</tr>
</thead>
<tbody>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1">Rice (
<italic>Oryza sativa</italic>
L.)</td>
<td valign="top" align="left" rowspan="1" colspan="1">As, Cd</td>
<td valign="top" align="center" rowspan="1" colspan="1">Ca</td>
<td valign="top" align="left" rowspan="1" colspan="1">Gly I ↑ Gly II ↑ (As)</td>
<td valign="top" align="center" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1">
<xref rid="B84" ref-type="bibr">Rahman et al., 2015a</xref>
,
<xref rid="B85" ref-type="bibr">b</xref>
</td>
</tr>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1"></td>
<td valign="top" align="center" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1">Gly I ↑ Gly II ↑ (Cd)</td>
<td valign="top" align="center" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1"></td>
</tr>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1">Rice (
<italic>Oryza sativa</italic>
L.)</td>
<td valign="top" align="left" rowspan="1" colspan="1">Cu</td>
<td valign="top" align="center" rowspan="1" colspan="1">SA</td>
<td valign="top" align="left" rowspan="1" colspan="1">Gly I ↑</td>
<td valign="top" align="center" rowspan="1" colspan="1">ND</td>
<td valign="top" align="left" rowspan="1" colspan="1">
<xref rid="B62" ref-type="bibr">Mostofa and Fujita, 2013</xref>
;
<xref rid="B67" ref-type="bibr">Mostofa et al., 2014a</xref>
</td>
</tr>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1"></td>
<td valign="top" align="center" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1">Gly II ↑</td>
<td valign="top" align="center" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1"></td>
</tr>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1">Rice (
<italic>Oryza sativa</italic>
L.)</td>
<td valign="top" align="left" rowspan="1" colspan="1">Heat</td>
<td valign="top" align="center" rowspan="1" colspan="1">Spd</td>
<td valign="top" align="left" rowspan="1" colspan="1">Gly I ↑</td>
<td valign="top" align="center" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1">
<xref rid="B68" ref-type="bibr">Mostofa et al., 2014b</xref>
</td>
</tr>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1"></td>
<td valign="top" align="center" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1">Gly II ↑</td>
<td valign="top" align="center" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1"></td>
</tr>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1">Rice (
<italic>Oryza sativa</italic>
L.)</td>
<td valign="top" align="left" rowspan="1" colspan="1">NaCl, Cu</td>
<td valign="top" align="center" rowspan="1" colspan="1">Tre</td>
<td valign="top" align="left" rowspan="1" colspan="1">Gly I ↕ Gly II ↑ (NaCl)</td>
<td valign="top" align="center" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1">
<xref rid="B63" ref-type="bibr">Mostofa et al., 2015a</xref>
,
<xref rid="B64" ref-type="bibr">b</xref>
</td>
</tr>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1"></td>
<td valign="top" align="center" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1">Gly I ↑ Gly II ↑ (Cu)</td>
<td valign="top" align="center" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1"></td>
</tr>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1">Rice (
<italic>Oryza sativa</italic>
L.)</td>
<td valign="top" align="left" rowspan="1" colspan="1">Cd, NaCl</td>
<td valign="top" align="center" rowspan="1" colspan="1">H
<sub>2</sub>
S</td>
<td valign="top" align="left" rowspan="1" colspan="1">Gly I ↓ Gly II ↑ (Cd)</td>
<td valign="top" align="center" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1">
<xref rid="B65" ref-type="bibr">Mostofa et al., 2015c</xref>
,
<xref rid="B66" ref-type="bibr">d</xref>
</td>
</tr>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1"></td>
<td valign="top" align="center" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1">Gly I ↓ Gly II ↑ (NaCl)</td>
<td valign="top" align="center" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1"></td>
</tr>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1">Mung bean (
<italic>Vigna radiata</italic>
L.)</td>
<td valign="top" align="left" rowspan="1" colspan="1">Cd</td>
<td valign="top" align="center" rowspan="1" colspan="1">Pro and GB</td>
<td valign="top" align="left" rowspan="1" colspan="1">Gly I ↑</td>
<td valign="top" align="center" rowspan="1" colspan="1">ND</td>
<td valign="top" align="left" rowspan="1" colspan="1">
<xref rid="B34" ref-type="bibr">Hossain et al., 2010</xref>
</td>
</tr>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1"></td>
<td valign="top" align="center" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1">Gly II ↑</td>
<td valign="top" align="center" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1"></td>
</tr>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1">Mustard (
<italic>Brassica juncea</italic>
L.)</td>
<td valign="top" align="left" rowspan="1" colspan="1">Drought</td>
<td valign="top" align="center" rowspan="1" colspan="1">Pro and GB</td>
<td valign="top" align="left" rowspan="1" colspan="1">Gly I ↕ Gly II ↑</td>
<td valign="top" align="center" rowspan="1" colspan="1">ND</td>
<td valign="top" align="left" rowspan="1" colspan="1">
<xref rid="B36" ref-type="bibr">Hossain et al., 2014</xref>
</td>
</tr>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1">Tea (
<italic>Camellia sinensis</italic>
L.)</td>
<td valign="top" align="left" rowspan="1" colspan="1">Cold</td>
<td valign="top" align="center" rowspan="1" colspan="1">Pro and GB</td>
<td valign="top" align="left" rowspan="1" colspan="1">Gly I ↑</td>
<td valign="top" align="center" rowspan="1" colspan="1">ND</td>
<td valign="top" align="left" rowspan="1" colspan="1">
<xref rid="B51" ref-type="bibr">Kumar and Yadav, 2009</xref>
</td>
</tr>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1"></td>
<td valign="top" align="center" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1">Gly II ↑</td>
<td valign="top" align="center" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1"></td>
</tr>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1">Tobacco (
<italic>Nicotiana tabacum</italic>
L.)</td>
<td valign="top" align="left" rowspan="1" colspan="1">NaCl</td>
<td valign="top" align="center" rowspan="1" colspan="1">Pro and GB</td>
<td valign="top" align="left" rowspan="1" colspan="1">Gly I ↑</td>
<td valign="top" align="center" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1">
<xref rid="B26" ref-type="bibr">Hoque et al., 2008</xref>
</td>
</tr>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1"></td>
<td valign="top" align="center" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1">Gly II ↕</td>
<td valign="top" align="center" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1"></td>
</tr>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1">Mung bean (
<italic>Vigna radiata</italic>
L.)</td>
<td valign="top" align="left" rowspan="1" colspan="1">Heat, Drought</td>
<td valign="top" align="center" rowspan="1" colspan="1">GSH</td>
<td valign="top" align="left" rowspan="1" colspan="1">Gly I ↓ Gly II ↑ (Drought)</td>
<td valign="top" align="center" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1">
<xref rid="B72" ref-type="bibr">Nahar et al., 2015b</xref>
,
<xref rid="B73" ref-type="bibr">c</xref>
</td>
</tr>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1"></td>
<td valign="top" align="center" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1">Gly I ↑ Gly II ↑ (Heat)</td>
<td valign="top" align="center" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1"></td>
</tr>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1">Wheat (
<italic>Triticum aestivum</italic>
)</td>
<td valign="top" align="left" rowspan="1" colspan="1">Heat, NaCl</td>
<td valign="top" align="center" rowspan="1" colspan="1">NO</td>
<td valign="top" align="left" rowspan="1" colspan="1">Gly I ↑ Gly II ↕ (Heat)</td>
<td valign="top" align="center" rowspan="1" colspan="1">ND</td>
<td valign="top" align="left" rowspan="1" colspan="1">
<xref rid="B22" ref-type="bibr">Hasanuzzaman et al., 2011a</xref>
,
<xref rid="B25" ref-type="bibr">2012b</xref>
</td>
</tr>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1"></td>
<td valign="top" align="center" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1">Gly I ↑ Gly II ↑ (NaCl)</td>
<td valign="top" align="center" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1"></td>
</tr>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1">Rapeseed (
<italic>Brassica napus</italic>
)</td>
<td valign="top" align="left" rowspan="1" colspan="1">Drought, NaCl, Cd</td>
<td valign="top" align="center" rowspan="1" colspan="1">Se</td>
<td valign="top" align="left" rowspan="1" colspan="1">Gly I ↑ Gly II ↑ (Drought)</td>
<td valign="top" align="center" rowspan="1" colspan="1">ND</td>
<td valign="top" align="left" rowspan="1" colspan="1">
<xref rid="B21" ref-type="bibr">Hasanuzzaman and Fujita, 2011</xref>
;
<xref rid="B23" ref-type="bibr">Hasanuzzaman et al., 2011b</xref>
,
<xref rid="B24" ref-type="bibr">2012a</xref>
</td>
</tr>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1"></td>
<td valign="top" align="center" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1">Gly I ↑ Gly II ↑ (NaCl)</td>
<td valign="top" align="center" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1"></td>
</tr>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1"></td>
<td valign="top" align="center" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1">Gly I ↑ Gly II ↑ (Cd)</td>
<td valign="top" align="center" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1"></td>
</tr>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1">
<italic>Ficusconcinna</italic>
</td>
<td valign="top" align="left" rowspan="1" colspan="1">Heat</td>
<td valign="top" align="center" rowspan="1" colspan="1">BRs</td>
<td valign="top" align="left" rowspan="1" colspan="1">Gly I ↑ Gly II ↑</td>
<td valign="top" align="center" rowspan="1" colspan="1"></td>
<td valign="top" align="left" rowspan="1" colspan="1">
<xref rid="B40" ref-type="bibr">Jin et al., 2015</xref>
</td>
</tr>
<tr>
<td valign="top" align="left" rowspan="1" colspan="1"></td>
</tr>
</tbody>
</table>
<table-wrap-foot>
<attrib>
<italic>As, Cd, Cu, Ca, SA, Spd, Tre, H
<sub>2</sub>
S, Pro, GB, GSH, NO, Se, and BRs correspond to arsenic, cadmium, copper, calcium, salicylic acid, spermidine, trehalose, hydrogen sulfide, proline, glycinebetaine, glutathione, nitric oxide, selenium, and brassinosteroids, respectively. Gly, glyoxalase; ↑, increased; ↕, unchanged; ↓, decreased; ND, not determined.</italic>
</attrib>
</table-wrap-foot>
</table-wrap>
</sec>
<sec>
<title>Conclusion and Future Perspectives</title>
<p>Recent studies of MG metabolism have revealed many important functions of MG related to stress responses and tolerance in plants. The excessive accumulation of MG in plants is an inevitable stress, but MG can stimulate the components of different stress-protection pathways (
<bold>Figure
<xref ref-type="fig" rid="F2">2</xref>
</bold>
;
<xref rid="B13" ref-type="bibr">Engqvist et al., 2009</xref>
;
<xref rid="B30" ref-type="bibr">Hoque et al., 2012a</xref>
,
<xref rid="B31" ref-type="bibr">b</xref>
,
<xref rid="B32" ref-type="bibr">c</xref>
;
<xref rid="B113" ref-type="bibr">Wienstroer et al., 2012</xref>
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<xref rid="B44" ref-type="bibr">Kaur et al., 2015a</xref>
), which could be considered as an acclimation/adaptation process. The glyoxalase pathway scavenges MG and confers tolerance to multiple stresses; and thus, MG levels and glyoxalase pathway are closely associated with abiotic stress tolerance in plants. The signaling roles of MG in up-regulating stress-responsive pathways and its potential to active multiple pathways have made MG a suitable marker for abiotic stress tolerance in plants. Recent progress made by genome-wide and
<italic>in silico</italic>
analyses has revealed intricate regulatory networks associated with MG signaling, which control gene expression, protein modification and the metabolite composition of plants. Further omic studies investigating the roles of MG would be worthwhile to improve our understanding of multiple abiotic stress tolerance. In-depth understanding of the interactions of MG with Ca
<sup>2+</sup>
, ROS, NO, H
<sub>2</sub>
S, plant hormones, TFs, and the glyoxalase system, as well as with other MG detoxification systems in different subcellular compartments will reveal more regulatory roles for MG in plant abiotic stress responses and tolerance.</p>
</sec>
<sec>
<title>Author Contributions</title>
<p>TH and MH conceived the idea. TH, MH, MM, DB, MF, and L-ST wrote the manuscript. All authors read and approved the final manuscript.</p>
</sec>
<sec>
<title>Conflict of Interest Statement</title>
<p>The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.</p>
</sec>
</body>
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