Glyoxalase Goes Green: The Expanding Roles of Glyoxalase in Plants

Sankaranarayanan, Subramanian; Jamshed, Muhammad; Abhinandan, Kumar; Skori, Logan; Scandola, Sabine; Wang, Tina; Spiegel, David A.; Samuel, Marcus A.

doi:10.3390/ijms18040898

Cited by 68 publications

(50 citation statements)

References 73 publications

(104 reference statements)

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“…It was found that over-expressed GLYI and/or GLYII in plants significantly increased their tolerance to various abiotic stresses such as salinity, drought, extreme temperature and heavy-metal toxicity [32][33][34][35][36]. Thus, glyoxalases have been suggested as biomarkers for plant stress resistance [31,37]. In addition to abiotic stress responses, glyoxalase genes have also been reported to be regulated by biotic stresses.…”

Section: Introductionmentioning

confidence: 99%

Genome-wide analysis of glyoxalase-like gene families in grape (Vitis vinifera L.) and their expression profiling in response to downy mildew infection

Cheng

Wang

et al. 2019

BMC Genomics

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Background: The glyoxalase system usually comprises two enzymes, glyoxalase I (GLYI) and glyoxalase II (GLYII). This system converts cytotoxic methylglyoxal (MG) into non-toxic D-lactate in the presence of reduced glutathione (GSH) in two enzymatic steps. Recently, a novel type of glyoxalase III (GLYIII) activity has observed in Escherichia coli that can detoxify MG into D-lactate directly, in one step, without a cofactor. Investigation of the glyoxalase enzymes of a number of plant species shows the importance of their roles in response both to abiotic and to biotic stresses. Until now, glyoxalase gene families have been identified in the genomes of four plants, Arabidopsis, Oryza sativa, Glycine max and Medicago truncatula but no similar study has been done with the grapevine Vitis vinifera L. Results: In this study, four GLYI-like, two GLYII-like and three GLYIII-like genes are identified from the genome database of grape. All these genes were analysed in detail, including their chromosomal locations, phylogenetic relationships, exon-intron distributions, protein domain organisations and the presence of conserved binding sites. Using quantitative real-time PCR analysis (qRT-PCR), the expression profiles of these genes were analysed in different tissues of grape, and also when under infection stress from downy mildew (Plasmopara viticola). The study reveals that most VvGLY-like genes had higher expressions in stem, leaf, tendril and ovule but lower expressions in the flower. In addition, most of the VvGLY-like gene members were P. viticola responsive with high expressions 6-12 h and 96-120 h after inoculation. However, VvGLYI-like1 was highly expressed 48 h after inoculation, similar to VvPR1 and VvNPR1 which are involved in the defence response. Conclusions: This study identified the GLYI-like, GLYII-like and GLYIII-like full gene families of the grapevine. Based on a phylogenetic analysis and the presence of conserved binding sites, we speculate that these glyoxalase-like genes in grape encode active glyoxalases. Moreover, our study provides a basis for discussing the roles of VvGLYIlike, VvGLYII-like and VvGLYIII-like genes in grape's response to downy mildew infection. Our results shed light on the selection of candidate genes for downy mildew tolerance in grape and lay the foundation for further functional investigations of these glyoxalase genes.

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Section: Introductionmentioning

confidence: 99%

Genome-wide analysis of glyoxalase-like gene families in grape (Vitis vinifera L.) and their expression profiling in response to downy mildew infection

Cheng

Wang

et al. 2019

BMC Genomics

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“…The importance of the glyoxalase system has been well established in multiple developmental, physiological, and pathological processes in both prokaryotes and eukaryotes, including organismal longevity, cell proliferation, embryogenesis, and cell death (23,24). Both plant glyoxalase enzymes exist as multigene families, and both are required for regulation of cell division, mitigation of biotic and abiotic stress, reproductive and morphogenetic cognizance, signaling cascades, and the regulation of protein turnover (25).…”

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confidence: 99%

Concomitant Loss of the Glyoxalase System and Glycolysis Makes the Uncultured Pathogen “Candidatus Liberibacter asiaticus” an Energy Scavenger

Jain

Muñoz-Bodnar

Gabriel

2017

Appl Environ Microbiol

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Methylglyoxal (MG) is a cytotoxic, nonenzymatic by-product of glycolysis that readily glycates proteins and DNA, resulting in carbonyl stress. Glyoxalase I and II (GloA and GloB) sequentially convert MG into D-lactic acid using glutathione (GSH) as a cofactor. The glyoxalase system is essential for the mitigation of MG-induced carbonyl stress, preventing subsequent cell death, and recycling GSH for maintenance of cellular redox poise. All pathogenic liberibacters identified to date are uncultured, including "Candidatus Liberibacter asiaticus," a psyllid endosymbiont and causal agent of the severely damaging citrus disease "huanglongbing." In silico analysis revealed the absence of gloA in "Ca. Liberibacter asiaticus" and all other pathogenic liberibacters. Both gloA and gloB are present in Liberibacter crescens, the only liberibacter that has been cultured. L. crescens GloA was functional in a heterologous host. Marker interruption of gloA in L. crescens appeared to be lethal. Key glycolytic enzymes were either missing or significantly downregulated in "Ca. Liberibacter asiaticus" compared to (cultured) L. crescens. Marker interruption of sut, a sucrose transporter gene in L. crescens, decreased its ability to take up exogenously supplied sucrose in culture. "Ca. Liberibacter asiaticus" lacks a homologous sugar transporter but has a functional ATP/ADP translocase, enabling it to thrive both in psyllids and in the sugar-rich citrus phloem by (i) avoiding sucrose uptake, (ii) avoiding MG generation via glycolysis, and (iii) directly importing ATP from the host cell. MG detoxification enzymes appear to be predictive of "Candidatus" status for many uncultured pathogenic and environmental bacteria.IMPORTANCE Discovered more than 100 years ago, the glyoxalase system is thought to be present across all domains of life and fundamental to cellular growth and viability. The glyoxalase system protects against carbonyl stress caused by methylglyoxal (MG), a highly reactive, mutagenic and cytotoxic compound that is nonenzymatically formed as a by-product of glycolysis. The uncultured alphaproteobacterium "Ca. Liberibacter asiaticus" is a well-adapted endosymbiont of the Asian citrus psyllid, which transmits the severely damaging citrus disease "huanglongbing." "Ca. Liberibacter asiaticus" lacks a functional glyoxalase pathway. We report here that the bacterium is able to thrive both in psyllids and in the sugar-rich citrus phloem by (i) avoiding sucrose uptake, (ii) avoiding (significant) MG generation via glycolysis, and (iii) directly importing ATP from the host cell. We hypothesize that failure to culture "Ca. Liberibacter asiaticus" is at least partly due to its dependence on host cells for both ATP and MG detoxification.KEYWORDS ATP/ADP translocase, carbonyl stress, citrus greening, culturability, glycolysis, glyoxalase, huanglongbing, liberibacter, methylglyoxal, sugar transporter

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“…In the GSH-dependent glyoxalase pathway, Gly I is the first enzyme which catalyzes the isomerization of MG into S-2-hydroxyacylglutathione and then Gly II hydrolyzes these thiolesters to produce D-lactate, which will eventually be converted into pyruvate to feed into tricarboxylic acid (TCA) cycle [19][20][21] . Since its initial characterization of the glyoxalase pathway back in 1913 22,23 , the importance of the glyoxalase system in plant defense against various types of biotic and abiotic stresses has been more and more firmly recognized 24,25 .…”

Section: Introductionmentioning

confidence: 99%

Al-induced proteomics changes in tomato plants over-expressing a glyoxalase I gene

Thapa

et al. 2020

Hortic Res

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Glyoxalase I (Gly I) is the first enzyme in the glutathionine-dependent glyoxalase pathway for detoxification of methylglyoxal (MG) under stress conditions. Transgenic tomato 'Money Maker' plants overexpressing tomato SlGlyI gene (tomato unigene accession SGN-U582631/Solyc09g082120.3.1) were generated and homozygous lines were obtained after four generations of self-pollination. In this study, SlGlyI-overepxressing line (GlyI), wild type (WT, negative control) and plants transformed with empty vector (ECtr, positive control), were subjected to Al-treatment by growing in Magnavaca's nutrient solution (pH 4.5) supplemented with 20 µM Al 3+ ion activity. After 30 days of treatments, the fresh and dry weight of shoots and roots of plants from Al-treated conditions decreased significantly compared to the non-treated conditions for all the three lines. When compared across the three lines, root fresh and dry weight of GlyI was significant higher than WT and ECtr, whereas there was no difference in shoot tissues. The basal 5 mm root-tips of GlyI plants expressed a significantly higher level of glyoxalase activity under both non-Al-treated and Al-treated conditions compared to the two control lines. Under Al-treated condition, there was a significant increase in MG content in ECtr and WT lines, but not in GlyI line. Quantitative proteomics analysis using tandem mass tags mass spectrometry identified 4080 quantifiable proteins and 201 Al-induced differentially expressed proteins (DEPs) in roottip tissues from GlyI, and 4273 proteins and 230 DEPs from ECtr. The Al-down-regulated DEPs were classified into molecular pathways of gene transcription, RNA splicing and protein biosynthesis in both GlyI and ECtr lines. The Alinduced DEPs in GlyI associated with tolerance to Al 3+ and MG toxicity are involved in callose degradation, cell wall components (xylan acetylation and pectin degradation), oxidative stress (antioxidants) and turnover of Al-damaged epidermal cells, repair of damaged DNA, epigenetics, gene transcription, and protein translation. A protein-protein association network was constructed to aid the selection of proteins in the same pathway but differentially regulated in GlyI or ECtr lines. Proteomics data are available via ProteomeXchange with identifiers PXD009456 under project title '25Dec2017_Suping_XSexp2_ITAG3.2' for SlGlyI-overexpressing tomato plants and PXD009848 under project title '25Dec2017_Suping_XSexp3_ITAG3.2' for positive control ECtr line transformed with empty vector.

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Glyoxalase Goes Green: The Expanding Roles of Glyoxalase in Plants

Cited by 68 publications

References 73 publications

Genome-wide analysis of glyoxalase-like gene families in grape (Vitis vinifera L.) and their expression profiling in response to downy mildew infection

Genome-wide analysis of glyoxalase-like gene families in grape (Vitis vinifera L.) and their expression profiling in response to downy mildew infection

Concomitant Loss of the Glyoxalase System and Glycolysis Makes the Uncultured Pathogen “Candidatus Liberibacter asiaticus” an Energy Scavenger

Al-induced proteomics changes in tomato plants over-expressing a glyoxalase I gene

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