Comparative Characterization of Three Homologous Glutathione Transferases from the Weed <i>Lolium perenne</i>

The comparative analysis of homologous enzymes is a valuable approach for elucidating enzymes’ structure–function relationships. Glutathione transferases (GSTs, EC. 2.5.1.18) are crucial enzymes in maintaining the homeostatic stability of plant cells by performing various metabolic, regulatory, and...

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Main Authors: Annie Kontouri, Farid Shokry Ataya, Panagiotis Madesis, Nikolaos Labrou
Format: Article
Language:English
Published: MDPI AG 2024-11-01
Series:Foods
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Online Access:https://www.mdpi.com/2304-8158/13/22/3584
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author Annie Kontouri
Farid Shokry Ataya
Panagiotis Madesis
Nikolaos Labrou
author_facet Annie Kontouri
Farid Shokry Ataya
Panagiotis Madesis
Nikolaos Labrou
author_sort Annie Kontouri
collection DOAJ
description The comparative analysis of homologous enzymes is a valuable approach for elucidating enzymes’ structure–function relationships. Glutathione transferases (GSTs, EC. 2.5.1.18) are crucial enzymes in maintaining the homeostatic stability of plant cells by performing various metabolic, regulatory, and detoxifying functions. They are promiscuous enzymes that catalyze a broad range of reactions that involve the nucleophilic attack of the activated thiolate of glutathione (GSH) to electrophilic compounds. In the present work, three highly homologous (96–98%) GSTs from ryegrass <i>Lolium perenne</i> (<i>Lp</i>GSTs) were identified by in silico homology searches and their full-length cDNAs were isolated, cloned, and expressed in <i>E. coli</i> cells. The recombinant enzymes were purified by affinity chromatography and their substrate specificity and kinetic parameters were determined. <i>Lp</i>GSTs belong to the tau class of the GST superfamily, and despite their high sequence homology, their substrate specificity displays remarkable differences. High catalytic activity was determined towards hydroxyperoxides and alkenals, suggesting a detoxification role towards oxidative stress metabolites. The prediction of the structure of the most active <i>Lp</i>GST by molecular modeling allowed the identification of a non-conserved residue (Phe215) with key structural and functional roles. Site-saturation mutagenesis at position 215 and the characterization of eight mutant enzymes revealed that this site plays pleiotropic roles, affecting the affinity of the enzyme for the substrates, catalytic constant, and structural stability. The results of the work have improved our understanding of the GST family in <i>L. perenne</i>, a significant threat to agriculture, sustainable food production, and safety worldwide.
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spelling doaj-art-61277dd8e21849298ec889f55521d5112024-11-26T18:04:26ZengMDPI AGFoods2304-81582024-11-011322358410.3390/foods13223584Comparative Characterization of Three Homologous Glutathione Transferases from the Weed <i>Lolium perenne</i>Annie Kontouri0Farid Shokry Ataya1Panagiotis Madesis2Nikolaos Labrou3Laboratory of Enzyme Technology, Department of Biotechnology, School of Applied Biology and Biotechnology, Agricultural University of Athens, 75 Iera Odos Street, GR-11855 Athens, GreeceDepartment of Biochemistry, College of Science, King Saud University, P.O. Box 2455, Riyadh 11451, Saudi ArabiaInstitute of Applied Biosciences, CERTH, 6th km Charilaou-Thermis Road, P.O. Box 361, Thermi, GR-57001 Thessaloniki, GreeceLaboratory of Enzyme Technology, Department of Biotechnology, School of Applied Biology and Biotechnology, Agricultural University of Athens, 75 Iera Odos Street, GR-11855 Athens, GreeceThe comparative analysis of homologous enzymes is a valuable approach for elucidating enzymes’ structure–function relationships. Glutathione transferases (GSTs, EC. 2.5.1.18) are crucial enzymes in maintaining the homeostatic stability of plant cells by performing various metabolic, regulatory, and detoxifying functions. They are promiscuous enzymes that catalyze a broad range of reactions that involve the nucleophilic attack of the activated thiolate of glutathione (GSH) to electrophilic compounds. In the present work, three highly homologous (96–98%) GSTs from ryegrass <i>Lolium perenne</i> (<i>Lp</i>GSTs) were identified by in silico homology searches and their full-length cDNAs were isolated, cloned, and expressed in <i>E. coli</i> cells. The recombinant enzymes were purified by affinity chromatography and their substrate specificity and kinetic parameters were determined. <i>Lp</i>GSTs belong to the tau class of the GST superfamily, and despite their high sequence homology, their substrate specificity displays remarkable differences. High catalytic activity was determined towards hydroxyperoxides and alkenals, suggesting a detoxification role towards oxidative stress metabolites. The prediction of the structure of the most active <i>Lp</i>GST by molecular modeling allowed the identification of a non-conserved residue (Phe215) with key structural and functional roles. Site-saturation mutagenesis at position 215 and the characterization of eight mutant enzymes revealed that this site plays pleiotropic roles, affecting the affinity of the enzyme for the substrates, catalytic constant, and structural stability. The results of the work have improved our understanding of the GST family in <i>L. perenne</i>, a significant threat to agriculture, sustainable food production, and safety worldwide.https://www.mdpi.com/2304-8158/13/22/3584abiotic stressglutathione transferasebiotic stressherbicide detoxification<i>Lolium perenne</i><i>Lolium</i> sp.
spellingShingle Annie Kontouri
Farid Shokry Ataya
Panagiotis Madesis
Nikolaos Labrou
Comparative Characterization of Three Homologous Glutathione Transferases from the Weed <i>Lolium perenne</i>
Foods
abiotic stress
glutathione transferase
biotic stress
herbicide detoxification
<i>Lolium perenne</i>
<i>Lolium</i> sp.
title Comparative Characterization of Three Homologous Glutathione Transferases from the Weed <i>Lolium perenne</i>
title_full Comparative Characterization of Three Homologous Glutathione Transferases from the Weed <i>Lolium perenne</i>
title_fullStr Comparative Characterization of Three Homologous Glutathione Transferases from the Weed <i>Lolium perenne</i>
title_full_unstemmed Comparative Characterization of Three Homologous Glutathione Transferases from the Weed <i>Lolium perenne</i>
title_short Comparative Characterization of Three Homologous Glutathione Transferases from the Weed <i>Lolium perenne</i>
title_sort comparative characterization of three homologous glutathione transferases from the weed i lolium perenne i
topic abiotic stress
glutathione transferase
biotic stress
herbicide detoxification
<i>Lolium perenne</i>
<i>Lolium</i> sp.
url https://www.mdpi.com/2304-8158/13/22/3584
work_keys_str_mv AT anniekontouri comparativecharacterizationofthreehomologousglutathionetransferasesfromtheweediloliumperennei
AT faridshokryataya comparativecharacterizationofthreehomologousglutathionetransferasesfromtheweediloliumperennei
AT panagiotismadesis comparativecharacterizationofthreehomologousglutathionetransferasesfromtheweediloliumperennei
AT nikolaoslabrou comparativecharacterizationofthreehomologousglutathionetransferasesfromtheweediloliumperennei