Selective herbicide safening in dicot plants: a case study in Arabidopsis

Safeners are agrochemicals co-applied with herbicides that facilitate selective control of weeds by protecting monocot crops from chemical injury through enhancing the expression of detoxifying enzymes such as glutathione transferases (GSTs). Even though the application of safeners causes the induct...

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Main Authors: Gabriela Pingarron-Cardenas, Nawaporn Onkokesung, Alina Goldberg-Cavalleri, Gudrun Lange, Jan Dittgen, Robert Edwards
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-01-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2023.1335764/full
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author Gabriela Pingarron-Cardenas
Nawaporn Onkokesung
Alina Goldberg-Cavalleri
Gudrun Lange
Jan Dittgen
Robert Edwards
author_facet Gabriela Pingarron-Cardenas
Nawaporn Onkokesung
Alina Goldberg-Cavalleri
Gudrun Lange
Jan Dittgen
Robert Edwards
author_sort Gabriela Pingarron-Cardenas
collection DOAJ
description Safeners are agrochemicals co-applied with herbicides that facilitate selective control of weeds by protecting monocot crops from chemical injury through enhancing the expression of detoxifying enzymes such as glutathione transferases (GSTs). Even though the application of safeners causes the induction of genes encoding GSTs in model dicots such as Arabidopsis thaliana, safeners do not protect broadleaf crops from herbicide injury. In this study, we proposed that the localized induction of Arabidopsis GSTs and the fundamental differences in their detoxifying activity between dicot and monocot species, underpin the failure of safeners to protect Arabidopsis from herbicide toxicity. Using the herbicide safener, isoxadifen-ethyl, we showed that three tau (U) family GSTs namely AtGSTU7, AtGSTU19 and AtGSTU24 were induced with different magnitude by isoxadifen treatment in root and rosette tissues. The higher magnitude of inducibility of these AtGSTUs in the root tissues coincided with the enhanced metabolism of flufenacet, a herbicide that is active in root tissue, protecting Arabidopsis plants from chemical injury. Assay of the recombinant enzyme activities and the significant reduction in flufenacet metabolism determined in the T-DNA insertion mutant of AtGSTU7 (gstu7) in Arabidopsis plants identified an important function for AtGSTU7 protein in flufenacet detoxification. In-silico structural modeling of AtGSTU7, suggested the unique high activity of this enzyme toward flufenacet was due to a less constrained active site compared to AtGSTU19 and AtGSTU24. We demonstrate here that it is possible to induce herbicide detoxification in dicotyledonous plants by safener treatment, albeit with this activity being restricted to very specific combinations of herbicide chemistry, and the localized induction of enzymes with specific detoxifying activities.
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spelling doaj.art-1298a68b83a9486d8a3f3684f1bc15632024-01-15T04:23:38ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2024-01-011410.3389/fpls.2023.13357641335764Selective herbicide safening in dicot plants: a case study in ArabidopsisGabriela Pingarron-Cardenas0Nawaporn Onkokesung1Alina Goldberg-Cavalleri2Gudrun Lange3Jan Dittgen4Robert Edwards5Agriculture, School of Natural and Environmental Sciences, Newcastle University, Newcastle Upon Tyne, United KingdomAgriculture, School of Natural and Environmental Sciences, Newcastle University, Newcastle Upon Tyne, United KingdomAgriculture, School of Natural and Environmental Sciences, Newcastle University, Newcastle Upon Tyne, United KingdomBayer Aktiengesellschaft (AG), Crop Science Division, Computational Life Sciences, Frankfurt, GermanyBayer Aktiengesellschaft (AG), Crop Science Division, Weed Control Research, Frankfurt, GermanyAgriculture, School of Natural and Environmental Sciences, Newcastle University, Newcastle Upon Tyne, United KingdomSafeners are agrochemicals co-applied with herbicides that facilitate selective control of weeds by protecting monocot crops from chemical injury through enhancing the expression of detoxifying enzymes such as glutathione transferases (GSTs). Even though the application of safeners causes the induction of genes encoding GSTs in model dicots such as Arabidopsis thaliana, safeners do not protect broadleaf crops from herbicide injury. In this study, we proposed that the localized induction of Arabidopsis GSTs and the fundamental differences in their detoxifying activity between dicot and monocot species, underpin the failure of safeners to protect Arabidopsis from herbicide toxicity. Using the herbicide safener, isoxadifen-ethyl, we showed that three tau (U) family GSTs namely AtGSTU7, AtGSTU19 and AtGSTU24 were induced with different magnitude by isoxadifen treatment in root and rosette tissues. The higher magnitude of inducibility of these AtGSTUs in the root tissues coincided with the enhanced metabolism of flufenacet, a herbicide that is active in root tissue, protecting Arabidopsis plants from chemical injury. Assay of the recombinant enzyme activities and the significant reduction in flufenacet metabolism determined in the T-DNA insertion mutant of AtGSTU7 (gstu7) in Arabidopsis plants identified an important function for AtGSTU7 protein in flufenacet detoxification. In-silico structural modeling of AtGSTU7, suggested the unique high activity of this enzyme toward flufenacet was due to a less constrained active site compared to AtGSTU19 and AtGSTU24. We demonstrate here that it is possible to induce herbicide detoxification in dicotyledonous plants by safener treatment, albeit with this activity being restricted to very specific combinations of herbicide chemistry, and the localized induction of enzymes with specific detoxifying activities.https://www.frontiersin.org/articles/10.3389/fpls.2023.1335764/fullcerealflufenacetglutathione transferaseherbicide detoxificationisoxadifen-ethyl
spellingShingle Gabriela Pingarron-Cardenas
Nawaporn Onkokesung
Alina Goldberg-Cavalleri
Gudrun Lange
Jan Dittgen
Robert Edwards
Selective herbicide safening in dicot plants: a case study in Arabidopsis
Frontiers in Plant Science
cereal
flufenacet
glutathione transferase
herbicide detoxification
isoxadifen-ethyl
title Selective herbicide safening in dicot plants: a case study in Arabidopsis
title_full Selective herbicide safening in dicot plants: a case study in Arabidopsis
title_fullStr Selective herbicide safening in dicot plants: a case study in Arabidopsis
title_full_unstemmed Selective herbicide safening in dicot plants: a case study in Arabidopsis
title_short Selective herbicide safening in dicot plants: a case study in Arabidopsis
title_sort selective herbicide safening in dicot plants a case study in arabidopsis
topic cereal
flufenacet
glutathione transferase
herbicide detoxification
isoxadifen-ethyl
url https://www.frontiersin.org/articles/10.3389/fpls.2023.1335764/full
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AT gudrunlange selectiveherbicidesafeningindicotplantsacasestudyinarabidopsis
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