Identification of the first plant caffeoyl-quinate esterases in Cichorium intybus

Chlorogenic acid (5-CQA) is a caffeic acid ester widely accumulated in higher plants. It plays roles in defense against biotic and abiotic stresses. As its biosynthetic pathway shares common enzymes and intermediates with that of lignin, 5-CQA has long been hypothesized to be involved in lignin form...

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Main Authors: Antoine Mallavergne, David Mathiron, Roland Molinié, Jean-Louis Hilbert, David Gagneul
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-08-01
Series:Frontiers in Plant Science
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Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2025.1632036/full
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author Antoine Mallavergne
David Mathiron
Roland Molinié
Jean-Louis Hilbert
David Gagneul
author_facet Antoine Mallavergne
David Mathiron
Roland Molinié
Jean-Louis Hilbert
David Gagneul
author_sort Antoine Mallavergne
collection DOAJ
description Chlorogenic acid (5-CQA) is a caffeic acid ester widely accumulated in higher plants. It plays roles in defense against biotic and abiotic stresses. As its biosynthetic pathway shares common enzymes and intermediates with that of lignin, 5-CQA has long been hypothesized to be involved in lignin formation. However, to date, no plant enzymes have been identified that efficiently convert 5-CQA into lignin precursors. While investigating enzymes involved in the conversion of 5-CQA to isochlorogenic acid (3,5-DiCQA) in chicory (Cichorium intybus), we identified two enzymes from the GDSL esterase/lipase family, CiCQE1 and CiCQE3. Biochemical characterization and functional analysis in tobacco revealed that both enzymes can hydrolyze 5-CQA and 3,5-DiCQA to release caffeic acid (CA) both in vitro and in planta. The genes encoding CiCQE1 and CiCQE3 are predominantly expressed in chicory roots, where 5-CQA and 3,5-DiCQA accumulate to high levels. When transiently expressed in tobacco leaves, accumulation of caffeoyl-putrescine in addition to CA was observed. This may suggest that released CA may be converted to caffeoyl-CoA to fuel other metabolic paths. The hydrolysis of caffeoyl-shikimate, a compound structurally close to 5-CQA, to caffeic acid, and its subsequent conversion to caffeoyl-CoA, has been shown to be an important step in the biosynthesis of G and S monolignols. Since CiCQE1 and CiCQE3 catalyze similar reactions using 5-CQA as substrate, these enzymes may represent a novel route for 5-CQA remobilization in chicory roots. Further functional characterization of the role of these genes using mutant lines is still required to fully understand their role in planta.
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spelling doaj-art-fa186656e2dd41b195fa3cee109377292025-08-20T05:32:54ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2025-08-011610.3389/fpls.2025.16320361632036Identification of the first plant caffeoyl-quinate esterases in Cichorium intybusAntoine Mallavergne0David Mathiron1Roland Molinié2Jean-Louis Hilbert3David Gagneul4Joint Laboratory CHIC41H University of Lille-Florimond-Desprez, Université de Picardie Jules Verne, Université de Liège, Univ. Lille, Junia, UMRT 1158 BioEcoAgro - Specialized Metabolites of Plant Origin, Villeneuve d’Ascq, FranceBIOlogie des Plantes et Innovation (BIOPI), Université de Picardie Jules Verne, Université de Liège, Univ. Lille, Junia, UMRT 1158 BioEcoAgro - Specialized Metabolites of Plant Origin, Amiens, FrancePlateforme Analytique (PFA), Université de Picardie Jules Verne, Amiens, FranceJoint Laboratory CHIC41H University of Lille-Florimond-Desprez, Université de Picardie Jules Verne, Université de Liège, Univ. Lille, Junia, UMRT 1158 BioEcoAgro - Specialized Metabolites of Plant Origin, Villeneuve d’Ascq, FranceJoint Laboratory CHIC41H University of Lille-Florimond-Desprez, Université de Picardie Jules Verne, Université de Liège, Univ. Lille, Junia, UMRT 1158 BioEcoAgro - Specialized Metabolites of Plant Origin, Villeneuve d’Ascq, FranceChlorogenic acid (5-CQA) is a caffeic acid ester widely accumulated in higher plants. It plays roles in defense against biotic and abiotic stresses. As its biosynthetic pathway shares common enzymes and intermediates with that of lignin, 5-CQA has long been hypothesized to be involved in lignin formation. However, to date, no plant enzymes have been identified that efficiently convert 5-CQA into lignin precursors. While investigating enzymes involved in the conversion of 5-CQA to isochlorogenic acid (3,5-DiCQA) in chicory (Cichorium intybus), we identified two enzymes from the GDSL esterase/lipase family, CiCQE1 and CiCQE3. Biochemical characterization and functional analysis in tobacco revealed that both enzymes can hydrolyze 5-CQA and 3,5-DiCQA to release caffeic acid (CA) both in vitro and in planta. The genes encoding CiCQE1 and CiCQE3 are predominantly expressed in chicory roots, where 5-CQA and 3,5-DiCQA accumulate to high levels. When transiently expressed in tobacco leaves, accumulation of caffeoyl-putrescine in addition to CA was observed. This may suggest that released CA may be converted to caffeoyl-CoA to fuel other metabolic paths. The hydrolysis of caffeoyl-shikimate, a compound structurally close to 5-CQA, to caffeic acid, and its subsequent conversion to caffeoyl-CoA, has been shown to be an important step in the biosynthesis of G and S monolignols. Since CiCQE1 and CiCQE3 catalyze similar reactions using 5-CQA as substrate, these enzymes may represent a novel route for 5-CQA remobilization in chicory roots. Further functional characterization of the role of these genes using mutant lines is still required to fully understand their role in planta.https://www.frontiersin.org/articles/10.3389/fpls.2025.1632036/fullchlorogenic acidsGDSLchicorycaffeic acidcaffeoyl-putrescinetobacco
spellingShingle Antoine Mallavergne
David Mathiron
Roland Molinié
Jean-Louis Hilbert
David Gagneul
Identification of the first plant caffeoyl-quinate esterases in Cichorium intybus
Frontiers in Plant Science
chlorogenic acids
GDSL
chicory
caffeic acid
caffeoyl-putrescine
tobacco
title Identification of the first plant caffeoyl-quinate esterases in Cichorium intybus
title_full Identification of the first plant caffeoyl-quinate esterases in Cichorium intybus
title_fullStr Identification of the first plant caffeoyl-quinate esterases in Cichorium intybus
title_full_unstemmed Identification of the first plant caffeoyl-quinate esterases in Cichorium intybus
title_short Identification of the first plant caffeoyl-quinate esterases in Cichorium intybus
title_sort identification of the first plant caffeoyl quinate esterases in cichorium intybus
topic chlorogenic acids
GDSL
chicory
caffeic acid
caffeoyl-putrescine
tobacco
url https://www.frontiersin.org/articles/10.3389/fpls.2025.1632036/full
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AT rolandmolinie identificationofthefirstplantcaffeoylquinateesterasesincichoriumintybus
AT jeanlouishilbert identificationofthefirstplantcaffeoylquinateesterasesincichoriumintybus
AT davidgagneul identificationofthefirstplantcaffeoylquinateesterasesincichoriumintybus