Inhibition of Aminotransferases by Aminoethoxyvinylglycine Triggers a Nitrogen Limitation Condition and Deregulation of Histidine Homeostasis That Impact Root and Shoot Development and Nitrate Uptake

Background and Aims: Although AVG (aminoethoxyvinylglycine) is intensely used to decipher signaling in ethylene/indol-3-acetic acid (IAA) interactions on root morphogenesis, AVG is not a specific inhibitor of aminocyclopropane-1-carboxylate synthase (ACS) and tryptophan aminotransferase (TAA) and tr...

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Main Authors: Erwan Le Deunff, Patrick Beauclair, Carole Deleu, Julien Lecourt
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-11-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fpls.2019.01387/full
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spelling doaj-980f2e13f7714534891758b91669fd592020-11-25T01:55:20ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2019-11-011010.3389/fpls.2019.01387477017Inhibition of Aminotransferases by Aminoethoxyvinylglycine Triggers a Nitrogen Limitation Condition and Deregulation of Histidine Homeostasis That Impact Root and Shoot Development and Nitrate UptakeErwan Le Deunff0Patrick Beauclair1Carole Deleu2Julien Lecourt3Normandie Université, UNICAEN, SF ICORE 4206, Caen, FranceINRA Unité Expérimentale Fourrages Environnement Ruminants (FERLUS) et Système d’Observation et d’Expérimentation pour la Recherche en Environnement (SOERE), Les Verrines CS 80006, Lusignan, FranceINRA—Agrocampus Ouest—Université de Rennes 1, UMR 1349 Institut de Génétique, Environnement et Protection des Plantes (IGEPP) Université de Rennes 1, Rennes, FranceNIAB EMR, Crop Science and Production Systems New Road, East Malling, United KingdomBackground and Aims: Although AVG (aminoethoxyvinylglycine) is intensely used to decipher signaling in ethylene/indol-3-acetic acid (IAA) interactions on root morphogenesis, AVG is not a specific inhibitor of aminocyclopropane-1-carboxylate synthase (ACS) and tryptophan aminotransferase (TAA) and tryptophan aminotransferase related (TAR) activities since it is able to inhibit several aminotransferases involved in N metabolism. Indeed, 1 mM glutamate (Glu) supply to the roots in plants treated with 10 μM AVG partially restores the root growth. Here, we highlight the changes induced by AVG and AVG + Glu treatments on the N metabolism impairment and root morphogenetic program.Methods: Root nitrate uptake induced by AVG and AVG + Glu treatments was measured by a differential labeling with 15NO3- and 15Nglutamate. In parallel a profiling of amino acids (AA) was performed to decipher the impairment of AA metabolism.Key Results: 10 μM AVG treatment increases K15NO3 uptake and 15N translocation during root growth inhibition whereas 10 μM AVG + 1 mM 15Nglutamate treatment inhibits K15NO3 uptake and increases 15Nglutamate uptake during partial root growth restoration. This is explained by a nitrogen (N) limitation condition induced by AVG treatment and a N excess condition induced by AVG + Glu treatment. AA levels were mainly impaired by AVG treatment in roots, where levels of Ser, Thr, α-Ala, β-Ala, Val, Asn and His were significantly increased. His was the only amino acid for which no restoration was observed in roots and shoots after glutamate treatment suggesting important control of His homeostasis on aminotransferase network. Results were discussed in light of recent findings on the interconnection between His homeostasis and the general amino acid control system (GAAC) in eukaryotes.Conclusions: These results demonstrate that AVG concentration above 5 μM is a powerful pharmacological tool for unraveling the involvement of GAAC system or new N sensory system in morphological and metabolic changes of the roots in leguminous and non-leguminous plants.https://www.frontiersin.org/article/10.3389/fpls.2019.01387/fullAminoethoxyvinylglycinetryptophan aminotransferasehistidine catabolismaminocyclopropane-1-carboxylate synthaseBrassica napusnitrate uptake
collection DOAJ
language English
format Article
sources DOAJ
author Erwan Le Deunff
Patrick Beauclair
Carole Deleu
Julien Lecourt
spellingShingle Erwan Le Deunff
Patrick Beauclair
Carole Deleu
Julien Lecourt
Inhibition of Aminotransferases by Aminoethoxyvinylglycine Triggers a Nitrogen Limitation Condition and Deregulation of Histidine Homeostasis That Impact Root and Shoot Development and Nitrate Uptake
Frontiers in Plant Science
Aminoethoxyvinylglycine
tryptophan aminotransferase
histidine catabolism
aminocyclopropane-1-carboxylate synthase
Brassica napus
nitrate uptake
author_facet Erwan Le Deunff
Patrick Beauclair
Carole Deleu
Julien Lecourt
author_sort Erwan Le Deunff
title Inhibition of Aminotransferases by Aminoethoxyvinylglycine Triggers a Nitrogen Limitation Condition and Deregulation of Histidine Homeostasis That Impact Root and Shoot Development and Nitrate Uptake
title_short Inhibition of Aminotransferases by Aminoethoxyvinylglycine Triggers a Nitrogen Limitation Condition and Deregulation of Histidine Homeostasis That Impact Root and Shoot Development and Nitrate Uptake
title_full Inhibition of Aminotransferases by Aminoethoxyvinylglycine Triggers a Nitrogen Limitation Condition and Deregulation of Histidine Homeostasis That Impact Root and Shoot Development and Nitrate Uptake
title_fullStr Inhibition of Aminotransferases by Aminoethoxyvinylglycine Triggers a Nitrogen Limitation Condition and Deregulation of Histidine Homeostasis That Impact Root and Shoot Development and Nitrate Uptake
title_full_unstemmed Inhibition of Aminotransferases by Aminoethoxyvinylglycine Triggers a Nitrogen Limitation Condition and Deregulation of Histidine Homeostasis That Impact Root and Shoot Development and Nitrate Uptake
title_sort inhibition of aminotransferases by aminoethoxyvinylglycine triggers a nitrogen limitation condition and deregulation of histidine homeostasis that impact root and shoot development and nitrate uptake
publisher Frontiers Media S.A.
series Frontiers in Plant Science
issn 1664-462X
publishDate 2019-11-01
description Background and Aims: Although AVG (aminoethoxyvinylglycine) is intensely used to decipher signaling in ethylene/indol-3-acetic acid (IAA) interactions on root morphogenesis, AVG is not a specific inhibitor of aminocyclopropane-1-carboxylate synthase (ACS) and tryptophan aminotransferase (TAA) and tryptophan aminotransferase related (TAR) activities since it is able to inhibit several aminotransferases involved in N metabolism. Indeed, 1 mM glutamate (Glu) supply to the roots in plants treated with 10 μM AVG partially restores the root growth. Here, we highlight the changes induced by AVG and AVG + Glu treatments on the N metabolism impairment and root morphogenetic program.Methods: Root nitrate uptake induced by AVG and AVG + Glu treatments was measured by a differential labeling with 15NO3- and 15Nglutamate. In parallel a profiling of amino acids (AA) was performed to decipher the impairment of AA metabolism.Key Results: 10 μM AVG treatment increases K15NO3 uptake and 15N translocation during root growth inhibition whereas 10 μM AVG + 1 mM 15Nglutamate treatment inhibits K15NO3 uptake and increases 15Nglutamate uptake during partial root growth restoration. This is explained by a nitrogen (N) limitation condition induced by AVG treatment and a N excess condition induced by AVG + Glu treatment. AA levels were mainly impaired by AVG treatment in roots, where levels of Ser, Thr, α-Ala, β-Ala, Val, Asn and His were significantly increased. His was the only amino acid for which no restoration was observed in roots and shoots after glutamate treatment suggesting important control of His homeostasis on aminotransferase network. Results were discussed in light of recent findings on the interconnection between His homeostasis and the general amino acid control system (GAAC) in eukaryotes.Conclusions: These results demonstrate that AVG concentration above 5 μM is a powerful pharmacological tool for unraveling the involvement of GAAC system or new N sensory system in morphological and metabolic changes of the roots in leguminous and non-leguminous plants.
topic Aminoethoxyvinylglycine
tryptophan aminotransferase
histidine catabolism
aminocyclopropane-1-carboxylate synthase
Brassica napus
nitrate uptake
url https://www.frontiersin.org/article/10.3389/fpls.2019.01387/full
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