A Multi-Species Analysis Defines Anaplerotic Enzymes and Amides as Metabolic Markers for Ammonium Nutrition

Nitrate and ammonium are the main nitrogen sources in agricultural soils. In the last decade, ammonium (NH4+), a double-sided metabolite, has attracted considerable attention by researchers. Its ubiquitous presence in plant metabolism and its metabolic energy economy for being assimilated contrast w...

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Autores: González Moro, María Begoña, González Moro, Itziar, De la Peña Cuao, Marlon, Estavillo Aurre, José María, Aparicio Tejo, Pedro M., Marino Bilbao, Daniel, González Murua, María del Carmen Begoña, Vega Mas, Izargi Aida
Tipo de recurso: artículo
Fecha de publicación:2021
País:España
Institución:Universidad del País Vasco
Repositorio:Addi. Archivo Digital para la Docencia y la Investigación
OAI Identifier:oai:addi.ehu.eus:10810/50604
Acceso en línea:http://hdl.handle.net/10810/50604
Access Level:acceso abierto
Palabra clave:ammonium
amino acid
glutamate dehydrogenase
glutamine synthease
isocitrate dehydrogenase
malic enzyme
phosphoenolpyruvate carboxylase
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spelling A Multi-Species Analysis Defines Anaplerotic Enzymes and Amides as Metabolic Markers for Ammonium NutritionGonzález Moro, María BegoñaGonzález Moro, ItziarDe la Peña Cuao, MarlonEstavillo Aurre, José MaríaAparicio Tejo, Pedro M.Marino Bilbao, DanielGonzález Murua, María del Carmen BegoñaVega Mas, Izargi Aidaammoniumamino acidglutamate dehydrogenaseglutamine syntheaseisocitrate dehydrogenasemalic enzymephosphoenolpyruvate carboxylaseNitrate and ammonium are the main nitrogen sources in agricultural soils. In the last decade, ammonium (NH4+), a double-sided metabolite, has attracted considerable attention by researchers. Its ubiquitous presence in plant metabolism and its metabolic energy economy for being assimilated contrast with its toxicity when present in high amounts in the external medium. Plant species can adopt different strategies to maintain NH4+ homeostasis, as the maximization of its compartmentalization and assimilation in organic compounds, primarily as amino acids and proteins. In the present study, we report an integrative metabolic response to ammonium nutrition of seven plant species, belonging to four different families: Gramineae (ryegrass, wheat, Brachypodium distachyon), Leguminosae (clover), Solanaceae (tomato), and Brassicaceae (oilseed rape, Arabidopsis thaliana). We use principal component analysis (PCA) and correlations among metabolic and biochemical data from 40 experimental conditions to understand the whole-plant response. The nature of main amino acids is analyzed among species, under the hypothesis that those Asn-accumulating species will show a better response to ammonium nutrition. Given the provision of carbon (C) skeletons is crucial for promotion of the nitrogen assimilation, the role of different anaplerotic enzymes is discussed in relation to ammonium nutrition at a whole-plant level. Among these enzymes, isocitrate dehydrogenase (ICDH) shows to be a good candidate to increase nitrogen assimilation in plants. Overall, metabolic adaptation of different carbon anaplerotic activities is linked with the preference to synthesize Asn or Gln in their organs. Lastly, glutamate dehydrogenase (GDH) reveals as an important enzyme to surpass C limitation during ammonium assimilation in roots, with a disparate collaboration of glutamine synthetase (GS).The design of the study, analysis, and interpretation of data and writing of the manuscript was supported by the Basque Government [IT932-16] or GIC15/179, the Spanish Ministry of Economy and Competitiveness [AGL2015-64582-C3-2-R] and [BIO2017-84035-R]. IVM held a postdoctoral grant from the Basque Government (conv. 2018) and MDLP held a PhD grant by COLCIENCIAS (conv. 672).Frontiers Media202120212021info:eu-repo/semantics/articleapplication/pdfhttp://hdl.handle.net/10810/50604reponame:Addi. Archivo Digital para la Docencia y la Investigacióninstname:Universidad del País VascoInglésinfo:eu-repo/grantAgreement/MINECO/AGL2015-64582-C3-2-R/info:eu-repo/grantAgreement/MINECO/BIO2017-84035-R/https://www.frontiersin.org/articles/10.3389/fpls.2020.632285/fullinfo:eu-repo/semantics/openAccesshttp://creativecommons.org/licenses/by/3.0/es/2021 González-Moro, González-Moro, de la Peña, Estavillo, Aparicio-Tejo, Marino, González-Murua and Vega-Mas. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.Atribución 3.0 Españaoai:addi.ehu.eus:10810/506042026-06-18T09:23:17Z
dc.title.none.fl_str_mv A Multi-Species Analysis Defines Anaplerotic Enzymes and Amides as Metabolic Markers for Ammonium Nutrition
title A Multi-Species Analysis Defines Anaplerotic Enzymes and Amides as Metabolic Markers for Ammonium Nutrition
spellingShingle A Multi-Species Analysis Defines Anaplerotic Enzymes and Amides as Metabolic Markers for Ammonium Nutrition
González Moro, María Begoña
ammonium
amino acid
glutamate dehydrogenase
glutamine synthease
isocitrate dehydrogenase
malic enzyme
phosphoenolpyruvate carboxylase
title_short A Multi-Species Analysis Defines Anaplerotic Enzymes and Amides as Metabolic Markers for Ammonium Nutrition
title_full A Multi-Species Analysis Defines Anaplerotic Enzymes and Amides as Metabolic Markers for Ammonium Nutrition
title_fullStr A Multi-Species Analysis Defines Anaplerotic Enzymes and Amides as Metabolic Markers for Ammonium Nutrition
title_full_unstemmed A Multi-Species Analysis Defines Anaplerotic Enzymes and Amides as Metabolic Markers for Ammonium Nutrition
title_sort A Multi-Species Analysis Defines Anaplerotic Enzymes and Amides as Metabolic Markers for Ammonium Nutrition
dc.creator.none.fl_str_mv González Moro, María Begoña
González Moro, Itziar
De la Peña Cuao, Marlon
Estavillo Aurre, José María
Aparicio Tejo, Pedro M.
Marino Bilbao, Daniel
González Murua, María del Carmen Begoña
Vega Mas, Izargi Aida
author González Moro, María Begoña
author_facet González Moro, María Begoña
González Moro, Itziar
De la Peña Cuao, Marlon
Estavillo Aurre, José María
Aparicio Tejo, Pedro M.
Marino Bilbao, Daniel
González Murua, María del Carmen Begoña
Vega Mas, Izargi Aida
author_role author
author2 González Moro, Itziar
De la Peña Cuao, Marlon
Estavillo Aurre, José María
Aparicio Tejo, Pedro M.
Marino Bilbao, Daniel
González Murua, María del Carmen Begoña
Vega Mas, Izargi Aida
author2_role author
author
author
author
author
author
author
dc.subject.none.fl_str_mv ammonium
amino acid
glutamate dehydrogenase
glutamine synthease
isocitrate dehydrogenase
malic enzyme
phosphoenolpyruvate carboxylase
topic ammonium
amino acid
glutamate dehydrogenase
glutamine synthease
isocitrate dehydrogenase
malic enzyme
phosphoenolpyruvate carboxylase
description Nitrate and ammonium are the main nitrogen sources in agricultural soils. In the last decade, ammonium (NH4+), a double-sided metabolite, has attracted considerable attention by researchers. Its ubiquitous presence in plant metabolism and its metabolic energy economy for being assimilated contrast with its toxicity when present in high amounts in the external medium. Plant species can adopt different strategies to maintain NH4+ homeostasis, as the maximization of its compartmentalization and assimilation in organic compounds, primarily as amino acids and proteins. In the present study, we report an integrative metabolic response to ammonium nutrition of seven plant species, belonging to four different families: Gramineae (ryegrass, wheat, Brachypodium distachyon), Leguminosae (clover), Solanaceae (tomato), and Brassicaceae (oilseed rape, Arabidopsis thaliana). We use principal component analysis (PCA) and correlations among metabolic and biochemical data from 40 experimental conditions to understand the whole-plant response. The nature of main amino acids is analyzed among species, under the hypothesis that those Asn-accumulating species will show a better response to ammonium nutrition. Given the provision of carbon (C) skeletons is crucial for promotion of the nitrogen assimilation, the role of different anaplerotic enzymes is discussed in relation to ammonium nutrition at a whole-plant level. Among these enzymes, isocitrate dehydrogenase (ICDH) shows to be a good candidate to increase nitrogen assimilation in plants. Overall, metabolic adaptation of different carbon anaplerotic activities is linked with the preference to synthesize Asn or Gln in their organs. Lastly, glutamate dehydrogenase (GDH) reveals as an important enzyme to surpass C limitation during ammonium assimilation in roots, with a disparate collaboration of glutamine synthetase (GS).
publishDate 2021
dc.date.none.fl_str_mv 2021
2021
2021
dc.type.none.fl_str_mv info:eu-repo/semantics/article
format article
dc.identifier.none.fl_str_mv http://hdl.handle.net/10810/50604
url http://hdl.handle.net/10810/50604
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv info:eu-repo/grantAgreement/MINECO/AGL2015-64582-C3-2-R/
info:eu-repo/grantAgreement/MINECO/BIO2017-84035-R/
https://www.frontiersin.org/articles/10.3389/fpls.2020.632285/full
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
http://creativecommons.org/licenses/by/3.0/es/
Atribución 3.0 España
eu_rights_str_mv openAccess
rights_invalid_str_mv http://creativecommons.org/licenses/by/3.0/es/
Atribución 3.0 España
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv Frontiers Media
publisher.none.fl_str_mv Frontiers Media
dc.source.none.fl_str_mv reponame:Addi. Archivo Digital para la Docencia y la Investigación
instname:Universidad del País Vasco
instname_str Universidad del País Vasco
reponame_str Addi. Archivo Digital para la Docencia y la Investigación
collection Addi. Archivo Digital para la Docencia y la Investigación
repository.name.fl_str_mv
repository.mail.fl_str_mv
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