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Mineral nitrogen sources differently affect root glutamine synthetase isoforms and amino acid balance among organs in maize

BACKGROUND: Glutamine synthetase (GS) catalyzes the first step of nitrogen assimilation in plant cell. The main GS are classified as cytosolic GS1 and plastidial GS2, of which the functionality is variable according to the nitrogen sources, organs and developmental stages. In maize (Zea mays L.) one...

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Autores principales: Prinsi, Bhakti, Espen, Luca
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4393875/
https://www.ncbi.nlm.nih.gov/pubmed/25886826
http://dx.doi.org/10.1186/s12870-015-0482-9
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author Prinsi, Bhakti
Espen, Luca
author_facet Prinsi, Bhakti
Espen, Luca
author_sort Prinsi, Bhakti
collection PubMed
description BACKGROUND: Glutamine synthetase (GS) catalyzes the first step of nitrogen assimilation in plant cell. The main GS are classified as cytosolic GS1 and plastidial GS2, of which the functionality is variable according to the nitrogen sources, organs and developmental stages. In maize (Zea mays L.) one gene for GS2 and five genes for GS1 subunits are known, but their roles in root metabolism are not yet well defined. In this work, proteomic and biochemical approaches have been used to study root GS enzymes and nitrogen assimilation in maize plants re-supplied with nitrate, ammonium or both. RESULTS: The plant metabolic status highlighted the relevance of root system in maize nitrogen assimilation during both nitrate and ammonium nutrition. The analysis of root proteomes allowed a study to be made of the accumulation and phosphorylation of six GS proteins. Three forms of GS2 were identified, among which only the phosphorylated one showed an accumulation trend consistent with plastidial GS activity. Nitrogen availabilities enabled increments in root total GS synthetase activity, associated with different GS1 isoforms according to the nitrogen sources. Nitrate nutrition induced the specific accumulation of GS1-5 while ammonium led to up-accumulation of both GS1-1 and GS1-5, highlighting co-participation. Moreover, the changes in thermal sensitivity of root GS transferase activity suggested differential rearrangements of the native enzyme. The amino acid accumulation and composition in roots, xylem sap and leaves deeply changed in response to mineral sources. Glutamine showed the prevalent changes in all nitrogen nutritions. Besides, the ammonium nutrition was associated with an accumulation of asparagine and reducing sugars and a drop in glutamic acid level, significantly alleviated by the co-provision with nitrate. CONCLUSION: This work provides new information about the multifaceted regulation of the GS enzyme in maize roots, indicating the involvement of specific isoenzymes/isoforms, post-translational events and biochemical factors. For the first time, the proteomic approach allowed to discriminate the individual contribution of the GS1 isoforms, highlighting the participation of GS1-5 in nitrate metabolism. Moreover, the results give new insights about the influence of amino acid metabolism in plant C/N balance. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12870-015-0482-9) contains supplementary material, which is available to authorized users.
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spelling pubmed-43938752015-04-13 Mineral nitrogen sources differently affect root glutamine synthetase isoforms and amino acid balance among organs in maize Prinsi, Bhakti Espen, Luca BMC Plant Biol Research Article BACKGROUND: Glutamine synthetase (GS) catalyzes the first step of nitrogen assimilation in plant cell. The main GS are classified as cytosolic GS1 and plastidial GS2, of which the functionality is variable according to the nitrogen sources, organs and developmental stages. In maize (Zea mays L.) one gene for GS2 and five genes for GS1 subunits are known, but their roles in root metabolism are not yet well defined. In this work, proteomic and biochemical approaches have been used to study root GS enzymes and nitrogen assimilation in maize plants re-supplied with nitrate, ammonium or both. RESULTS: The plant metabolic status highlighted the relevance of root system in maize nitrogen assimilation during both nitrate and ammonium nutrition. The analysis of root proteomes allowed a study to be made of the accumulation and phosphorylation of six GS proteins. Three forms of GS2 were identified, among which only the phosphorylated one showed an accumulation trend consistent with plastidial GS activity. Nitrogen availabilities enabled increments in root total GS synthetase activity, associated with different GS1 isoforms according to the nitrogen sources. Nitrate nutrition induced the specific accumulation of GS1-5 while ammonium led to up-accumulation of both GS1-1 and GS1-5, highlighting co-participation. Moreover, the changes in thermal sensitivity of root GS transferase activity suggested differential rearrangements of the native enzyme. The amino acid accumulation and composition in roots, xylem sap and leaves deeply changed in response to mineral sources. Glutamine showed the prevalent changes in all nitrogen nutritions. Besides, the ammonium nutrition was associated with an accumulation of asparagine and reducing sugars and a drop in glutamic acid level, significantly alleviated by the co-provision with nitrate. CONCLUSION: This work provides new information about the multifaceted regulation of the GS enzyme in maize roots, indicating the involvement of specific isoenzymes/isoforms, post-translational events and biochemical factors. For the first time, the proteomic approach allowed to discriminate the individual contribution of the GS1 isoforms, highlighting the participation of GS1-5 in nitrate metabolism. Moreover, the results give new insights about the influence of amino acid metabolism in plant C/N balance. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12870-015-0482-9) contains supplementary material, which is available to authorized users. BioMed Central 2015-04-03 /pmc/articles/PMC4393875/ /pubmed/25886826 http://dx.doi.org/10.1186/s12870-015-0482-9 Text en © Prinsi and Espen; licensee BioMed Central. 2015 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Prinsi, Bhakti
Espen, Luca
Mineral nitrogen sources differently affect root glutamine synthetase isoforms and amino acid balance among organs in maize
title Mineral nitrogen sources differently affect root glutamine synthetase isoforms and amino acid balance among organs in maize
title_full Mineral nitrogen sources differently affect root glutamine synthetase isoforms and amino acid balance among organs in maize
title_fullStr Mineral nitrogen sources differently affect root glutamine synthetase isoforms and amino acid balance among organs in maize
title_full_unstemmed Mineral nitrogen sources differently affect root glutamine synthetase isoforms and amino acid balance among organs in maize
title_short Mineral nitrogen sources differently affect root glutamine synthetase isoforms and amino acid balance among organs in maize
title_sort mineral nitrogen sources differently affect root glutamine synthetase isoforms and amino acid balance among organs in maize
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4393875/
https://www.ncbi.nlm.nih.gov/pubmed/25886826
http://dx.doi.org/10.1186/s12870-015-0482-9
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