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Genes for asparagine metabolism in Lotus japonicus: differential expression and interconnection with photorespiration

BACKGROUND: Asparagine is a very important nitrogen transport and storage compound in plants due to its high nitrogen/carbon ratio and stability. Asparagine intracellular concentration depends on a balance between asparagine biosynthesis and degradation. The main enzymes involved in asparagine metab...

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Autores principales: García-Calderón, Margarita, Pérez-Delgado, Carmen M., Credali, Alfredo, Vega, José M., Betti, Marco, Márquez, Antonio J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5639745/
https://www.ncbi.nlm.nih.gov/pubmed/29025409
http://dx.doi.org/10.1186/s12864-017-4200-x
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author García-Calderón, Margarita
Pérez-Delgado, Carmen M.
Credali, Alfredo
Vega, José M.
Betti, Marco
Márquez, Antonio J.
author_facet García-Calderón, Margarita
Pérez-Delgado, Carmen M.
Credali, Alfredo
Vega, José M.
Betti, Marco
Márquez, Antonio J.
author_sort García-Calderón, Margarita
collection PubMed
description BACKGROUND: Asparagine is a very important nitrogen transport and storage compound in plants due to its high nitrogen/carbon ratio and stability. Asparagine intracellular concentration depends on a balance between asparagine biosynthesis and degradation. The main enzymes involved in asparagine metabolism are asparagine synthetase (ASN), asparaginase (NSE) and serine-glyoxylate aminotransferase (SGAT). The study of the genes encoding for these enzymes in the model legume Lotus japonicus is of particular interest since it has been proposed that asparagine is the principal molecule used to transport reduced nitrogen within the plant in most temperate legumes. RESULTS: A differential expression of genes encoding for several enzymes involved in asparagine metabolism was detected in L. japonicus. ASN is encoded by three genes, LjASN1 was the most highly expressed in mature leaves while LjASN2 expression was negligible and LjASN3 showed a low expression in this organ, suggesting that LjASN1 is the main gene responsible for asparagine synthesis in mature leaves. In young leaves, LjASN3 was the only ASN gene expressed although at low levels, while all the three genes encoding for NSE were highly expressed, especially LjNSE1. In nodules, LjASN2 and LjNSE2 were the most highly expressed genes, suggesting an important role for these genes in this organ. Several lines of evidence support the connection between asparagine metabolic genes and photorespiration in L. japonicus: a) a mutant plant deficient in LjNSE1 showed a dramatic decrease in the expression of the two genes encoding for SGAT; b) expression of the genes involved in asparagine metabolism is altered in a photorespiratory mutant lacking plastidic glutamine synthetase; c) a clustering analysis indicated a similar pattern of expression among several genes involved in photorespiratory and asparagine metabolism, indicating a clear link between LjASN1 and LjSGAT genes and photorespiration. CONCLUSIONS: The results obtained in this paper indicate the existence of a differential expression of asparagine metabolic genes in L. japonicus and point out the crucial relevance of particular genes in different organs. Moreover, the data presented establish clear links between asparagine and photorespiratory metabolic genes in this plant. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-017-4200-x) contains supplementary material, which is available to authorized users.
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spelling pubmed-56397452017-10-18 Genes for asparagine metabolism in Lotus japonicus: differential expression and interconnection with photorespiration García-Calderón, Margarita Pérez-Delgado, Carmen M. Credali, Alfredo Vega, José M. Betti, Marco Márquez, Antonio J. BMC Genomics Research Article BACKGROUND: Asparagine is a very important nitrogen transport and storage compound in plants due to its high nitrogen/carbon ratio and stability. Asparagine intracellular concentration depends on a balance between asparagine biosynthesis and degradation. The main enzymes involved in asparagine metabolism are asparagine synthetase (ASN), asparaginase (NSE) and serine-glyoxylate aminotransferase (SGAT). The study of the genes encoding for these enzymes in the model legume Lotus japonicus is of particular interest since it has been proposed that asparagine is the principal molecule used to transport reduced nitrogen within the plant in most temperate legumes. RESULTS: A differential expression of genes encoding for several enzymes involved in asparagine metabolism was detected in L. japonicus. ASN is encoded by three genes, LjASN1 was the most highly expressed in mature leaves while LjASN2 expression was negligible and LjASN3 showed a low expression in this organ, suggesting that LjASN1 is the main gene responsible for asparagine synthesis in mature leaves. In young leaves, LjASN3 was the only ASN gene expressed although at low levels, while all the three genes encoding for NSE were highly expressed, especially LjNSE1. In nodules, LjASN2 and LjNSE2 were the most highly expressed genes, suggesting an important role for these genes in this organ. Several lines of evidence support the connection between asparagine metabolic genes and photorespiration in L. japonicus: a) a mutant plant deficient in LjNSE1 showed a dramatic decrease in the expression of the two genes encoding for SGAT; b) expression of the genes involved in asparagine metabolism is altered in a photorespiratory mutant lacking plastidic glutamine synthetase; c) a clustering analysis indicated a similar pattern of expression among several genes involved in photorespiratory and asparagine metabolism, indicating a clear link between LjASN1 and LjSGAT genes and photorespiration. CONCLUSIONS: The results obtained in this paper indicate the existence of a differential expression of asparagine metabolic genes in L. japonicus and point out the crucial relevance of particular genes in different organs. Moreover, the data presented establish clear links between asparagine and photorespiratory metabolic genes in this plant. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-017-4200-x) contains supplementary material, which is available to authorized users. BioMed Central 2017-10-12 /pmc/articles/PMC5639745/ /pubmed/29025409 http://dx.doi.org/10.1186/s12864-017-4200-x Text en © The Author(s). 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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
García-Calderón, Margarita
Pérez-Delgado, Carmen M.
Credali, Alfredo
Vega, José M.
Betti, Marco
Márquez, Antonio J.
Genes for asparagine metabolism in Lotus japonicus: differential expression and interconnection with photorespiration
title Genes for asparagine metabolism in Lotus japonicus: differential expression and interconnection with photorespiration
title_full Genes for asparagine metabolism in Lotus japonicus: differential expression and interconnection with photorespiration
title_fullStr Genes for asparagine metabolism in Lotus japonicus: differential expression and interconnection with photorespiration
title_full_unstemmed Genes for asparagine metabolism in Lotus japonicus: differential expression and interconnection with photorespiration
title_short Genes for asparagine metabolism in Lotus japonicus: differential expression and interconnection with photorespiration
title_sort genes for asparagine metabolism in lotus japonicus: differential expression and interconnection with photorespiration
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5639745/
https://www.ncbi.nlm.nih.gov/pubmed/29025409
http://dx.doi.org/10.1186/s12864-017-4200-x
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