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Metabolic diversification of nitrogen‐containing metabolites by the expression of a heterologous lysine decarboxylase gene in Arabidopsis

Lysine decarboxylase converts l‐lysine to cadaverine as a branching point for the biosynthesis of plant Lys‐derived alkaloids. Although cadaverine contributes towards the biosynthesis of Lys‐derived alkaloids, its catabolism, including metabolic intermediates and the enzymes involved, is not known....

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Autores principales: Shimizu, Yohei, Rai, Amit, Okawa, Yuko, Tomatsu, Hajime, Sato, Masaru, Kera, Kota, Suzuki, Hideyuki, Saito, Kazuki, Yamazaki, Mami
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6899585/
https://www.ncbi.nlm.nih.gov/pubmed/31364191
http://dx.doi.org/10.1111/tpj.14454
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author Shimizu, Yohei
Rai, Amit
Okawa, Yuko
Tomatsu, Hajime
Sato, Masaru
Kera, Kota
Suzuki, Hideyuki
Saito, Kazuki
Yamazaki, Mami
author_facet Shimizu, Yohei
Rai, Amit
Okawa, Yuko
Tomatsu, Hajime
Sato, Masaru
Kera, Kota
Suzuki, Hideyuki
Saito, Kazuki
Yamazaki, Mami
author_sort Shimizu, Yohei
collection PubMed
description Lysine decarboxylase converts l‐lysine to cadaverine as a branching point for the biosynthesis of plant Lys‐derived alkaloids. Although cadaverine contributes towards the biosynthesis of Lys‐derived alkaloids, its catabolism, including metabolic intermediates and the enzymes involved, is not known. Here, we generated transgenic Arabidopsis lines by expressing an exogenous lysine/ornithine decarboxylase gene from Lupinus angustifolius (La‐L/ODC) and identified cadaverine‐derived metabolites as the products of the emerged biosynthetic pathway. Through untargeted metabolic profiling, we observed the upregulation of polyamine metabolism, phenylpropanoid biosynthesis and the biosynthesis of several Lys‐derived alkaloids in the transgenic lines. Moreover, we found several cadaverine‐derived metabolites specifically detected in the transgenic lines compared with the non‐transformed control. Among these, three specific metabolites were identified and confirmed as 5‐aminopentanal, 5‐aminopentanoate and δ‐valerolactam. Cadaverine catabolism in a representative transgenic line (DC29) was traced by feeding stable isotope‐labeled [α‐(15)N]‐ or [ε‐(15)N]‐l‐lysine. Our results show similar (15)N incorporation ratios from both isotopomers for the specific metabolite features identified, indicating that these metabolites were synthesized via the symmetric structure of cadaverine. We propose biosynthetic pathways for the metabolites on the basis of metabolite chemistry and enzymes known or identified through catalyzing specific biochemical reactions in this study. Our study shows that this pool of enzymes with promiscuous activities is the driving force for metabolite diversification in plants. Thus, this study not only provides valuable information for understanding the catabolic mechanism of cadaverine but also demonstrates that cadaverine accumulation is one of the factors to expand plant chemodiversity, which may lead to the emergence of Lys‐derived alkaloid biosynthesis.
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spelling pubmed-68995852019-12-19 Metabolic diversification of nitrogen‐containing metabolites by the expression of a heterologous lysine decarboxylase gene in Arabidopsis Shimizu, Yohei Rai, Amit Okawa, Yuko Tomatsu, Hajime Sato, Masaru Kera, Kota Suzuki, Hideyuki Saito, Kazuki Yamazaki, Mami Plant J Original Articles Lysine decarboxylase converts l‐lysine to cadaverine as a branching point for the biosynthesis of plant Lys‐derived alkaloids. Although cadaverine contributes towards the biosynthesis of Lys‐derived alkaloids, its catabolism, including metabolic intermediates and the enzymes involved, is not known. Here, we generated transgenic Arabidopsis lines by expressing an exogenous lysine/ornithine decarboxylase gene from Lupinus angustifolius (La‐L/ODC) and identified cadaverine‐derived metabolites as the products of the emerged biosynthetic pathway. Through untargeted metabolic profiling, we observed the upregulation of polyamine metabolism, phenylpropanoid biosynthesis and the biosynthesis of several Lys‐derived alkaloids in the transgenic lines. Moreover, we found several cadaverine‐derived metabolites specifically detected in the transgenic lines compared with the non‐transformed control. Among these, three specific metabolites were identified and confirmed as 5‐aminopentanal, 5‐aminopentanoate and δ‐valerolactam. Cadaverine catabolism in a representative transgenic line (DC29) was traced by feeding stable isotope‐labeled [α‐(15)N]‐ or [ε‐(15)N]‐l‐lysine. Our results show similar (15)N incorporation ratios from both isotopomers for the specific metabolite features identified, indicating that these metabolites were synthesized via the symmetric structure of cadaverine. We propose biosynthetic pathways for the metabolites on the basis of metabolite chemistry and enzymes known or identified through catalyzing specific biochemical reactions in this study. Our study shows that this pool of enzymes with promiscuous activities is the driving force for metabolite diversification in plants. Thus, this study not only provides valuable information for understanding the catabolic mechanism of cadaverine but also demonstrates that cadaverine accumulation is one of the factors to expand plant chemodiversity, which may lead to the emergence of Lys‐derived alkaloid biosynthesis. John Wiley and Sons Inc. 2019-08-27 2019-11 /pmc/articles/PMC6899585/ /pubmed/31364191 http://dx.doi.org/10.1111/tpj.14454 Text en © 2019 The Authors The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Articles
Shimizu, Yohei
Rai, Amit
Okawa, Yuko
Tomatsu, Hajime
Sato, Masaru
Kera, Kota
Suzuki, Hideyuki
Saito, Kazuki
Yamazaki, Mami
Metabolic diversification of nitrogen‐containing metabolites by the expression of a heterologous lysine decarboxylase gene in Arabidopsis
title Metabolic diversification of nitrogen‐containing metabolites by the expression of a heterologous lysine decarboxylase gene in Arabidopsis
title_full Metabolic diversification of nitrogen‐containing metabolites by the expression of a heterologous lysine decarboxylase gene in Arabidopsis
title_fullStr Metabolic diversification of nitrogen‐containing metabolites by the expression of a heterologous lysine decarboxylase gene in Arabidopsis
title_full_unstemmed Metabolic diversification of nitrogen‐containing metabolites by the expression of a heterologous lysine decarboxylase gene in Arabidopsis
title_short Metabolic diversification of nitrogen‐containing metabolites by the expression of a heterologous lysine decarboxylase gene in Arabidopsis
title_sort metabolic diversification of nitrogen‐containing metabolites by the expression of a heterologous lysine decarboxylase gene in arabidopsis
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6899585/
https://www.ncbi.nlm.nih.gov/pubmed/31364191
http://dx.doi.org/10.1111/tpj.14454
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