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Metabolome analysis of 20 taxonomically related benzylisoquinoline alkaloid-producing plants

BACKGROUND: Recent progress toward the elucidation of benzylisoquinoline alkaloid (BIA) metabolism has focused on a small number of model plant species. Current understanding of BIA metabolism in plants such as opium poppy, which accumulates important pharmacological agents such as codeine and morph...

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Autores principales: Hagel, Jillian M., Mandal, Rupasri, Han, Beomsoo, Han, Jun, Dinsmore, Donald R., Borchers, Christoph H., Wishart, David S., Facchini, Peter J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4570626/
https://www.ncbi.nlm.nih.gov/pubmed/26369413
http://dx.doi.org/10.1186/s12870-015-0594-2
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author Hagel, Jillian M.
Mandal, Rupasri
Han, Beomsoo
Han, Jun
Dinsmore, Donald R.
Borchers, Christoph H.
Wishart, David S.
Facchini, Peter J.
author_facet Hagel, Jillian M.
Mandal, Rupasri
Han, Beomsoo
Han, Jun
Dinsmore, Donald R.
Borchers, Christoph H.
Wishart, David S.
Facchini, Peter J.
author_sort Hagel, Jillian M.
collection PubMed
description BACKGROUND: Recent progress toward the elucidation of benzylisoquinoline alkaloid (BIA) metabolism has focused on a small number of model plant species. Current understanding of BIA metabolism in plants such as opium poppy, which accumulates important pharmacological agents such as codeine and morphine, has relied on a combination of genomics and metabolomics to facilitate gene discovery. Metabolomics studies provide important insight into the primary biochemical networks underpinning specialized metabolism, and serve as a key resource for metabolic engineering, gene discovery, and elucidation of governing regulatory mechanisms. Beyond model plants, few broad-scope metabolomics reports are available for the vast number of plant species known to produce an estimated 2500 structurally diverse BIAs, many of which exhibit promising medicinal properties. RESULTS: We applied a multi-platform approach incorporating four different analytical methods to examine 20 non-model, BIA-accumulating plant species. Plants representing four families in the Ranunculales were chosen based on reported BIA content, taxonomic distribution and importance in modern/traditional medicine. One-dimensional (1)H NMR-based profiling quantified 91 metabolites and revealed significant species- and tissue-specific variation in sugar, amino acid and organic acid content. Mono- and disaccharide sugars were generally lower in roots and rhizomes compared with stems, and a variety of metabolites distinguished callus tissue from intact plant organs. Direct flow infusion tandem mass spectrometry provided a broad survey of 110 lipid derivatives including phosphatidylcholines and acylcarnitines, and high-performance liquid chromatography coupled with UV detection quantified 15 phenolic compounds including flavonoids, benzoic acid derivatives and hydroxycinnamic acids. Ultra-performance liquid chromatography coupled with high-resolution Fourier transform mass spectrometry generated extensive mass lists for all species, which were mined for metabolites putatively corresponding to BIAs. Different alkaloids profiles, including both ubiquitous and potentially rare compounds, were observed. CONCLUSIONS: Extensive metabolite profiling combining multiple analytical platforms enabled a more complete picture of overall metabolism occurring in selected plant species. This study represents the first time a metabolomics approach has been applied to most of these species, despite their importance in modern and traditional medicine. Coupled with genomics data, these metabolomics resources serve as a key resource for the investigation of BIA biosynthesis in non-model plant species. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12870-015-0594-2) contains supplementary material, which is available to authorized users.
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spelling pubmed-45706262015-09-16 Metabolome analysis of 20 taxonomically related benzylisoquinoline alkaloid-producing plants Hagel, Jillian M. Mandal, Rupasri Han, Beomsoo Han, Jun Dinsmore, Donald R. Borchers, Christoph H. Wishart, David S. Facchini, Peter J. BMC Plant Biol Research Article BACKGROUND: Recent progress toward the elucidation of benzylisoquinoline alkaloid (BIA) metabolism has focused on a small number of model plant species. Current understanding of BIA metabolism in plants such as opium poppy, which accumulates important pharmacological agents such as codeine and morphine, has relied on a combination of genomics and metabolomics to facilitate gene discovery. Metabolomics studies provide important insight into the primary biochemical networks underpinning specialized metabolism, and serve as a key resource for metabolic engineering, gene discovery, and elucidation of governing regulatory mechanisms. Beyond model plants, few broad-scope metabolomics reports are available for the vast number of plant species known to produce an estimated 2500 structurally diverse BIAs, many of which exhibit promising medicinal properties. RESULTS: We applied a multi-platform approach incorporating four different analytical methods to examine 20 non-model, BIA-accumulating plant species. Plants representing four families in the Ranunculales were chosen based on reported BIA content, taxonomic distribution and importance in modern/traditional medicine. One-dimensional (1)H NMR-based profiling quantified 91 metabolites and revealed significant species- and tissue-specific variation in sugar, amino acid and organic acid content. Mono- and disaccharide sugars were generally lower in roots and rhizomes compared with stems, and a variety of metabolites distinguished callus tissue from intact plant organs. Direct flow infusion tandem mass spectrometry provided a broad survey of 110 lipid derivatives including phosphatidylcholines and acylcarnitines, and high-performance liquid chromatography coupled with UV detection quantified 15 phenolic compounds including flavonoids, benzoic acid derivatives and hydroxycinnamic acids. Ultra-performance liquid chromatography coupled with high-resolution Fourier transform mass spectrometry generated extensive mass lists for all species, which were mined for metabolites putatively corresponding to BIAs. Different alkaloids profiles, including both ubiquitous and potentially rare compounds, were observed. CONCLUSIONS: Extensive metabolite profiling combining multiple analytical platforms enabled a more complete picture of overall metabolism occurring in selected plant species. This study represents the first time a metabolomics approach has been applied to most of these species, despite their importance in modern and traditional medicine. Coupled with genomics data, these metabolomics resources serve as a key resource for the investigation of BIA biosynthesis in non-model plant species. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12870-015-0594-2) contains supplementary material, which is available to authorized users. BioMed Central 2015-09-15 /pmc/articles/PMC4570626/ /pubmed/26369413 http://dx.doi.org/10.1186/s12870-015-0594-2 Text en © Hagel et al. 2015 Open Access This 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
Hagel, Jillian M.
Mandal, Rupasri
Han, Beomsoo
Han, Jun
Dinsmore, Donald R.
Borchers, Christoph H.
Wishart, David S.
Facchini, Peter J.
Metabolome analysis of 20 taxonomically related benzylisoquinoline alkaloid-producing plants
title Metabolome analysis of 20 taxonomically related benzylisoquinoline alkaloid-producing plants
title_full Metabolome analysis of 20 taxonomically related benzylisoquinoline alkaloid-producing plants
title_fullStr Metabolome analysis of 20 taxonomically related benzylisoquinoline alkaloid-producing plants
title_full_unstemmed Metabolome analysis of 20 taxonomically related benzylisoquinoline alkaloid-producing plants
title_short Metabolome analysis of 20 taxonomically related benzylisoquinoline alkaloid-producing plants
title_sort metabolome analysis of 20 taxonomically related benzylisoquinoline alkaloid-producing plants
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4570626/
https://www.ncbi.nlm.nih.gov/pubmed/26369413
http://dx.doi.org/10.1186/s12870-015-0594-2
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