Combined transcript, proteome, and metabolite analysis of transgenic maize seeds engineered for enhanced carotenoid synthesis reveals pleotropic effects in core metabolism

The aim of this study was to assess whether endosperm-specific carotenoid biosynthesis influenced core metabolic processes in maize embryo and endosperm and how global seed metabolism adapted to this expanded biosynthetic capacity. Although enhancement of carotenoid biosynthesis was targeted to the...

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Autores: Decourcelle, Mathilde, Perez-Fons, Laura, Baulande, Sylvain, Steiger, Sabine, Couvelard, Linhdavanh, Hem, Sonia, Zhu, Changfu, Capell Capell, Teresa, Christou, Paul, Fraser, Paul, Sandmann, Gerhard
Tipo de documento: artigo
Estado:Versão publicada
Data de publicação:2015
País:España
Recursos:Universitat de Lleida (UdL)
Repositório:Repositori Obert UdL
OAI Identifier:oai:repositori.udl.cat:10459.1/66296
Acesso em linha:https://doi.org/10.1093/jxb/erv120
http://hdl.handle.net/10459.1/66296
Access Level:Acceso aberto
Palavra-chave:Genetically engineered carotenoid biosynthesis
GM maize
Pathway regulation
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spelling Combined transcript, proteome, and metabolite analysis of transgenic maize seeds engineered for enhanced carotenoid synthesis reveals pleotropic effects in core metabolismDecourcelle, MathildePerez-Fons, LauraBaulande, SylvainSteiger, SabineCouvelard, LinhdavanhHem, SoniaZhu, ChangfuCapell Capell, TeresaChristou, PaulFraser, PaulSandmann, GerhardGenetically engineered carotenoid biosynthesisGM maizePathway regulationThe aim of this study was to assess whether endosperm-specific carotenoid biosynthesis influenced core metabolic processes in maize embryo and endosperm and how global seed metabolism adapted to this expanded biosynthetic capacity. Although enhancement of carotenoid biosynthesis was targeted to the endosperm of maize kernels, a concurrent up-regulation of sterol and fatty acid biosynthesis in the embryo was measured. Targeted terpenoid analysis, and non-targeted metabolomic, proteomic, and transcriptomic profiling revealed changes especially in carbohydrate metabolism in the transgenic line. In-depth analysis of the data, including changes of metabolite pools and increased enzyme and transcript concentrations, gave a first insight into the metabolic variation precipitated by the higher up-stream metabolite demand by the extended biosynthesis capacities for terpenoids and fatty acids. An integrative model is put forward to explain the metabolic regulation for the increased provision of terpenoid and fatty acid precursors, particularly glyceraldehyde 3-phosphate and pyruvate or acetyl-CoA from imported fructose and glucose. The model was supported by higher activities of fructokinase, glucose 6-phosphate isomerase, and fructose 1,6-bisphosphate aldolase indicating a higher flux through the glycolytic pathway. Although pyruvate and acetyl-CoA utilization was higher in the engineered line, pyruvate kinase activity was lower. A sufficient provision of both metabolites may be supported by a by-pass in a reaction sequence involving phosphoenolpyruvate carboxylase, malate dehydrogenase, and malic enzyme.Funding through the Plant KBBE project CaroMaize is gratefully acknowledged. PDF and LP are grateful for funding from the EU FP7 project DISCO grant number 613513.Oxford University Press2015info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttps://doi.org/10.1093/jxb/erv120http://hdl.handle.net/10459.1/66296reponame:Repositori Obert UdL instname:Universitat de Lleida (UdL)InglésReproducció del document publicat a https://doi.org/10.1093/jxb/erv120Journal of Experimental Botany, 2015, vol. 66, núm. 11, p. 3141–3150info:eu-repo/grantAgreement/EC/FP7/613513cc-by, (c) Decourcelle et al., 2015info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by/3.0/oai:repositori.udl.cat:10459.1/662962026-06-24T12:42:17Z
dc.title.none.fl_str_mv Combined transcript, proteome, and metabolite analysis of transgenic maize seeds engineered for enhanced carotenoid synthesis reveals pleotropic effects in core metabolism
title Combined transcript, proteome, and metabolite analysis of transgenic maize seeds engineered for enhanced carotenoid synthesis reveals pleotropic effects in core metabolism
spellingShingle Combined transcript, proteome, and metabolite analysis of transgenic maize seeds engineered for enhanced carotenoid synthesis reveals pleotropic effects in core metabolism
Decourcelle, Mathilde
Genetically engineered carotenoid biosynthesis
GM maize
Pathway regulation
title_short Combined transcript, proteome, and metabolite analysis of transgenic maize seeds engineered for enhanced carotenoid synthesis reveals pleotropic effects in core metabolism
title_full Combined transcript, proteome, and metabolite analysis of transgenic maize seeds engineered for enhanced carotenoid synthesis reveals pleotropic effects in core metabolism
title_fullStr Combined transcript, proteome, and metabolite analysis of transgenic maize seeds engineered for enhanced carotenoid synthesis reveals pleotropic effects in core metabolism
title_full_unstemmed Combined transcript, proteome, and metabolite analysis of transgenic maize seeds engineered for enhanced carotenoid synthesis reveals pleotropic effects in core metabolism
title_sort Combined transcript, proteome, and metabolite analysis of transgenic maize seeds engineered for enhanced carotenoid synthesis reveals pleotropic effects in core metabolism
dc.creator.none.fl_str_mv Decourcelle, Mathilde
Perez-Fons, Laura
Baulande, Sylvain
Steiger, Sabine
Couvelard, Linhdavanh
Hem, Sonia
Zhu, Changfu
Capell Capell, Teresa
Christou, Paul
Fraser, Paul
Sandmann, Gerhard
author Decourcelle, Mathilde
author_facet Decourcelle, Mathilde
Perez-Fons, Laura
Baulande, Sylvain
Steiger, Sabine
Couvelard, Linhdavanh
Hem, Sonia
Zhu, Changfu
Capell Capell, Teresa
Christou, Paul
Fraser, Paul
Sandmann, Gerhard
author_role author
author2 Perez-Fons, Laura
Baulande, Sylvain
Steiger, Sabine
Couvelard, Linhdavanh
Hem, Sonia
Zhu, Changfu
Capell Capell, Teresa
Christou, Paul
Fraser, Paul
Sandmann, Gerhard
author2_role author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Genetically engineered carotenoid biosynthesis
GM maize
Pathway regulation
topic Genetically engineered carotenoid biosynthesis
GM maize
Pathway regulation
description The aim of this study was to assess whether endosperm-specific carotenoid biosynthesis influenced core metabolic processes in maize embryo and endosperm and how global seed metabolism adapted to this expanded biosynthetic capacity. Although enhancement of carotenoid biosynthesis was targeted to the endosperm of maize kernels, a concurrent up-regulation of sterol and fatty acid biosynthesis in the embryo was measured. Targeted terpenoid analysis, and non-targeted metabolomic, proteomic, and transcriptomic profiling revealed changes especially in carbohydrate metabolism in the transgenic line. In-depth analysis of the data, including changes of metabolite pools and increased enzyme and transcript concentrations, gave a first insight into the metabolic variation precipitated by the higher up-stream metabolite demand by the extended biosynthesis capacities for terpenoids and fatty acids. An integrative model is put forward to explain the metabolic regulation for the increased provision of terpenoid and fatty acid precursors, particularly glyceraldehyde 3-phosphate and pyruvate or acetyl-CoA from imported fructose and glucose. The model was supported by higher activities of fructokinase, glucose 6-phosphate isomerase, and fructose 1,6-bisphosphate aldolase indicating a higher flux through the glycolytic pathway. Although pyruvate and acetyl-CoA utilization was higher in the engineered line, pyruvate kinase activity was lower. A sufficient provision of both metabolites may be supported by a by-pass in a reaction sequence involving phosphoenolpyruvate carboxylase, malate dehydrogenase, and malic enzyme.
publishDate 2015
dc.date.none.fl_str_mv 2015
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv https://doi.org/10.1093/jxb/erv120
http://hdl.handle.net/10459.1/66296
url https://doi.org/10.1093/jxb/erv120
http://hdl.handle.net/10459.1/66296
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Reproducció del document publicat a https://doi.org/10.1093/jxb/erv120
Journal of Experimental Botany, 2015, vol. 66, núm. 11, p. 3141–3150
info:eu-repo/grantAgreement/EC/FP7/613513
dc.rights.none.fl_str_mv cc-by, (c) Decourcelle et al., 2015
info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by/3.0/
rights_invalid_str_mv cc-by, (c) Decourcelle et al., 2015
https://creativecommons.org/licenses/by/3.0/
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv Oxford University Press
publisher.none.fl_str_mv Oxford University Press
dc.source.none.fl_str_mv reponame:Repositori Obert UdL
instname:Universitat de Lleida (UdL)
instname_str Universitat de Lleida (UdL)
reponame_str Repositori Obert UdL
collection Repositori Obert UdL
repository.name.fl_str_mv
repository.mail.fl_str_mv
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score 15,811543

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