Integration of C1 and C2 metabolism in trees

Detalhes bibliográficos
Autor(a) principal: Jardine, Kolby J.
Data de Publicação: 2017
Outros Autores: Souza, Vinícius Fernandes de, Oikawa, Patricia Yoshino, Higuchi, Niro, Bill, Markus, Porras, Rachel C., Niinemets, Ülo, Chambers, Jeffrey Quintin
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Institucional do INPA
Texto Completo: https://repositorio.inpa.gov.br/handle/1/15710
Resumo: C1 metabolism in plants is known to be involved in photorespiration, nitrogen and amino acid metabolism, as well as methylation and biosynthesis of metabolites and biopolymers. Although the flux of carbon through the C1 pathway is thought to be large, its intermediates are difficult to measure and relatively little is known about this potentially ubiquitous pathway. In this study, we evaluated the C1 pathway and its integration with the central metabolism using aqueous solutions of13C-labeled C1 and C2 intermediates delivered to branches of the tropical species Inga edulis via the transpiration stream. Delivery of [13C]methanol and [13C]formaldehyde rapidly stimulated leaf emissions of [13C]methanol, [13C]formaldehyde, [13C]formic acid, and13CO2, confirming the existence of the C1 pathway and rapid interconversion between methanol and formaldehyde. However, while [13C]formate solutions stimulated emissions of13CO2, emissions of [13C]methanol or [13C]formaldehyde were not detected, suggesting that once oxidation to formate occurs it is rapidly oxidized to CO2 within chloroplasts.13C-labeling of isoprene, a known photosynthetic product, was linearly related to13CO2 across C1 and C2 ([13C2]acetate and [2-13C]glycine) substrates, consistent with reassimilation of C1, respiratory, and photorespiratory CO2. Moreover, [13C]methanol and [13C]formaldehyde induced a quantitative labeling of both carbon atoms of acetic acid emissions, possibly through the rapid turnover of the chloroplastic acetyl-CoA pool via glycolate oxidation. The results support a role of the C1 pathway to provide an alternative carbon source for glycine methylation in photorespiration, enhance CO2 concentrations within chloroplasts, and produce key C2 intermediates (e.g., acetyl-CoA) central to anabolic and catabolic metabolism. © 2017 by the authors. Licensee MDPI, Basel, Switzerland.
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spelling Jardine, Kolby J.Souza, Vinícius Fernandes deOikawa, Patricia YoshinoHiguchi, NiroBill, MarkusPorras, Rachel C.Niinemets, ÜloChambers, Jeffrey Quintin2020-05-18T15:08:09Z2020-05-18T15:08:09Z2017https://repositorio.inpa.gov.br/handle/1/1571010.3390/ijms18102045C1 metabolism in plants is known to be involved in photorespiration, nitrogen and amino acid metabolism, as well as methylation and biosynthesis of metabolites and biopolymers. Although the flux of carbon through the C1 pathway is thought to be large, its intermediates are difficult to measure and relatively little is known about this potentially ubiquitous pathway. In this study, we evaluated the C1 pathway and its integration with the central metabolism using aqueous solutions of13C-labeled C1 and C2 intermediates delivered to branches of the tropical species Inga edulis via the transpiration stream. Delivery of [13C]methanol and [13C]formaldehyde rapidly stimulated leaf emissions of [13C]methanol, [13C]formaldehyde, [13C]formic acid, and13CO2, confirming the existence of the C1 pathway and rapid interconversion between methanol and formaldehyde. However, while [13C]formate solutions stimulated emissions of13CO2, emissions of [13C]methanol or [13C]formaldehyde were not detected, suggesting that once oxidation to formate occurs it is rapidly oxidized to CO2 within chloroplasts.13C-labeling of isoprene, a known photosynthetic product, was linearly related to13CO2 across C1 and C2 ([13C2]acetate and [2-13C]glycine) substrates, consistent with reassimilation of C1, respiratory, and photorespiratory CO2. Moreover, [13C]methanol and [13C]formaldehyde induced a quantitative labeling of both carbon atoms of acetic acid emissions, possibly through the rapid turnover of the chloroplastic acetyl-CoA pool via glycolate oxidation. The results support a role of the C1 pathway to provide an alternative carbon source for glycine methylation in photorespiration, enhance CO2 concentrations within chloroplasts, and produce key C2 intermediates (e.g., acetyl-CoA) central to anabolic and catabolic metabolism. © 2017 by the authors. Licensee MDPI, Basel, Switzerland.Volume 18, Número 10Attribution-NonCommercial-NoDerivs 3.0 Brazilhttp://creativecommons.org/licenses/by-nc-nd/3.0/br/info:eu-repo/semantics/openAccessAcetic AcidCarbon-13Carbon DioxideFormaldehydeFormic AcidGlycineIsopreneMethanol1,3 Butadiene DerivativeCarbonCarbon-13Formic Acid DerivativeHemiterpenePentaneVolatile Organic CompoundCarbon MetabolismChloroplastInga EdulisIsotope LabelingMass FragmentographyMass SpectrometryMetaboliteNonhumanPhotorespirationPlant GrowthPlant LeafProton Transfer Reaction Mass SpectrometryProton TransportQuantitative AnalysisReassimilationTreeChemistryMetabolismTreeButadienesCarbonCarbon IsotopesFormaldehydeFormatesHemiterpenesIsotope LabelingMetabolic Networks And PathwaysMethanolPentanesTreesVolatile Organic CompoundsIntegration of C1 and C2 metabolism in treesinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleInternational Journal of Molecular Sciencesengreponame:Repositório Institucional do INPAinstname:Instituto Nacional de Pesquisas da Amazônia (INPA)instacron:INPAORIGINALartigo-inpa.pdfartigo-inpa.pdfapplication/pdf2539764https://repositorio.inpa.gov.br/bitstream/1/15710/1/artigo-inpa.pdf2b2a81ca61cee40c8de975b46c00af5cMD511/157102020-05-18 11:32:47.134oai:repositorio:1/15710Repositório de PublicaçõesPUBhttps://repositorio.inpa.gov.br/oai/requestopendoar:2020-05-18T15:32:47Repositório Institucional do INPA - Instituto Nacional de Pesquisas da Amazônia (INPA)false
dc.title.en.fl_str_mv Integration of C1 and C2 metabolism in trees
title Integration of C1 and C2 metabolism in trees
spellingShingle Integration of C1 and C2 metabolism in trees
Jardine, Kolby J.
Acetic Acid
Carbon-13
Carbon Dioxide
Formaldehyde
Formic Acid
Glycine
Isoprene
Methanol
1,3 Butadiene Derivative
Carbon
Carbon-13
Formic Acid Derivative
Hemiterpene
Pentane
Volatile Organic Compound
Carbon Metabolism
Chloroplast
Inga Edulis
Isotope Labeling
Mass Fragmentography
Mass Spectrometry
Metabolite
Nonhuman
Photorespiration
Plant Growth
Plant Leaf
Proton Transfer Reaction Mass Spectrometry
Proton Transport
Quantitative Analysis
Reassimilation
Tree
Chemistry
Metabolism
Tree
Butadienes
Carbon
Carbon Isotopes
Formaldehyde
Formates
Hemiterpenes
Isotope Labeling
Metabolic Networks And Pathways
Methanol
Pentanes
Trees
Volatile Organic Compounds
title_short Integration of C1 and C2 metabolism in trees
title_full Integration of C1 and C2 metabolism in trees
title_fullStr Integration of C1 and C2 metabolism in trees
title_full_unstemmed Integration of C1 and C2 metabolism in trees
title_sort Integration of C1 and C2 metabolism in trees
author Jardine, Kolby J.
author_facet Jardine, Kolby J.
Souza, Vinícius Fernandes de
Oikawa, Patricia Yoshino
Higuchi, Niro
Bill, Markus
Porras, Rachel C.
Niinemets, Ülo
Chambers, Jeffrey Quintin
author_role author
author2 Souza, Vinícius Fernandes de
Oikawa, Patricia Yoshino
Higuchi, Niro
Bill, Markus
Porras, Rachel C.
Niinemets, Ülo
Chambers, Jeffrey Quintin
author2_role author
author
author
author
author
author
author
dc.contributor.author.fl_str_mv Jardine, Kolby J.
Souza, Vinícius Fernandes de
Oikawa, Patricia Yoshino
Higuchi, Niro
Bill, Markus
Porras, Rachel C.
Niinemets, Ülo
Chambers, Jeffrey Quintin
dc.subject.eng.fl_str_mv Acetic Acid
Carbon-13
Carbon Dioxide
Formaldehyde
Formic Acid
Glycine
Isoprene
Methanol
1,3 Butadiene Derivative
Carbon
Carbon-13
Formic Acid Derivative
Hemiterpene
Pentane
Volatile Organic Compound
Carbon Metabolism
Chloroplast
Inga Edulis
Isotope Labeling
Mass Fragmentography
Mass Spectrometry
Metabolite
Nonhuman
Photorespiration
Plant Growth
Plant Leaf
Proton Transfer Reaction Mass Spectrometry
Proton Transport
Quantitative Analysis
Reassimilation
Tree
Chemistry
Metabolism
Tree
Butadienes
Carbon
Carbon Isotopes
Formaldehyde
Formates
Hemiterpenes
Isotope Labeling
Metabolic Networks And Pathways
Methanol
Pentanes
Trees
Volatile Organic Compounds
topic Acetic Acid
Carbon-13
Carbon Dioxide
Formaldehyde
Formic Acid
Glycine
Isoprene
Methanol
1,3 Butadiene Derivative
Carbon
Carbon-13
Formic Acid Derivative
Hemiterpene
Pentane
Volatile Organic Compound
Carbon Metabolism
Chloroplast
Inga Edulis
Isotope Labeling
Mass Fragmentography
Mass Spectrometry
Metabolite
Nonhuman
Photorespiration
Plant Growth
Plant Leaf
Proton Transfer Reaction Mass Spectrometry
Proton Transport
Quantitative Analysis
Reassimilation
Tree
Chemistry
Metabolism
Tree
Butadienes
Carbon
Carbon Isotopes
Formaldehyde
Formates
Hemiterpenes
Isotope Labeling
Metabolic Networks And Pathways
Methanol
Pentanes
Trees
Volatile Organic Compounds
description C1 metabolism in plants is known to be involved in photorespiration, nitrogen and amino acid metabolism, as well as methylation and biosynthesis of metabolites and biopolymers. Although the flux of carbon through the C1 pathway is thought to be large, its intermediates are difficult to measure and relatively little is known about this potentially ubiquitous pathway. In this study, we evaluated the C1 pathway and its integration with the central metabolism using aqueous solutions of13C-labeled C1 and C2 intermediates delivered to branches of the tropical species Inga edulis via the transpiration stream. Delivery of [13C]methanol and [13C]formaldehyde rapidly stimulated leaf emissions of [13C]methanol, [13C]formaldehyde, [13C]formic acid, and13CO2, confirming the existence of the C1 pathway and rapid interconversion between methanol and formaldehyde. However, while [13C]formate solutions stimulated emissions of13CO2, emissions of [13C]methanol or [13C]formaldehyde were not detected, suggesting that once oxidation to formate occurs it is rapidly oxidized to CO2 within chloroplasts.13C-labeling of isoprene, a known photosynthetic product, was linearly related to13CO2 across C1 and C2 ([13C2]acetate and [2-13C]glycine) substrates, consistent with reassimilation of C1, respiratory, and photorespiratory CO2. Moreover, [13C]methanol and [13C]formaldehyde induced a quantitative labeling of both carbon atoms of acetic acid emissions, possibly through the rapid turnover of the chloroplastic acetyl-CoA pool via glycolate oxidation. The results support a role of the C1 pathway to provide an alternative carbon source for glycine methylation in photorespiration, enhance CO2 concentrations within chloroplasts, and produce key C2 intermediates (e.g., acetyl-CoA) central to anabolic and catabolic metabolism. © 2017 by the authors. Licensee MDPI, Basel, Switzerland.
publishDate 2017
dc.date.issued.fl_str_mv 2017
dc.date.accessioned.fl_str_mv 2020-05-18T15:08:09Z
dc.date.available.fl_str_mv 2020-05-18T15:08:09Z
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
format article
status_str publishedVersion
dc.identifier.uri.fl_str_mv https://repositorio.inpa.gov.br/handle/1/15710
dc.identifier.doi.none.fl_str_mv 10.3390/ijms18102045
url https://repositorio.inpa.gov.br/handle/1/15710
identifier_str_mv 10.3390/ijms18102045
dc.language.iso.fl_str_mv eng
language eng
dc.relation.ispartof.pt_BR.fl_str_mv Volume 18, Número 10
dc.rights.driver.fl_str_mv Attribution-NonCommercial-NoDerivs 3.0 Brazil
http://creativecommons.org/licenses/by-nc-nd/3.0/br/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv Attribution-NonCommercial-NoDerivs 3.0 Brazil
http://creativecommons.org/licenses/by-nc-nd/3.0/br/
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv International Journal of Molecular Sciences
publisher.none.fl_str_mv International Journal of Molecular Sciences
dc.source.none.fl_str_mv reponame:Repositório Institucional do INPA
instname:Instituto Nacional de Pesquisas da Amazônia (INPA)
instacron:INPA
instname_str Instituto Nacional de Pesquisas da Amazônia (INPA)
instacron_str INPA
institution INPA
reponame_str Repositório Institucional do INPA
collection Repositório Institucional do INPA
bitstream.url.fl_str_mv https://repositorio.inpa.gov.br/bitstream/1/15710/1/artigo-inpa.pdf
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repository.name.fl_str_mv Repositório Institucional do INPA - Instituto Nacional de Pesquisas da Amazônia (INPA)
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