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Integration of C(1) and C(2) Metabolism in Trees

C(1) 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 C(1) pathway is thought to be large, its intermediates are difficult to measure a...

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Autores principales: Jardine, Kolby J., Fernandes de Souza, Vinicius, Oikawa, Patty, Higuchi, Niro, Bill, Markus, Porras, Rachel, Niinemets, Ülo, Chambers, Jeffrey Q.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5666727/
https://www.ncbi.nlm.nih.gov/pubmed/28946627
http://dx.doi.org/10.3390/ijms18102045
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author Jardine, Kolby J.
Fernandes de Souza, Vinicius
Oikawa, Patty
Higuchi, Niro
Bill, Markus
Porras, Rachel
Niinemets, Ülo
Chambers, Jeffrey Q.
author_facet Jardine, Kolby J.
Fernandes de Souza, Vinicius
Oikawa, Patty
Higuchi, Niro
Bill, Markus
Porras, Rachel
Niinemets, Ülo
Chambers, Jeffrey Q.
author_sort Jardine, Kolby J.
collection PubMed
description C(1) 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 C(1) 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 C(1) pathway and its integration with the central metabolism using aqueous solutions of (13)C-labeled C(1) and C(2) intermediates delivered to branches of the tropical species Inga edulis via the transpiration stream. Delivery of [(13)C]methanol and [(13)C]formaldehyde rapidly stimulated leaf emissions of [(13)C]methanol, [(13)C]formaldehyde, [(13)C]formic acid, and (13)CO(2), confirming the existence of the C1 pathway and rapid interconversion between methanol and formaldehyde. However, while [(13)C]formate solutions stimulated emissions of (13)CO(2), emissions of [(13)C]methanol or [(13)C]formaldehyde were not detected, suggesting that once oxidation to formate occurs it is rapidly oxidized to CO(2) within chloroplasts. (13)C-labeling of isoprene, a known photosynthetic product, was linearly related to (13)CO(2) across C(1) and C(2) ([(13)C(2)]acetate and [2-(13)C]glycine) substrates, consistent with reassimilation of C(1), respiratory, and photorespiratory CO(2). Moreover, [(13)C]methanol and [(13)C]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 C(1) pathway to provide an alternative carbon source for glycine methylation in photorespiration, enhance CO(2) concentrations within chloroplasts, and produce key C(2) intermediates (e.g., acetyl-CoA) central to anabolic and catabolic metabolism.
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spelling pubmed-56667272017-11-09 Integration of C(1) and C(2) Metabolism in Trees Jardine, Kolby J. Fernandes de Souza, Vinicius Oikawa, Patty Higuchi, Niro Bill, Markus Porras, Rachel Niinemets, Ülo Chambers, Jeffrey Q. Int J Mol Sci Article C(1) 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 C(1) 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 C(1) pathway and its integration with the central metabolism using aqueous solutions of (13)C-labeled C(1) and C(2) intermediates delivered to branches of the tropical species Inga edulis via the transpiration stream. Delivery of [(13)C]methanol and [(13)C]formaldehyde rapidly stimulated leaf emissions of [(13)C]methanol, [(13)C]formaldehyde, [(13)C]formic acid, and (13)CO(2), confirming the existence of the C1 pathway and rapid interconversion between methanol and formaldehyde. However, while [(13)C]formate solutions stimulated emissions of (13)CO(2), emissions of [(13)C]methanol or [(13)C]formaldehyde were not detected, suggesting that once oxidation to formate occurs it is rapidly oxidized to CO(2) within chloroplasts. (13)C-labeling of isoprene, a known photosynthetic product, was linearly related to (13)CO(2) across C(1) and C(2) ([(13)C(2)]acetate and [2-(13)C]glycine) substrates, consistent with reassimilation of C(1), respiratory, and photorespiratory CO(2). Moreover, [(13)C]methanol and [(13)C]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 C(1) pathway to provide an alternative carbon source for glycine methylation in photorespiration, enhance CO(2) concentrations within chloroplasts, and produce key C(2) intermediates (e.g., acetyl-CoA) central to anabolic and catabolic metabolism. MDPI 2017-09-23 /pmc/articles/PMC5666727/ /pubmed/28946627 http://dx.doi.org/10.3390/ijms18102045 Text en © 2017 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Jardine, Kolby J.
Fernandes de Souza, Vinicius
Oikawa, Patty
Higuchi, Niro
Bill, Markus
Porras, Rachel
Niinemets, Ülo
Chambers, Jeffrey Q.
Integration of C(1) and C(2) Metabolism in Trees
title Integration of C(1) and C(2) Metabolism in Trees
title_full Integration of C(1) and C(2) Metabolism in Trees
title_fullStr Integration of C(1) and C(2) Metabolism in Trees
title_full_unstemmed Integration of C(1) and C(2) Metabolism in Trees
title_short Integration of C(1) and C(2) Metabolism in Trees
title_sort integration of c(1) and c(2) metabolism in trees
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5666727/
https://www.ncbi.nlm.nih.gov/pubmed/28946627
http://dx.doi.org/10.3390/ijms18102045
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