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Title: Integration of C1 and C2 Metabolism in Trees

Abstract

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 of 13C-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, and 13CO2, confirming the existence of the C1 pathway and rapid interconversion between methanol and formaldehyde. However, while [13C]formate solutions stimulated emissions of 13CO2, 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 to 13CO2 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, possiblymore » 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.« less

Authors:
 [1];  [2];  [3];  [2];  [1];  [1];  [4];  [5]
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  1. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  2. National Institute for Amazon Research, Manaus (Brazil)
  3. California State Univ. (CalState), Hayward, CA (United States)
  4. Estonian Univ. of Life Sciences, Tartu (Estonia); Estonian Academy of Sciences, Tallinn (Estonia)
  5. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1419438
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
International Journal of Molecular Sciences (Online)
Additional Journal Information:
Journal Name: International Journal of Molecular Sciences (Online); Journal Volume: 18; Journal Issue: 10; Journal ID: ISSN 1422-0067
Publisher:
MDPI
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; internal recycling of carbon; volatile emissions; central metabolism; plant growth and senescence; methanol; acetic acid

Citation Formats

Jardine, Kolby J., Fernandes de Souza, Vinicius, Oikawa, Patty, Higuchi, Niro, Bill, Markus, Porras, Rachel, Niinemets, Ulo, and Chambers, Jeffrey Q. Integration of C1 and C2 Metabolism in Trees. United States: N. p., 2017. Web. doi:10.3390/ijms18102045.
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Jardine, Kolby J., Fernandes de Souza, Vinicius, Oikawa, Patty, Higuchi, Niro, Bill, Markus, Porras, Rachel, Niinemets, Ulo, & Chambers, Jeffrey Q. Integration of C1 and C2 Metabolism in Trees. United States. https://doi.org/10.3390/ijms18102045
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Jardine, Kolby J., Fernandes de Souza, Vinicius, Oikawa, Patty, Higuchi, Niro, Bill, Markus, Porras, Rachel, Niinemets, Ulo, and Chambers, Jeffrey Q. Sat . "Integration of C1 and C2 Metabolism in Trees". United States. https://doi.org/10.3390/ijms18102045. https://www.osti.gov/servlets/purl/1419438.
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@article{osti_1419438,
title = {Integration of C1 and C2 Metabolism in Trees},
author = {Jardine, Kolby J. and Fernandes de Souza, Vinicius and Oikawa, Patty and Higuchi, Niro and Bill, Markus and Porras, Rachel and Niinemets, Ulo and Chambers, Jeffrey Q.},
abstractNote = {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 of 13C-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, and 13CO2, confirming the existence of the C1 pathway and rapid interconversion between methanol and formaldehyde. However, while [13C]formate solutions stimulated emissions of 13CO2, 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 to 13CO2 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.},
doi = {10.3390/ijms18102045},
journal = {International Journal of Molecular Sciences (Online)},
number = 10,
volume = 18,
place = {United States},
year = {2017},
month = {9}
}
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