Heat Waves Change Plant Carbon Allocation Among Primary and Secondary Metabolism Altering CO2 Assimilation, Respiration, and VOC Emissions

Processes controlling plant carbon allocation among primary and secondary metabolism, i.e., carbon assimilation, respiration, and VOC synthesis are still poorly constrained, particularly regarding their response to stress. To investigate these processes, we simulated a 10-day 38°C heat wave, analysi...

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Main Authors: Christiane Werner, Lukas Fasbender, Katarzyna M. Romek, Ana Maria Yáñez-Serrano, Jürgen Kreuzwieser
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-08-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fpls.2020.01242/full
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author Christiane Werner
Lukas Fasbender
Katarzyna M. Romek
Ana Maria Yáñez-Serrano
Ana Maria Yáñez-Serrano
Ana Maria Yáñez-Serrano
Jürgen Kreuzwieser
author_facet Christiane Werner
Lukas Fasbender
Katarzyna M. Romek
Ana Maria Yáñez-Serrano
Ana Maria Yáñez-Serrano
Ana Maria Yáñez-Serrano
Jürgen Kreuzwieser
author_sort Christiane Werner
collection DOAJ
description Processes controlling plant carbon allocation among primary and secondary metabolism, i.e., carbon assimilation, respiration, and VOC synthesis are still poorly constrained, particularly regarding their response to stress. To investigate these processes, we simulated a 10-day 38°C heat wave, analysing real-time carbon allocation into primary and secondary metabolism in the Mediterranean shrub Halimium halimifolium L. We traced position-specific 13C-labeled pyruvate into daytime VOC and CO2 emissions and during light-dark transition. Net CO2 assimilation strongly declined under heat, due to three-fold higher respiration rates. Interestingly, day respiration also increased two-fold. Decarboxylation of the C1-atom of pyruvate was the main process driving daytime CO2 release, whereas the C2-moiety was not decarboxylated in the TCA cycle. Heat induced high emissions of methanol, methyl acetate, acetaldehyde as well as mono- and sesquiterpenes, particularly during the first two days. After 10-days of heat a substantial proportion of 13C-labeled pyruvate was allocated into de novo synthesis of VOCs. Thus, during extreme heat waves high respiratory losses and reduced assimilation can shift plants into a negative carbon balance. Still, plants enhanced their investment into de novo VOC synthesis despite associated metabolic CO2 losses. We conclude that heat stress re-directed the proportional flux of key metabolites into pathways of VOC biosynthesis most likely at the expense of reactions of plant primary metabolism, which might highlight their importance for stress protection.
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spelling doaj.art-52f854f074cf4a8c8e76aac1c0a153d82022-12-22T01:29:28ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2020-08-011110.3389/fpls.2020.01242512788Heat Waves Change Plant Carbon Allocation Among Primary and Secondary Metabolism Altering CO2 Assimilation, Respiration, and VOC EmissionsChristiane Werner0Lukas Fasbender1Katarzyna M. Romek2Ana Maria Yáñez-Serrano3Ana Maria Yáñez-Serrano4Ana Maria Yáñez-Serrano5Jürgen Kreuzwieser6Ecosystem Physiology, University of Freiburg, Freiburg, GermanyEcosystem Physiology, University of Freiburg, Freiburg, GermanyEcosystem Physiology, University of Freiburg, Freiburg, GermanyEcosystem Physiology, University of Freiburg, Freiburg, GermanyCenter of Ecological Research and Forest Applications (CREAF), Universitat Autònoma de Barcelona, Barcelona, SpainGlobal Ecology Unit CREAF-CSIC-UAB, Cerdanyola del Vallès, Barcelona, SpainEcosystem Physiology, University of Freiburg, Freiburg, GermanyProcesses controlling plant carbon allocation among primary and secondary metabolism, i.e., carbon assimilation, respiration, and VOC synthesis are still poorly constrained, particularly regarding their response to stress. To investigate these processes, we simulated a 10-day 38°C heat wave, analysing real-time carbon allocation into primary and secondary metabolism in the Mediterranean shrub Halimium halimifolium L. We traced position-specific 13C-labeled pyruvate into daytime VOC and CO2 emissions and during light-dark transition. Net CO2 assimilation strongly declined under heat, due to three-fold higher respiration rates. Interestingly, day respiration also increased two-fold. Decarboxylation of the C1-atom of pyruvate was the main process driving daytime CO2 release, whereas the C2-moiety was not decarboxylated in the TCA cycle. Heat induced high emissions of methanol, methyl acetate, acetaldehyde as well as mono- and sesquiterpenes, particularly during the first two days. After 10-days of heat a substantial proportion of 13C-labeled pyruvate was allocated into de novo synthesis of VOCs. Thus, during extreme heat waves high respiratory losses and reduced assimilation can shift plants into a negative carbon balance. Still, plants enhanced their investment into de novo VOC synthesis despite associated metabolic CO2 losses. We conclude that heat stress re-directed the proportional flux of key metabolites into pathways of VOC biosynthesis most likely at the expense of reactions of plant primary metabolism, which might highlight their importance for stress protection.https://www.frontiersin.org/article/10.3389/fpls.2020.01242/fullcarbon allocationday respirationtemperature stress13C position-specific labelingphotosynthesispyruvate
spellingShingle Christiane Werner
Lukas Fasbender
Katarzyna M. Romek
Ana Maria Yáñez-Serrano
Ana Maria Yáñez-Serrano
Ana Maria Yáñez-Serrano
Jürgen Kreuzwieser
Heat Waves Change Plant Carbon Allocation Among Primary and Secondary Metabolism Altering CO2 Assimilation, Respiration, and VOC Emissions
Frontiers in Plant Science
carbon allocation
day respiration
temperature stress
13C position-specific labeling
photosynthesis
pyruvate
title Heat Waves Change Plant Carbon Allocation Among Primary and Secondary Metabolism Altering CO2 Assimilation, Respiration, and VOC Emissions
title_full Heat Waves Change Plant Carbon Allocation Among Primary and Secondary Metabolism Altering CO2 Assimilation, Respiration, and VOC Emissions
title_fullStr Heat Waves Change Plant Carbon Allocation Among Primary and Secondary Metabolism Altering CO2 Assimilation, Respiration, and VOC Emissions
title_full_unstemmed Heat Waves Change Plant Carbon Allocation Among Primary and Secondary Metabolism Altering CO2 Assimilation, Respiration, and VOC Emissions
title_short Heat Waves Change Plant Carbon Allocation Among Primary and Secondary Metabolism Altering CO2 Assimilation, Respiration, and VOC Emissions
title_sort heat waves change plant carbon allocation among primary and secondary metabolism altering co2 assimilation respiration and voc emissions
topic carbon allocation
day respiration
temperature stress
13C position-specific labeling
photosynthesis
pyruvate
url https://www.frontiersin.org/article/10.3389/fpls.2020.01242/full
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