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Leaf-level metabolic changes in response to drought affect daytime CO2 emission and isoprenoid synthesis

View ORCID ProfileS. Nemiah Ladd, View ORCID ProfileL. Erik Daber, Ines Bamberger, Angelika Kübert, View ORCID ProfileJürgen Kreuzwieser, View ORCID ProfileGemma Purser, View ORCID ProfileJohannes Ingrisch, Jason Deleeuw, Joost van Haren, View ORCID ProfileLaura K. Meredith, View ORCID ProfileChristiane Werner
doi: https://doi.org/10.1101/2022.04.29.490001
S. Nemiah Ladd
1Ecosystem Physiology, Albert-Ludwigs-University of Freiburg, Georges-Köhler-Allee 053/054, 79110 Freiburg, Germany
2Department of Environmental Sciences, University of Basel, Bernoullistrasse 30, 4056 Basel, Switzerland
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L. Erik Daber
1Ecosystem Physiology, Albert-Ludwigs-University of Freiburg, Georges-Köhler-Allee 053/054, 79110 Freiburg, Germany
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Ines Bamberger
1Ecosystem Physiology, Albert-Ludwigs-University of Freiburg, Georges-Köhler-Allee 053/054, 79110 Freiburg, Germany
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Angelika Kübert
1Ecosystem Physiology, Albert-Ludwigs-University of Freiburg, Georges-Köhler-Allee 053/054, 79110 Freiburg, Germany
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Jürgen Kreuzwieser
1Ecosystem Physiology, Albert-Ludwigs-University of Freiburg, Georges-Köhler-Allee 053/054, 79110 Freiburg, Germany
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Gemma Purser
3School of Chemistry, The University of Edinburgh, Joseph Black Building, David Brewster Road, Edinburgh, EH9 3FJ, UK
4UK Centre for Ecology & Hydrology, Bush Estate, Penicuik, EH26 0QB, U K
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Johannes Ingrisch
1Ecosystem Physiology, Albert-Ludwigs-University of Freiburg, Georges-Köhler-Allee 053/054, 79110 Freiburg, Germany
5Department of Ecology, University of Innsbruck, Sternwartestrasse 15, 6020 Innsbruck, Austria
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Jason Deleeuw
6Biosphere 2, University of Arizona, 32540 S. Biosphere Rd., Oracle, AZ, 85739, USA
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Joost van Haren
6Biosphere 2, University of Arizona, 32540 S. Biosphere Rd., Oracle, AZ, 85739, USA
7Honors College, University of Arizona, 1101 E. Mabel Street, Tucson, AZ, 85719, USA
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Laura K. Meredith
6Biosphere 2, University of Arizona, 32540 S. Biosphere Rd., Oracle, AZ, 85739, USA
8School of Natural Resources and the Environment, University of Arizona, Tucson, AZ, USA
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Christiane Werner
1Ecosystem Physiology, Albert-Ludwigs-University of Freiburg, Georges-Köhler-Allee 053/054, 79110 Freiburg, Germany
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Abstract

Daytime respiration in leaves is an integral component of plant metabolism, with CO2 produced as a byproduct during the synthesis of many secondary metabolites, including many common volatile organic compounds (VOCs). It remains unclear how the carbon fluxes associated with daytime respiration and VOC emission vary among mature trees, and how they are influenced by drought. We used position-specific 13C-pyruvate labeling to investigate CO2 and VOC fluxes from the leaves of four tropical species before and during an artificially imposed drought in an enclosed rainforest. Although daytime respiration was always dominated by non-mitochondrial processes, the relative contribution of CO2 from the tricarboxylic acid cycle increased under drought, likely due to osmolyte production. In the legume tree Clitoria fairchildiana, our data indicate that intermediates from the mevalonic acid pathway are used to produce the volatile monoterpene trans-β-ocimene, but not isoprene. This suggests that geranyl pyrophosphate is the more important intermediate for crosstalk between cytosolic and plastidic isoprenoid synthesis, not isopentenyl pyrophosphate. Crosstalk declined with drought, and although trans-β-ocimene emissions increased, they were primarily sourced from storage and not de novo synthesis. We found highly species-specific dynamics in carbon allocation into different metabolic processes including daytime respiration and VOC synthesis.

Highlight Intracellular carbon allocation into daytime respiration and VOCs is species-specific and changes with drought. Isoprenoid synthesis in the plastid can be fed with glyceraldehyde-3-phosphate and geranyl pyrophosphate from the cytosol.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Email addresses: n.ladd{at}unibas.ch, erik.daber{at}cep.uni-freiburg.de, i.bamberger{at}mail.de, angelika.kuebert{at}mail.cep.uni-freiburg.de, juergen.kreuzwieser{at}ctp.uni-freiburg.de. gepurse25{at}ceh.ac.uk, Johannes.Ingrisch{at}uibk.ac.at, jdeleeuw{at}arizona.edu, jvanhare{at}arizona.edu, laurameredith{at}arizona.edu, c.werner{at}cep.uni-freiburg.de

  • Abbreviations

    acetyl-CoA
    acetyl coenzyme A
    B2WALD
    Biosphere 2 Water Atmosphere and Life Dynamics
    DMAPP
    dimethylallyl pyrophosphate
    FEP
    fluorinated ethylene propylene
    GA-3-P
    glyceraldehyde-3-phosphate
    GABA
    γ-aminobutyric acid
    GC-MS-C
    Gas Chromatography – Mass Spectrometry – Combustion interface
    GPP
    geranyl pyrophosphate
    ID
    inner diameter
    IPP
    isopentenyl pyrophosphate
    IRIS
    isotope ratio infrared spectrometer
    IRMS
    isotope ratio mass spectrometer
    MVA
    mevalonic acid
    MEP
    methylerythritol 4-phosphate
    MSD
    mass-selective detector
    PAR
    photosynthetic active radiation
    PFA
    perfluoroalkoxy alkane
    PTR-TOF-MS
    proton transfer reaction – time of flight mass spectrometer
    TCA
    tricarboxylic acid
    VPDB
    Vienna Pee Dee Belemnite
    VOCs
    volatile organic compounds
  • Copyright 
    The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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    Leaf-level metabolic changes in response to drought affect daytime CO2 emission and isoprenoid synthesis
    S. Nemiah Ladd, L. Erik Daber, Ines Bamberger, Angelika Kübert, Jürgen Kreuzwieser, Gemma Purser, Johannes Ingrisch, Jason Deleeuw, Joost van Haren, Laura K. Meredith, Christiane Werner
    bioRxiv 2022.04.29.490001; doi: https://doi.org/10.1101/2022.04.29.490001
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    Leaf-level metabolic changes in response to drought affect daytime CO2 emission and isoprenoid synthesis
    S. Nemiah Ladd, L. Erik Daber, Ines Bamberger, Angelika Kübert, Jürgen Kreuzwieser, Gemma Purser, Johannes Ingrisch, Jason Deleeuw, Joost van Haren, Laura K. Meredith, Christiane Werner
    bioRxiv 2022.04.29.490001; doi: https://doi.org/10.1101/2022.04.29.490001

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