Real-time carbon allocation into biogenic volatile organic compounds (BVOCs) and respiratory carbon dioxide (CO2) traced by PTR-TOF-MS, 13CO2 laser spectroscopy and 13C-pyruvate labelling

PLoS One. 2018 Sep 25;13(9):e0204398. doi: 10.1371/journal.pone.0204398. eCollection 2018.

Abstract

Our understanding of biogenic volatile organic compound (BVOC) emissions improved substantially during the last years. Nevertheless, there are still large uncertainties of processes controlling plant carbon investment into BVOCs, of some biosynthetic pathways and their linkage to CO2 decarboxylation at central metabolic branching points. To shed more light on carbon partitioning during BVOC biosynthesis, we used an innovative approach combining δ13CO2 laser spectroscopy, high-sensitivity proton-transfer-reaction time-of-flight mass spectrometry and a multiple branch enclosure system in combination with position-specific 13C-metabolite labelling. Feeding experiments with position-specific 13C-labelled pyruvate, a central metabolite of BVOC synthesis, enabled online detection of carbon partitioning into 13C-BVOCs and respiratory 13CO2. Measurements of trace gas emissions of the Mediterranean shrub Halimium halimifolium revealed a broad range of emitted BVOCs. In general, [2-13C]-PYR was rapidly incorporated into emitted acetic acid, methyl acetate, toluene, cresol, trimethylbenzene, ethylphenol, monoterpenes and sesquiterpenes, indicating de novo BVOC biosynthesis of these compounds. In contrast, [1-13C]-pyruvate labelling substantially increased 13CO2 emissions in the light indicating C1-decarboxylation. Similar labelling patterns of methyl acetate and acetic acid suggested tightly connected biosynthetic pathways and, furthermore, there were hints of possible biosynthesis of benzenoids via the MEP-pathway. Overall, substantial CO2 emission from metabolic branching points during de novo BVOC biosynthesis indicated that decarboxylation of [1-13C]-pyruvate, as a non-mitochondrial source of CO2, seems to contribute considerably to daytime CO2 release from leaves. Our approach, combining synchronised BVOC and CO2 measurements in combination with position-specific labelling opens the door for real-time analysis tracing metabolic pathways and carbon turnover under different environmental conditions, which may enhance our understanding of regulatory mechanisms in plant carbon metabolism and BVOC biosynthesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Carbon Dioxide / analysis*
  • Carbon Dioxide / chemistry
  • Carbon Isotopes / chemistry*
  • Cell Respiration
  • Cistaceae / chemistry
  • Cistaceae / cytology
  • Isotope Labeling
  • Lasers*
  • Mass Spectrometry*
  • Pyruvic Acid / chemistry*
  • Time Factors
  • Volatile Organic Compounds / analysis*
  • Volatile Organic Compounds / chemistry

Substances

  • Carbon Isotopes
  • Volatile Organic Compounds
  • Carbon Dioxide
  • Pyruvic Acid
  • Carbon-13

Grants and funding

This work was supported by the European Research Council (ERC) Project VOCO2 (647008). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.