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.
Highlights
Our understanding on emissions of biogenic volatile organic compounds (BVOCs), including thousands of different compounds from different chemical classes, has improved substantially during the last decades, partially due to new developments in measuring techniques
The PTR-TOF-MS revealed a broad spectrum of over 60 different masses emitted by H. halimifolium branches at a considerable amount under controlled conditions (S2 Table); a selection of the most abundant compounds was identified and listed in Table 1 and a characteristic TOF spectrum is shown as supporting information (S4 Fig)
Each detected m/z was assigned to specific BVOCs, which were classified as terpenoids, benzenoids (1.3-cyclopentadiene, benzene, toluene, o-xylene, cresol, trimethylbenzene, ethylphenol), oxygenated BVOCs and green leaf volatiles
Summary
Our understanding on emissions of biogenic volatile organic compounds (BVOCs), including thousands of different compounds from different chemical classes, has improved substantially during the last decades, partially due to new developments in measuring techniques. Biosynthesis of monoterpenes and isoprene, the latter being the most important volatile emitted by vegetation, takes place in the chloroplasts and uses Calvin cycle intermediates (pyruvate and glyceraldehyde-3-phosphate) as direct precursors. Production of these compounds is tightly linked to photosynthetic CO2 fixation [5,6]. There are at least four main processes determining the CO2 exchange in plants, i.e. CO2 fixation during photosynthesis, photorespiration, CO2 generating processes in metabolic pathways and mitochondrial respiration mainly taking place in the tricarboxylic acid (TCA)-cycle. Tcherkez et al (2017) point out that a comprehensive analysis of metabolic fluxes, including partitioning at branching points, is still lacking and that the specific origin of carbon atoms fuelling day-respiration is still uncertain
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