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Biogenic volatile organic compound and respiratory CO2 emissions after 13C-labeling: online tracing of C translocation dynamics in poplar plants.

Ghirardo A, Gutknecht J, Zimmer I, Brüggemann N, Schnitzler JP - PLoS ONE (2011)

Bottom Line: The daily C loss as BVOC ranged between 1.6% in mature leaves and 7.0% in young leaves.Non-isoprene BVOC accounted under light conditions for half of the BVOC C loss in young leaves and one-third in mature leaves.We quantified the plants' C loss as respiratory CO(2) and BVOC emissions, allowing in tandem with metabolic analysis to deepen our understanding of ecosystem C flux.

View Article: PubMed Central - PubMed

Affiliation: Karlsruhe Institute of Technology, Institute for Meteorology and Climate Research, Garmisch-Partenkirchen, Germany.

ABSTRACT

Background: Globally plants are the primary sink of atmospheric CO(2), but are also the major contributor of a large spectrum of atmospheric reactive hydrocarbons such as terpenes (e.g. isoprene) and other biogenic volatile organic compounds (BVOC). The prediction of plant carbon (C) uptake and atmospheric oxidation capacity are crucial to define the trajectory and consequences of global environmental changes. To achieve this, the biosynthesis of BVOC and the dynamics of C allocation and translocation in both plants and ecosystems are important.

Methodology: We combined tunable diode laser absorption spectrometry (TDLAS) and proton transfer reaction mass spectrometry (PTR-MS) for studying isoprene biosynthesis and following C fluxes within grey poplar (Populus x canescens) saplings. This was achieved by feeding either (13)CO(2) to leaves or (13)C-glucose to shoots via xylem uptake. The translocation of (13)CO(2) from the source to other plant parts could be traced by (13)C-labeled isoprene and respiratory (13)CO(2) emission.

Principal finding: In intact plants, assimilated (13)CO(2) was rapidly translocated via the phloem to the roots within 1 hour, with an average phloem transport velocity of 20.3±2.5 cm h(-1). (13)C label was stored in the roots and partially reallocated to the plants' apical part one day after labeling, particularly in the absence of photosynthesis. The daily C loss as BVOC ranged between 1.6% in mature leaves and 7.0% in young leaves. Non-isoprene BVOC accounted under light conditions for half of the BVOC C loss in young leaves and one-third in mature leaves. The C loss as isoprene originated mainly (76-78%) from recently fixed CO(2), to a minor extent from xylem-transported sugars (7-11%) and from photosynthetic intermediates with slower turnover rates (8-11%).

Conclusion: We quantified the plants' C loss as respiratory CO(2) and BVOC emissions, allowing in tandem with metabolic analysis to deepen our understanding of ecosystem C flux.

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Isotopic composition of isoprene molecules and the corresponding 13C-incorporation during 13C-labeling of intact poplar plants and detached shoots.Pattern of isoprene isotopologues (m74, light blue; m73, magenta; m72, dark blue; m71, yellow; m70, green; m69, white) and 13C-incorporation (open circles) in (A) intact plants, (B) shoots labeled with 13CO2, and (C) shoots labeled with 13Glc. Panels (D), (E), and (F) show the isotopic composition of isoprene emitted by the same plants during the period with CO2-free air. Details of the experimental phases can be found in the Materials and Methods section. Data represent the mean of 3 experiments ± s.e.
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pone-0017393-g008: Isotopic composition of isoprene molecules and the corresponding 13C-incorporation during 13C-labeling of intact poplar plants and detached shoots.Pattern of isoprene isotopologues (m74, light blue; m73, magenta; m72, dark blue; m71, yellow; m70, green; m69, white) and 13C-incorporation (open circles) in (A) intact plants, (B) shoots labeled with 13CO2, and (C) shoots labeled with 13Glc. Panels (D), (E), and (F) show the isotopic composition of isoprene emitted by the same plants during the period with CO2-free air. Details of the experimental phases can be found in the Materials and Methods section. Data represent the mean of 3 experiments ± s.e.

Mentions: Feeding intact poplar plants and detached shoots with the two main C sources for isoprene biosynthesis resulted in different fractions of 13C-labeled isoprene molecules (Fig. 6, 7). After 1 h of labeling with 13CO2, fumigated leaves of intact plants and detached shoots incorporated 76–78% 13C into isoprene (Fig. 6C, 7B). The remaining 22–24% originated from C sources other than recently fixed atmospheric CO2. Over 8 h of 13CO2-labeling, the 13C incorporation into isoprene molecules increased continuously up to 86.3±0.2% (Fig. 6C), indicating that also alternative C sources became partially 13C-labeled. Isoprene molecules became gradually enriched in m74 (Fig. 8). This indicated that a fraction of one or both precursors of chloroplastic isoprene, pyruvate (PYR) and glyceraldehyde 3-phosphate (GAP) originated from plant/leaf-internal C pools with slow turnover. As an indication of the depletion of unlabeled carbon pools, the isoprene fraction with m71 decreased over the 8 h labeling period from 18±2.3% down to 8.2±0.4%, inversely proportionally to m74, which increased from 54±3.1% to 65±3.1% (Fig. 8). Therefore, we estimate that about 10% of carbon was derived from “older” C not originating from recent 13CO2 fixation. Subjecting the previously 13CO2-labeled leaves to CO2-free atmosphere and darkness led to a significant (P<0.01) increase of isoprene molecules with m70–m73 (containing one to four 13C atoms) (Fig. 8D, E). In contrast, in 13Glc-fed shoots only isoprene molecules containing one or two 13C-atoms (m70 and m71) could be detected (Fig. 8F).


Biogenic volatile organic compound and respiratory CO2 emissions after 13C-labeling: online tracing of C translocation dynamics in poplar plants.

Ghirardo A, Gutknecht J, Zimmer I, Brüggemann N, Schnitzler JP - PLoS ONE (2011)

Isotopic composition of isoprene molecules and the corresponding 13C-incorporation during 13C-labeling of intact poplar plants and detached shoots.Pattern of isoprene isotopologues (m74, light blue; m73, magenta; m72, dark blue; m71, yellow; m70, green; m69, white) and 13C-incorporation (open circles) in (A) intact plants, (B) shoots labeled with 13CO2, and (C) shoots labeled with 13Glc. Panels (D), (E), and (F) show the isotopic composition of isoprene emitted by the same plants during the period with CO2-free air. Details of the experimental phases can be found in the Materials and Methods section. Data represent the mean of 3 experiments ± s.e.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3046154&req=5

pone-0017393-g008: Isotopic composition of isoprene molecules and the corresponding 13C-incorporation during 13C-labeling of intact poplar plants and detached shoots.Pattern of isoprene isotopologues (m74, light blue; m73, magenta; m72, dark blue; m71, yellow; m70, green; m69, white) and 13C-incorporation (open circles) in (A) intact plants, (B) shoots labeled with 13CO2, and (C) shoots labeled with 13Glc. Panels (D), (E), and (F) show the isotopic composition of isoprene emitted by the same plants during the period with CO2-free air. Details of the experimental phases can be found in the Materials and Methods section. Data represent the mean of 3 experiments ± s.e.
Mentions: Feeding intact poplar plants and detached shoots with the two main C sources for isoprene biosynthesis resulted in different fractions of 13C-labeled isoprene molecules (Fig. 6, 7). After 1 h of labeling with 13CO2, fumigated leaves of intact plants and detached shoots incorporated 76–78% 13C into isoprene (Fig. 6C, 7B). The remaining 22–24% originated from C sources other than recently fixed atmospheric CO2. Over 8 h of 13CO2-labeling, the 13C incorporation into isoprene molecules increased continuously up to 86.3±0.2% (Fig. 6C), indicating that also alternative C sources became partially 13C-labeled. Isoprene molecules became gradually enriched in m74 (Fig. 8). This indicated that a fraction of one or both precursors of chloroplastic isoprene, pyruvate (PYR) and glyceraldehyde 3-phosphate (GAP) originated from plant/leaf-internal C pools with slow turnover. As an indication of the depletion of unlabeled carbon pools, the isoprene fraction with m71 decreased over the 8 h labeling period from 18±2.3% down to 8.2±0.4%, inversely proportionally to m74, which increased from 54±3.1% to 65±3.1% (Fig. 8). Therefore, we estimate that about 10% of carbon was derived from “older” C not originating from recent 13CO2 fixation. Subjecting the previously 13CO2-labeled leaves to CO2-free atmosphere and darkness led to a significant (P<0.01) increase of isoprene molecules with m70–m73 (containing one to four 13C atoms) (Fig. 8D, E). In contrast, in 13Glc-fed shoots only isoprene molecules containing one or two 13C-atoms (m70 and m71) could be detected (Fig. 8F).

Bottom Line: The daily C loss as BVOC ranged between 1.6% in mature leaves and 7.0% in young leaves.Non-isoprene BVOC accounted under light conditions for half of the BVOC C loss in young leaves and one-third in mature leaves.We quantified the plants' C loss as respiratory CO(2) and BVOC emissions, allowing in tandem with metabolic analysis to deepen our understanding of ecosystem C flux.

View Article: PubMed Central - PubMed

Affiliation: Karlsruhe Institute of Technology, Institute for Meteorology and Climate Research, Garmisch-Partenkirchen, Germany.

ABSTRACT

Background: Globally plants are the primary sink of atmospheric CO(2), but are also the major contributor of a large spectrum of atmospheric reactive hydrocarbons such as terpenes (e.g. isoprene) and other biogenic volatile organic compounds (BVOC). The prediction of plant carbon (C) uptake and atmospheric oxidation capacity are crucial to define the trajectory and consequences of global environmental changes. To achieve this, the biosynthesis of BVOC and the dynamics of C allocation and translocation in both plants and ecosystems are important.

Methodology: We combined tunable diode laser absorption spectrometry (TDLAS) and proton transfer reaction mass spectrometry (PTR-MS) for studying isoprene biosynthesis and following C fluxes within grey poplar (Populus x canescens) saplings. This was achieved by feeding either (13)CO(2) to leaves or (13)C-glucose to shoots via xylem uptake. The translocation of (13)CO(2) from the source to other plant parts could be traced by (13)C-labeled isoprene and respiratory (13)CO(2) emission.

Principal finding: In intact plants, assimilated (13)CO(2) was rapidly translocated via the phloem to the roots within 1 hour, with an average phloem transport velocity of 20.3±2.5 cm h(-1). (13)C label was stored in the roots and partially reallocated to the plants' apical part one day after labeling, particularly in the absence of photosynthesis. The daily C loss as BVOC ranged between 1.6% in mature leaves and 7.0% in young leaves. Non-isoprene BVOC accounted under light conditions for half of the BVOC C loss in young leaves and one-third in mature leaves. The C loss as isoprene originated mainly (76-78%) from recently fixed CO(2), to a minor extent from xylem-transported sugars (7-11%) and from photosynthetic intermediates with slower turnover rates (8-11%).

Conclusion: We quantified the plants' C loss as respiratory CO(2) and BVOC emissions, allowing in tandem with metabolic analysis to deepen our understanding of ecosystem C flux.

Show MeSH
Related in: MedlinePlus