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Contribution of various carbon sources toward isoprene biosynthesis in poplar leaves mediated by altered atmospheric CO2 concentrations.

Trowbridge AM, Asensio D, Eller AS, Way DA, Wilkinson MJ, Schnitzler JP, Jackson RB, Monson RK - PLoS ONE (2012)

Bottom Line: This is the first study to explicitly consider the effects of altered atmospheric CO(2) concentration on carbon partitioning to isoprene biosynthesis.These results suggest that under reduced atmospheric CO(2) availability, more carbon from stored/older carbon sources is involved in isoprene biosynthesis, and this carbon most likely enters the isoprene biosynthesis pathway through the pyruvate substrate.We offer direct evidence that extra-chloroplastic rather than chloroplastic carbon sources are mobilized to increase the availability of pyruvate required to up-regulate the isoprene biosynthesis pathway when trees are grown under sub-ambient CO(2).

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, Colorado, United States of America. amy.m.trowbridge@gmail.com

ABSTRACT
Biogenically released isoprene plays important roles in both tropospheric photochemistry and plant metabolism. We performed a (13)CO(2)-labeling study using proton-transfer-reaction mass spectrometry (PTR-MS) to examine the kinetics of recently assimilated photosynthate into isoprene emitted from poplar (Populus × canescens) trees grown and measured at different atmospheric CO(2) concentrations. This is the first study to explicitly consider the effects of altered atmospheric CO(2) concentration on carbon partitioning to isoprene biosynthesis. We studied changes in the proportion of labeled carbon as a function of time in two mass fragments, M41(+), which represents, in part, substrate derived from pyruvate, and M69(+), which represents the whole unlabeled isoprene molecule. We observed a trend of slower (13)C incorporation into isoprene carbon derived from pyruvate, consistent with the previously hypothesized origin of chloroplastic pyruvate from cytosolic phosphenolpyruvate (PEP). Trees grown under sub-ambient CO(2) (190 ppmv) had rates of isoprene emission and rates of labeling of M41(+) and M69(+) that were nearly twice those observed in trees grown under elevated CO(2) (590 ppmv). However, they also demonstrated the lowest proportion of completely labeled isoprene molecules. These results suggest that under reduced atmospheric CO(2) availability, more carbon from stored/older carbon sources is involved in isoprene biosynthesis, and this carbon most likely enters the isoprene biosynthesis pathway through the pyruvate substrate. We offer direct evidence that extra-chloroplastic rather than chloroplastic carbon sources are mobilized to increase the availability of pyruvate required to up-regulate the isoprene biosynthesis pathway when trees are grown under sub-ambient CO(2).

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Rates of 13C transference between isotopomers as a function of CO2 concentrations.Mean rates of loss (mean ± SEM) of the labeled isotopomers in units of molecules/cycle (cycle = detection every 30 seconds with a PTR-MS dwell time of 2 seconds) for both the parent molecule M69+ and its fragment M41+ (inset graph) among individuals grown at three different CO2 concentrations (sub-ambient = 190 ppm (black triangles; dashed line); ambient = 400 ppm (dark gray circles; dashed line); elevated = 590 ppm (light gray squares; solid line)). In general, the photosynthetic pools of the leaves grown in sub-ambient CO2 were labeled faster than leaves grown at ambient or elevated CO2.
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pone-0032387-g004: Rates of 13C transference between isotopomers as a function of CO2 concentrations.Mean rates of loss (mean ± SEM) of the labeled isotopomers in units of molecules/cycle (cycle = detection every 30 seconds with a PTR-MS dwell time of 2 seconds) for both the parent molecule M69+ and its fragment M41+ (inset graph) among individuals grown at three different CO2 concentrations (sub-ambient = 190 ppm (black triangles; dashed line); ambient = 400 ppm (dark gray circles; dashed line); elevated = 590 ppm (light gray squares; solid line)). In general, the photosynthetic pools of the leaves grown in sub-ambient CO2 were labeled faster than leaves grown at ambient or elevated CO2.

Mentions: Because on-line PTR-MS can distinguish individually labeled isoprene species during 13C labeling, we measured the rates at which each mass variant appeared and reached steady state. This, in turn, allowed us to estimate the rates of 13C transferred from 13C-labeled photosynthate into isoprene as the rate of mass loss from the M69+, M70+, M71+, M72+ and M73+ signals. The rate of transfer of 13C into isoprene was ∼2 times faster for the first four masses in the leaves of poplars grown and measured under sub-ambient CO2 conditions, compared to those grown and measured under ambient and elevated CO2 conditions (Fig. 4). The rate of transfer showed the same trend in the loss of M73+, compared to the other masses, but the trend was not statistically significant. Similarly, the rate of mass loss for M41+, M42+ and M43+ was approximately twice as fast for the leaves grown under sub-ambient CO2, compared to the other two treatments (Fig. 4, inset). Trees grown under sub-ambient CO2 exhibited net CO2 assimilation rates ∼2 times lower than trees grown under elevated CO2 as shown (Fig. 1A), despite having higher stomatal conductance rates (Fig. 1C). Thus, recently assimilated 13CO2 was transferred at a greater rate into isoprene in leaves grown under sub-ambient CO2 compared to leaves grown under elevated or ambient CO2, despite having lower net CO2 assimilation rates.


Contribution of various carbon sources toward isoprene biosynthesis in poplar leaves mediated by altered atmospheric CO2 concentrations.

Trowbridge AM, Asensio D, Eller AS, Way DA, Wilkinson MJ, Schnitzler JP, Jackson RB, Monson RK - PLoS ONE (2012)

Rates of 13C transference between isotopomers as a function of CO2 concentrations.Mean rates of loss (mean ± SEM) of the labeled isotopomers in units of molecules/cycle (cycle = detection every 30 seconds with a PTR-MS dwell time of 2 seconds) for both the parent molecule M69+ and its fragment M41+ (inset graph) among individuals grown at three different CO2 concentrations (sub-ambient = 190 ppm (black triangles; dashed line); ambient = 400 ppm (dark gray circles; dashed line); elevated = 590 ppm (light gray squares; solid line)). In general, the photosynthetic pools of the leaves grown in sub-ambient CO2 were labeled faster than leaves grown at ambient or elevated CO2.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3285681&req=5

pone-0032387-g004: Rates of 13C transference between isotopomers as a function of CO2 concentrations.Mean rates of loss (mean ± SEM) of the labeled isotopomers in units of molecules/cycle (cycle = detection every 30 seconds with a PTR-MS dwell time of 2 seconds) for both the parent molecule M69+ and its fragment M41+ (inset graph) among individuals grown at three different CO2 concentrations (sub-ambient = 190 ppm (black triangles; dashed line); ambient = 400 ppm (dark gray circles; dashed line); elevated = 590 ppm (light gray squares; solid line)). In general, the photosynthetic pools of the leaves grown in sub-ambient CO2 were labeled faster than leaves grown at ambient or elevated CO2.
Mentions: Because on-line PTR-MS can distinguish individually labeled isoprene species during 13C labeling, we measured the rates at which each mass variant appeared and reached steady state. This, in turn, allowed us to estimate the rates of 13C transferred from 13C-labeled photosynthate into isoprene as the rate of mass loss from the M69+, M70+, M71+, M72+ and M73+ signals. The rate of transfer of 13C into isoprene was ∼2 times faster for the first four masses in the leaves of poplars grown and measured under sub-ambient CO2 conditions, compared to those grown and measured under ambient and elevated CO2 conditions (Fig. 4). The rate of transfer showed the same trend in the loss of M73+, compared to the other masses, but the trend was not statistically significant. Similarly, the rate of mass loss for M41+, M42+ and M43+ was approximately twice as fast for the leaves grown under sub-ambient CO2, compared to the other two treatments (Fig. 4, inset). Trees grown under sub-ambient CO2 exhibited net CO2 assimilation rates ∼2 times lower than trees grown under elevated CO2 as shown (Fig. 1A), despite having higher stomatal conductance rates (Fig. 1C). Thus, recently assimilated 13CO2 was transferred at a greater rate into isoprene in leaves grown under sub-ambient CO2 compared to leaves grown under elevated or ambient CO2, despite having lower net CO2 assimilation rates.

Bottom Line: This is the first study to explicitly consider the effects of altered atmospheric CO(2) concentration on carbon partitioning to isoprene biosynthesis.These results suggest that under reduced atmospheric CO(2) availability, more carbon from stored/older carbon sources is involved in isoprene biosynthesis, and this carbon most likely enters the isoprene biosynthesis pathway through the pyruvate substrate.We offer direct evidence that extra-chloroplastic rather than chloroplastic carbon sources are mobilized to increase the availability of pyruvate required to up-regulate the isoprene biosynthesis pathway when trees are grown under sub-ambient CO(2).

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, Colorado, United States of America. amy.m.trowbridge@gmail.com

ABSTRACT
Biogenically released isoprene plays important roles in both tropospheric photochemistry and plant metabolism. We performed a (13)CO(2)-labeling study using proton-transfer-reaction mass spectrometry (PTR-MS) to examine the kinetics of recently assimilated photosynthate into isoprene emitted from poplar (Populus × canescens) trees grown and measured at different atmospheric CO(2) concentrations. This is the first study to explicitly consider the effects of altered atmospheric CO(2) concentration on carbon partitioning to isoprene biosynthesis. We studied changes in the proportion of labeled carbon as a function of time in two mass fragments, M41(+), which represents, in part, substrate derived from pyruvate, and M69(+), which represents the whole unlabeled isoprene molecule. We observed a trend of slower (13)C incorporation into isoprene carbon derived from pyruvate, consistent with the previously hypothesized origin of chloroplastic pyruvate from cytosolic phosphenolpyruvate (PEP). Trees grown under sub-ambient CO(2) (190 ppmv) had rates of isoprene emission and rates of labeling of M41(+) and M69(+) that were nearly twice those observed in trees grown under elevated CO(2) (590 ppmv). However, they also demonstrated the lowest proportion of completely labeled isoprene molecules. These results suggest that under reduced atmospheric CO(2) availability, more carbon from stored/older carbon sources is involved in isoprene biosynthesis, and this carbon most likely enters the isoprene biosynthesis pathway through the pyruvate substrate. We offer direct evidence that extra-chloroplastic rather than chloroplastic carbon sources are mobilized to increase the availability of pyruvate required to up-regulate the isoprene biosynthesis pathway when trees are grown under sub-ambient CO(2).

Show MeSH
Related in: MedlinePlus