Detecting long-term metabolic shifts using isotopomers: CO 2 -driven suppression of photorespiration in C 3 plants over the 20th century

Decadal-scale metabolic responses of plants to environmental changes, including the magnitude of the “CO 2 fertilization” effect, are a major knowledge gap in Earth system models, in agricultural models, and for societal adaptation. We introduce intramolecular isotope distributions (isotopomers) as...

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Veröffentlicht in:Proceedings of the National Academy of Sciences - PNAS 2015-12, Vol.112 (51), p.15585-15590
Hauptverfasser: Ehlers, Ina, Augusti, Angela, Betson, Tatiana R., Nilsson, Mats B., Marshall, John D., Schleucher, Jürgen
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Sprache:eng
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Zusammenfassung:Decadal-scale metabolic responses of plants to environmental changes, including the magnitude of the “CO 2 fertilization” effect, are a major knowledge gap in Earth system models, in agricultural models, and for societal adaptation. We introduce intramolecular isotope distributions (isotopomers) as a methodology for detecting shifts in plant carbon metabolism over long times. Trends in a deuterium isotopomer ratio allow quantification of a biogeochemically relevant shift in the metabolism of C 3 plants toward photosynthesis, driven by increasing atmospheric CO 2 since industrialization. Isotopomers strongly increase the information content of isotope archives, and may therefore reveal long-term acclimation or adaptations to environmental changes in general. The metabolic information encoded in isotopomers of plant archives bridges a fundamental gap between experimental plant science and paleoenvironmental studies. Terrestrial vegetation currently absorbs approximately a third of anthropogenic CO 2 emissions, mitigating the rise of atmospheric CO 2 . However, terrestrial net primary production is highly sensitive to atmospheric CO 2 levels and associated climatic changes. In C 3 plants, which dominate terrestrial vegetation, net photosynthesis depends on the ratio between photorespiration and gross photosynthesis. This metabolic flux ratio depends strongly on CO 2 levels, but changes in this ratio over the past CO 2 rise have not been analyzed experimentally. Combining CO 2 manipulation experiments and deuterium NMR, we first establish that the intramolecular deuterium distribution (deuterium isotopomers) of photosynthetic C 3 glucose contains a signal of the photorespiration/photosynthesis ratio. By tracing this isotopomer signal in herbarium samples of natural C 3 vascular plant species, crops, and a Sphagnum moss species, we detect a consistent reduction in the photorespiration/photosynthesis ratio in response to the ∼100-ppm CO 2 increase between ∼1900 and 2013. No difference was detected in the isotopomer trends between beet sugar samples covering the 20th century and CO 2 manipulation experiments, suggesting that photosynthetic metabolism in sugar beet has not acclimated to increasing CO 2 over >100 y. This provides observational evidence that the reduction of the photorespiration/photosynthesis ratio was ca. 25%. The Sphagnum results are consistent with the observed positive correlations between peat accumulation rates and photosynthetic rates over t
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.1504493112