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

Abstract

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 the Northern Hemisphere. Our results establish that isotopomers of plant archives contain metabolic information covering centuries. Our data provide direct quantitative information on the "CO 2 fertilization" effect over decades, thus addressing a major uncertainty in Earth system models.A tmospheric CO 2 levels have increased from ∼200 ppm during the last ice age to currently 400 ppm, and they may, according to pessimistic scenarios, exceed 1,000 ppm in the year 2100 (1). Understanding plant responses to increasing CO 2 is currently hampered by two fundamental limitations: First, it is unknown how well manipulation experiments represent responses to the gradual CO 2 increase over decades and centuries. In Free-Air CO 2 Enrichment (FACE) experiments, which most closely mimic natural conditions, increases in [CO 2 ] generally increase plant growth, but this "CO 2 fertilization" effect often declines after a few years of enrichment (2). Such transient responses may be related to the step increases in [CO 2 ] used in the experiments, their limited duration (2), or factors other than CO 2 becoming limiting (3). Second, in response to the [CO 2 ] increase since industrialization, genetic (4) and phenotypic plant responses (5-7) have been observed. Although century-scale changes have been detected in carbon isotopes (δ 13 C) and attributed to [CO 2 ], these responses are tied to differences in intercellular substrate concentrations that reflect several metabolic fluxes and dif...

2H‐fractionations during the biosynthesis of carbohydrates and lipids imprint a metabolic signal on the δ2H values of plant organic compounds

“…We fitted hyperbolic functions (expressing the balance between photosynthetic and post‐photosynthetic effects on Δ 2 H‐ε bio ) enhanced with linear functions (expressing the possible influence of photorespiration; Ehlers et al ., ) into the relationships between the independent variables we manipulated in the two experiments and Δ 2 H‐ε bio :where x is either the light intensity or the p CO 2 values and a to d represent model‐calculated parameters. At the positive end, the photosynthetic processes dominate and the inputs of new assimilates and light‐derived NADPH are at a maximum value and drive Δ 2 H‐ε bio towards negative values.…”

The new face of isotopic NMR at natural abundance

“…In this study, high magnetic fields (>14 T) associated to cryo‐probes made it possible to work with much smaller amounts of material, that is, hundred of milligrams instead of grams. The authors demonstrated that the 2 H intramolecular pattern in glucose depended on the CO 2 level in atmosphere, establishing an indicator of the long‐term increase of CO 2 in plants …”

Elevated atmospheric CO2 negatively impacts photosynthesis through radiative forcing and physiology‐mediated climate feedback

“…Summing ΔGPP FERT , ΔGPP RAD , and ΔGPP VCF gives a global net increase of global GPP, consistent with evidence from the Dole effect from oxygen isotopes of O 2 trapped in ice for preindustrial GPP [ Ciais et al ., ] and current data‐driven estimates [ Beer et al ., ; Zhao et al ., ] and from indirect deuterium isotopomer measurements on plant material [ Ehlers et al ., ]. Both the radiative and eCO 2 ‐VCF have a net negative impact on global GPP, which jointly offsets approximate half of the fertilization‐induced increase of GPP (Figure a).…”