[Source: Proceedings of the National Academy of Sciences of the United States of America, full page: (LINK). Abstract, edited.]
Detecting long-term metabolic shifts using isotopomers: CO2-driven suppression of photorespiration in C3 plants over the 20th century [ ]
Ina Ehlers a,1, Angela Augusti a,1,2, Tatiana R. Betson a, Mats B. Nilsson b, John D. Marshall b,c, and Jürgen Schleucher a,3
Author Affiliations: aDepartment of Medical Biochemistry & Biophysics, Umeå University, 901 87 Umea, Sweden; bDepartment of Forest Ecology and Management, Swedish University of Agricultural Sciences, 901 83 Umea, Sweden; cDepartment of Forest, Rangeland, and Fire Sciences, University of Idaho, Moscow, ID 83844-1133
Edited by Katherine H. Freeman, Pennsylvania State University, University Park, PA, and approved November 9, 2015 (received for review July 26, 2015)
Decadal-scale metabolic responses of plants to environmental changes, including the magnitude of the “CO2 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 C3 plants toward photosynthesis, driven by increasing atmospheric CO2 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 CO2 emissions, mitigating the rise of atmospheric CO2. However, terrestrial net primary production is highly sensitive to atmospheric CO2 levels and associated climatic changes. In C3 plants, which dominate terrestrial vegetation, net photosynthesis depends on the ratio between photorespiration and gross photosynthesis. This metabolic flux ratio depends strongly on CO2 levels, but changes in this ratio over the past CO2 rise have not been analyzed experimentally. Combining CO2 manipulation experiments and deuterium NMR, we first establish that the intramolecular deuterium distribution (deuterium isotopomers) of photosynthetic C3 glucose contains a signal of the photorespiration/photosynthesis ratio. By tracing this isotopomer signal in herbarium samples of natural C3 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 CO2 increase between ∼1900 and 2013. No difference was detected in the isotopomer trends between beet sugar samples covering the 20th century and CO2 manipulation experiments, suggesting that photosynthetic metabolism in sugar beet has not acclimated to increasing CO2 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 “CO2 fertilization” effect over decades, thus addressing a major uncertainty in Earth system models.
isotopomer – acclimation – deuterium – CO2 fertilization – atmospheric change
1I.E. and A.A. contributed equally to this work.
2Present address: Institute of Agro-environmental and Forest Biology, National Council of Research, 05010 Porano (TR), Italy.
3To whom correspondence should be addressed. Email: email@example.com.
Author contributions: I.E., A.A., and J.S. designed research; I.E., A.A., and J.S. performed research; T.R.B. and M.B.N. contributed new reagents/analytic tools; I.E., A.A., T.R.B., M.B.N., J.D.M., and J.S. analyzed data; and I.E., A.A., T.R.B., M.B.N., J.D.M., and J.S. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1504493112/-/DCSupplemental.
Freely available online through the PNAS open access option. http://www.pnas.org/preview_site/misc/userlicense.xhtml
Keywords: Research; Abstracts; Climate Change; Biodiversity.