Abstract
Total protein and nitrogen concentrations in plants generally decline under elevated CO2 atmospheres1,2. Explanations for this decline include that plants under elevated CO2 grow larger, diluting the protein within their tissues3,4; that carbohydrates accumulate within leaves, downregulating the amount of the most prevalent protein Rubisco2; that carbon enrichment of the rhizosphere leads to progressively greater limitations of the nitrogen available to plants4; and that elevated CO2 directly inhibits plant nitrogen metabolism, especially the assimilation of nitrate into proteins in leaves of C3 plants5. Recently, several meta-analyses have indicated that CO2 inhibition of nitrate assimilation is the explanation most consistent with observations6,7,8. Here, we present the first direct field test of this explanation. We analysed wheat (Triticum aestivum L.) grown under elevated and ambient CO2 concentrations in the free-air CO2 enrichment experiment at Maricopa, Arizona. In leaf tissue, the ratio of nitrate to total nitrogen concentration and the stable isotope ratios of organic nitrogen and free nitrate showed that nitrate assimilation was slower under elevated than ambient CO2. These findings imply that food quality will suffer under the CO2 levels anticipated during this century unless more sophisticated approaches to nitrogen fertilization are employed.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Cotrufo, M. F., Ineson, P. & Scott, A. Elevated CO2 reduces the nitrogen concentration of plant tissues. Glob. Change Biol. 4, 43–54 (1998).
Long, S. P., Ainsworth, E. A., Rogers, A. & Ort, D. R. Rising atmospheric carbon dioxide: Plants face the future. Annu. Rev. Plant Biol. 55, 591–628 (2004).
Ellsworth, D. S. et al. Photosynthesis, carboxylation and leaf nitrogen responses of 16 species to elevated pCO2 across four free-air CO2 enrichment experiments in forest, grassland and desert. Glob. Change Biol. 10, 2121–2138 (2004).
Reich, P. B. et al. Nitrogen limitation constrains sustainability of ecosystem response to CO2 . Nature 440, 922–925 (2006).
Bloom, A. J. et al. CO2 enrichment inhibits shoot nitrate assimilation in C3 but not C4 plants and slows growth under nitrate in C3 plants. Ecology 93, 355–367 (2012).
Cheng, L. et al. Arbuscular mycorrhizal fungi increase organic carbon decomposition under elevated CO2 . Science 337, 1084–1087 (2012).
Pleijel, H. & Uddling, J. Yield vs quality trade-offs for wheat in response to carbon dioxide and ozone. Glob. Change Biol. 18, 596–605 (2012).
Myers, S. S. et al. Rising CO2 threatens food quality. Nature (in the press; 2014)
Rachmilevitch, S., Cousins, A. B. & Bloom, A. J. Nitrate assimilation in plant shoots depends on photorespiration. Proc. Natl Acad. Sci. USA 101, 11506–11510 (2004).
Bloom, A. J., Burger, M., Asensio, J. S. R. & Cousins, A. B. Carbon dioxide enrichment inhibits nitrate assimilation in wheat and Arabidopsis. Science 328, 899–903 (2010).
Lekshmy, S., Jain, V., Khetarpal, S. & Pandey, R. Inhibition of nitrate uptake and assimilation in wheat seedlings grown under elevated CO2 . Indian J. Plant Physiol. 1–7 (2013).
Bloom, A. J., Smart, D. R., Nguyen, D. T. & Searles, P. S. Nitrogen assimilation and growth of wheat under elevated carbon dioxide. Proc. Natl Acad. Sci. USA 99, 1730–1735 (2002).
Matt, P. et al. Elevated carbon dioxide increases nitrate uptake and nitrate reductase activity when tobacco is growing on nitrate, but increases ammonium uptake and inhibits nitrate reductase activity when tobacco is growing on ammonium nitrate. Plant Cell Environ. 24, 1119–1137 (2001).
Jamieson, P. D. et al. Modelling CO2 effects on wheat with varying nitrogen supplies. Agr. Ecosyst. Environ. 82, 27–37 (2000).
Sinclair, T. R. et al. Leaf nitrogen concentration of wheat subjected to elevated (CO2 and either water or N deficits. Agr. Ecosyst. Environ. 79, 53–60 (2000).
Kimball, B. A. et al. Elevated CO2, drought and soil nitrogen effects on wheat grain quality. New Phytol. 150, 295–303 (2001).
Prior, S. A. et al. Free-air carbon dioxide enrichment of wheat: Soil carbon and nitrogen dynamics. J. Environ. Qual. 26, 1161–1166 (1997).
Harborne, A. Phytochemical Methods: A Guide to Modern Techniques of Plant Analysis (Springer, 1998).
Sigman, D. M. et al. A bacterial method for the nitrogen isotopic analysis of nitrate in seawater and freshwater. Anal. Chem. 73, 4145–4153 (2001).
Tcherkez, G. & Farquhar, G. D. Isotopic fractionation by plant nitrate reductase, twenty years later. Funct. Plant Biol. 33, 531–537 (2006).
Kruse, J. et al. Elevated pCO2 favours nitrate reduction in the roots of wild-type tobacco (Nicotiana tabacum cv. Gat.) and significantly alters N-metabolism in transformants lacking functional nitrate reductase in the roots. J. Exp. Bot. 53, 2351–2367 (2002).
Backhausen, J. E. et al. Transgenic potato plants with altered expression levels of chloroplast NADP-malate dehydrogenase: interactions between photosynthetic electron transport and malate metabolism in leaves and in isolated intact chloroplasts. Planta 207, 105–114 (1998).
Igamberdiev, A. U., Bykova, N. V., Lea, P. J. & Gardestrom, P. The role of photorespiration in redox and energy balance of photosynthetic plant cells: A study with a barley mutant deficient in glycine decarboxylase. Physiol. Plant. 111, 427–438 (2001).
Robinson, J. M. in Models in Plant Physiology and Biochemistry 1 (eds Newman, D. W. & Stuart, K. G.) 25–35 (CRC Press, 1987).
Quesada, A., Gomez-Garcia, I. & Fernandez, E. Involvement of chloroplast and mitochondria redox valves in nitrate assimilation. Trends Plant Sci. 5, 463–464 (2000).
Knaff, D. B. in Oxygenic Photosynthesis: The Light Reactions 4 (eds Ort, D. R. & Yocum, C. F.) 333–361 (Advances in Photosynthesis, (Kluwer Academic, 1996).
Backhausen, J. E., Kitzmann, C., Horton, P. & Scheibe, R. Electron acceptors in isolated intact spinach chloroplasts act hierarchically to prevent over-reduction and competition for electrons. Photosynth. Res. 64, 1–13 (2000).
Adamsen, F. J. et al. Temporal changes in soil and biomass nitrogen for irrigated wheat grown under free-air carbon dioxide enrichment (FACE). Agron. J. 97, 160–168 (2005).
Erbs, M. et al. Effects of free-air CO2 enrichment and nitrogen supply on grain quality parameters and elemental composition of wheat and barley grown in a crop rotation. Agr. Ecosyst. Environ. 136, 59–68 (2010).
Manderscheid, R., Bender, J., Jäger, H-J. & Weigel, H. J. Effects of season long CO2 enrichment on cereals II Nutrient concentrations and grain quality. Agr. Ecosyst. Environ. 54, 175–185 (1995).
FAOSTAT Food Supply, Crops Primary Equivalent, http://faostat3.fao.org/faostat-gateway/go/to/download/C/CC/E (2013)
Pinter, P. J. Jr et al. Annual Research Report 71–74 (USDA Water Conservation Laboratory, 1997).
Ko, J. et al. Simulation of free air CO2 enriched wheat growth and interactions with water, nitrogen, and temperature. Agric. Forest Meteorol. 150, 1331–1346 (2010).
Nunes–Nesi, A., Fernie, A. R. & Stitt, M. Metabolic and signaling aspects underpinning the regulation of plant carbon nitrogen interactions. Mol. Plant 3, 973–996 (2010).
Hunsaker, D. J. et al. CO2 enrichment and soil nitrogen effects on wheat evapotranspiration and water use efficiency. Agric. Forest Meteorol. 104, 85–105 (2000).
Doane, T. A. & Horwath, W. R. Spectrophotometric determination of nitrate with a single reagent. Anal. Lett. 36, 2713–2722 (2003).
Acknowledgements
This work was supported by NSF IOS-08-18435 and the National Research Initiative Competitive Grant no. 2008-35100-04459 from the USDA National Institute of Food and Agriculture. We thank A. Torbert and S. Prior, USDA–ARS National Soil Dynamics Laboratory, Auburn, Alabama for sharing unpublished data from their Arizona FACE soil analyses.
Author information
Authors and Affiliations
Contributions
All authors contributed to the data set, discussed the results and commented on the manuscript. A.J.B. and M.B. designed the study. M.B. conducted the chemical analyses. A.J.B. carried out the statistical analysis and wrote the paper.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Rights and permissions
About this article
Cite this article
J. Bloom, A., Burger, M., A. Kimball, B. et al. Nitrate assimilation is inhibited by elevated CO2 in field-grown wheat. Nature Clim Change 4, 477–480 (2014). https://doi.org/10.1038/nclimate2183
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nclimate2183
This article is cited by
-
Combinatorial impacts of elevated CO2 and temperature affect growth, development, and fruit yield in Capsicum chinense Jacq
Physiology and Molecular Biology of Plants (2023)
-
Effects of combined abiotic stresses on nutrient content of European wheat and implications for nutritional security under climate change
Scientific Reports (2022)
-
Elevated CO2 alters tissue balance of nitrogen metabolism and downregulates nitrogen assimilation and signalling gene expression in wheat seedlings receiving high nitrate supply
Protoplasma (2021)
-
Nitrogen sources and CO2 concentration synergistically affect the growth and metabolism of tobacco plants
Photosynthesis Research (2020)
-
Diverse role of γ-aminobutyric acid in dynamic plant cell responses
Plant Cell Reports (2019)